Into the Illusive World: An Exploration of Animals’ Perception [1st ed.] 978-3-030-20201-9;978-3-030-20202-6

Table of contents :
Front Matter ....Pages i-xvi
Front Matter ....Pages 1-1
What’s Mine Is Mine and What’s Yours Is Yours (Paul A. Moore)....Pages 3-15
Front Matter ....Pages 17-17
Eyes as Windows to the Soul (Paul A. Moore)....Pages 19-26
The Pollinator’s Garden (Paul A. Moore)....Pages 27-31
Finding the Way Home (Paul A. Moore)....Pages 33-40
I Can See for Miles and Miles and Miles (Paul A. Moore)....Pages 41-48
Peering into the Darkness (Paul A. Moore)....Pages 49-54
Technicolor Dreamcoats (Paul A. Moore)....Pages 55-61
The Eye as a Window to the World (Paul A. Moore)....Pages 63-64
Front Matter ....Pages 65-65
The Music of Nature (Paul A. Moore)....Pages 67-70
All About the Bass (Paul A. Moore)....Pages 71-78
The Sound of Fear (Paul A. Moore)....Pages 79-84
Sound Beneath the Waves (Paul A. Moore)....Pages 85-93
The Lover’s Voice (Paul A. Moore)....Pages 95-100
The Power of Sound (Paul A. Moore)....Pages 101-102
Front Matter ....Pages 103-103
The Smell of Warm Bread (Paul A. Moore)....Pages 105-112
This Is Not My House (Paul A. Moore)....Pages 113-118
Better Lies Through Chemistry (Paul A. Moore)....Pages 119-124
Can’t We All Just Get Along? (Paul A. Moore)....Pages 125-131
Social Resume (Paul A. Moore)....Pages 133-139
The Emotion of Chemicals (Paul A. Moore)....Pages 141-142
Front Matter ....Pages 143-143
Putting Your Best Foot Forward (Paul A. Moore)....Pages 145-150
The Sweet Taste of Life (Paul A. Moore)....Pages 151-157
More Than a Feeling (Paul A. Moore)....Pages 159-164
At Death’s Door (Paul A. Moore)....Pages 165-171
A Different Chemical View (Paul A. Moore)....Pages 173-179
The Gustatory World (Paul A. Moore)....Pages 181-182
Front Matter ....Pages 183-183
Picking Up Good Vibrations (Paul A. Moore)....Pages 185-191
Coordinating the Team (Paul A. Moore)....Pages 193-199
The Rhythm of the Bass (Paul A. Moore)....Pages 201-206
The Rhythm of the Dance (Paul A. Moore)....Pages 207-212
Tapping into Love (Paul A. Moore)....Pages 213-219
The Sensible Reverberations (Paul A. Moore)....Pages 221-222
Front Matter ....Pages 223-223
The Diverse World (Paul A. Moore)....Pages 225-230
The Pull of Home (Paul A. Moore)....Pages 231-238
Warmth of the Season (Paul A. Moore)....Pages 239-245
I Go to Die, You to Live (Paul A. Moore)....Pages 247-253
A Shocking Discovery (Paul A. Moore)....Pages 255-261
Chasing Ghosts (Paul A. Moore)....Pages 263-269
The Uncharted World (Paul A. Moore)....Pages 271-272
Front Matter ....Pages 273-273
The Illusive World (Paul A. Moore)....Pages 275-281
Back Matter ....Pages 283-292

Citation preview

Paul A. Moore

Into the Illusive World An Exploration of Animals’ Perception

Into the Illusive World

Paul A. Moore

Into the Illusive World An Exploration of Animals’ Perception

Paul A. Moore Department of Biological Sciences Bowling Green State University Bowling Green, OH, USA

ISBN 978-3-030-20201-9    ISBN 978-3-030-20202-6 (eBook) https://doi.org/10.1007/978-3-030-20202-6 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Cover Caption: Illustrated by Alexandra Steele This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

To the past, current, and future students of the Laboratory for Sensory Ecology who have been bold enough to show me different perspectives.

Acknowledgments

I am not entirely sure where or when the original idea for this book started to crystalize in my mind. Countless of conversations at meetings, in bars, field settings, and classrooms planted many seeds that came together to form the ideas presented here. Needless to say, these words are my own, but the thoughts and ideas come from everyone that I have ever spoken to. I will attempt to thank those that played a more direct role in the development of this book. First and foremost, I was lucky enough to be awarded a Fulbright Scholarship to spend my sabbatical in Lund, Sweden. The time afforded me by this scholarship allowed me to create most of the book. Without the generous support from both the Governments from the United States and Sweden, I would never have finished this project. The Swedish Commission is run by a small but incredible group of individuals. I am indebted to Eric Jönsson, Monica Dahlén, and Maria Carle. They made my transition to Sweden painless and my stay a true joy. They organized programs with other Fulbrighters that truly enlightened me. Tack så mycket. While in Lund, the aquatic ecology group strove to engage me at every moment. Whether at the daily fika, crayfish parties, Ph.D. defenses, or during schnapps at holiday parties, this group was exceedingly brilliant and welcoming. The group is led by Christer Brönmark and Lars-Anders Hansson who are the very definition of gentleman scholars. My life is forever enlightened by these two. Along with Johan, Anders, Olaf, Kaj, and Sylvie and the brilliant graduate students, Caroline, Varpu, Jerker, Marja, and Marcus, I found myself surrounded by engaging, funny, and insightful scientists. A special mention to Raphael who braved a week of research/ fun with my lab in the field in Michigan. Back in the states, I must acknowledge the support of my home institution, Bowling Green State University, for the ability to take a sabbatical to write, think, and renew my scientific pursuits. Scientifically, I draw from two main sources of inspiration. The Society for Integrative and Comparative Biology has served as a home for my research and a great sounding board for my ideas and my students’ research. This is a society of people working at all levels of biology across a wide diverse spectrum of animals. None of the details provided in this book would be possible without this scientific society. The second source of inspiration is my yearly sensory ecology course. One vii

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of the main assignments of the course is to design the sensory apparatus of alien animals. Over the years, the students have challenged themselves as well as my knowledge on sensory ecology and have designed outstanding organisms. Some of these are far better than anything that appears in the movies. The students have forced me to really understand the limits of perception and the fundamental concepts on how the senses work. The Laboratory for Sensory Ecology has been alive and present at Bowling Green State University for almost 25 years now. This dedicated group of graduate students and undergraduate students has provided me with entertainment and enlightenment on a daily basis. Apart from my family, this group is my lifeblood, my testing ground, and my joy. They put up with me and have the brutal honesty to tell me that I am full of shit or to let me know when I might be on to something. As with my previous book, several of these members have read and commented on sections of this book. Molly Beattie, Ana Jurcak, Sara Stienecker, Allie Steele, and Becky Thublin have provided insight and editing on parts of this book. Kelly Jackson needs a special thanks. She has read and commented on the entire book. She, more than anyone, has kept me on track. Allie Steele has dedicated herself to make some of these thoughts come alive in her drawings. I am grateful for her time, patience, and creativity. Writing a book takes time. It takes painful hours when nothing is flowing and lost hours when the writing is flowing. This time is borrowed from somewhere, and that somewhere is, in part, from my family. They have graced me with the freedom to write another book and have supported me when I am locked away, pounding on a keyboard. Without them, there is no me. I am not certain what would happen to my mind if I wasn’t given the chance to put these thoughts to paper. Thankfully, Janet Slobodien and Springer Publishing have given me an outlet so that I wouldn’t have to find out. I am grateful for their help and guidance.

Contents

Part I The Sensuous World 1 What’s Mine Is Mine and What’s Yours Is Yours ��������������������������������    3 1.1 The Sensuous World ������������������������������������������������������������������������    6 1.2 The Mind’s Eye��������������������������������������������������������������������������������    9 1.3 The Illusive World����������������������������������������������������������������������������   11 1.4 What Really Is Reality?��������������������������������������������������������������������   14 Part II Vision 2 Eyes as Windows to the Soul ������������������������������������������������������������������   19 2.1 Double Vision�����������������������������������������������������������������������������������   21 2.2 The Science of the Four-Eyed Fish��������������������������������������������������   24 3 The Pollinator’s Garden��������������������������������������������������������������������������   27 3.1 On the Hunt for Nectar ��������������������������������������������������������������������   28 3.2 The Science of the Bee’s Flowery Vision ����������������������������������������   29 4 Finding the Way Home����������������������������������������������������������������������������   33 4.1 You Can Go Back Home Again��������������������������������������������������������   34 4.2 The Science of Seeing the Unseen����������������������������������������������������   36 5 I Can See for Miles and Miles and Miles ����������������������������������������������   41 5.1 I Spy with My Little Eye Something������������������������������������������������   43 5.2 The Science of Precision Talon Strikes��������������������������������������������   45 6 Peering into the Darkness�����������������������������������������������������������������������   49 6.1 Seeing in the Absence of Light ��������������������������������������������������������   50 6.2 The Science of Nighttime Vision������������������������������������������������������   52 7 Technicolor Dreamcoats��������������������������������������������������������������������������   55 7.1 The Different Hues of Aggression����������������������������������������������������   57 7.2 The Science of Multicolor Worlds����������������������������������������������������   60 8 The Eye as a Window to the World��������������������������������������������������������   63 ix

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Part III Audition 9 The Music of Nature��������������������������������������������������������������������������������   67 10 All About the Bass������������������������������������������������������������������������������������   71 10.1 Hearing the Earth Move Under Your Feet��������������������������������������   73 10.2 The Science of the Distant Rumble of Words��������������������������������   75 11 The Sound of Fear������������������������������������������������������������������������������������   79 11.1 The Song of the Flying Tigers��������������������������������������������������������   80 11.2 The Science of Jamming and Diving����������������������������������������������   82 12 Sound Beneath the Waves�����������������������������������������������������������������������   85 12.1 The Keith Moon of the Deep����������������������������������������������������������   88 12.2 The Science of the Fishy Sound������������������������������������������������������   90 13 The Lover’s Voice ������������������������������������������������������������������������������������   95 13.1 Kiss the Girl������������������������������������������������������������������������������������   97 13.2 The Science of Singing Silly Love Songs��������������������������������������   98 14 The Power of Sound��������������������������������������������������������������������������������  101 Part IV Olfaction 15 The Smell of Warm Bread����������������������������������������������������������������������  105 15.1 Long-Distance Relationships����������������������������������������������������������  108 15.2 The Science of Tracing the Call of Love����������������������������������������  110 16 This Is Not My House������������������������������������������������������������������������������  113 16.1 Following the Ribbon of Odor��������������������������������������������������������  115 16.2 The Science of Recognizing Home������������������������������������������������  117 17 Better Lies Through Chemistry��������������������������������������������������������������  119 17.1 When We First Practice to Deceive������������������������������������������������  121 17.2 The Science of Making Chemical Cocktails����������������������������������  123 18 Can’t We All Just Get Along? ����������������������������������������������������������������  125 18.1 The Secret Handshake��������������������������������������������������������������������  128 18.2 The Science of a Coat of Arms ������������������������������������������������������  129 19 Social Resume������������������������������������������������������������������������������������������  133 19.1 Fighting by Molecular Means��������������������������������������������������������  135 19.2 The Science of a Chemical History������������������������������������������������  138 20 The Emotion of Chemicals����������������������������������������������������������������������  141 Part V Gustation 21 Putting Your Best Foot Forward������������������������������������������������������������  145 21.1 The Walk of Life ����������������������������������������������������������������������������  146 21.2 The Science of Tasting with Your Feet�������������������������������������������  148

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22 The Sweet Taste of Life����������������������������������������������������������������������������  151 22.1 Searching the Dark for Food����������������������������������������������������������  154 22.2 The Science of Tasting with Your Body������������������������������������������  155 23 More Than a Feeling��������������������������������������������������������������������������������  159 23.1 A Sucker for Good Food����������������������������������������������������������������  161 23.2 The Science of Tasting with Tentacles��������������������������������������������  163 24 At Death’s Door����������������������������������������������������������������������������������������  165 24.1 A Gut Feeling����������������������������������������������������������������������������������  167 24.2 The Science of Internal Taste����������������������������������������������������������  169 25 A Different Chemical View����������������������������������������������������������������������  173 25.1 Smelling with a Fork����������������������������������������������������������������������  175 25.2 The Science of Tracking with Tongues������������������������������������������  177 26 The Gustatory World������������������������������������������������������������������������������  181 Part VI Tactile 27 Picking Up Good Vibrations ������������������������������������������������������������������  185 27.1 There Came a Tapping��������������������������������������������������������������������  188 27.2 The Science of a Touching Reply ��������������������������������������������������  190 28 Coordinating the Team����������������������������������������������������������������������������  193 28.1 Someone Gently Rapping ��������������������������������������������������������������  196 28.2 The Science of the Excavating Call������������������������������������������������  197 29 The Rhythm of the Bass��������������������������������������������������������������������������  201 29.1 Did Thee Feel the Earth Move?������������������������������������������������������  203 29.2 The Science of Bypassing the Eardrum������������������������������������������  205 30 The Rhythm of the Dance������������������������������������������������������������������������  207 30.1 Shaken, Not Stirred������������������������������������������������������������������������  209 30.2 The Science of Hips Don’t Lie ������������������������������������������������������  210 31 Tapping into Love������������������������������������������������������������������������������������  213 31.1 Going Bananas��������������������������������������������������������������������������������  215 31.2 The Science of the Vibrating Leaves����������������������������������������������  216 32 The Sensible Reverberations������������������������������������������������������������������  221 Part VII Other Senses 33 The Diverse World ����������������������������������������������������������������������������������  225 33.1 Magnetic Fields������������������������������������������������������������������������������  227 33.2 Infrared Energy ������������������������������������������������������������������������������  227 33.3 Electrical Signals����������������������������������������������������������������������������  228 33.4 A Rose by Any Other Name ����������������������������������������������������������  229

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34 The Pull of Home ������������������������������������������������������������������������������������  231 34.1 Guidance by an Invisible Hand������������������������������������������������������  234 34.2 The Science of Animal Magnetism������������������������������������������������  236 35 Warmth of the Season������������������������������������������������������������������������������  239 35.1 In the Heat of the Night������������������������������������������������������������������  241 35.2 The Science of Thermal Vision������������������������������������������������������  243 36 I Go to Die, You to Live���������������������������������������������������������������������������  247 36.1 Finding a Romantic Fire ����������������������������������������������������������������  249 36.2 The Science of Tracking the Heat��������������������������������������������������  251 37 A Shocking Discovery������������������������������������������������������������������������������  255 37.1 An Electric Soul������������������������������������������������������������������������������  257 37.2 The Science of Sensing Electricity ������������������������������������������������  259 38 Chasing Ghosts����������������������������������������������������������������������������������������  263 38.1 Fleeting Curls of Water ������������������������������������������������������������������  265 38.2 The Science of Sensing Wakes ������������������������������������������������������  267 39 The Uncharted World������������������������������������������������������������������������������  271 Part VIII The Illusive World 40 The Illusive World������������������������������������������������������������������������������������  275 40.1 What Is Reality?������������������������������������������������������������������������������  275 40.2 Walk a Mile in Someone’s….Brain?����������������������������������������������  278 40.3 To Be or Not to Be…����������������������������������������������������������������������  279 40.4 One Final Plea��������������������������������������������������������������������������������  280 Further Reading����������������������������������������������������������������������������������������������  283 Index������������������������������������������������������������������������������������������������������������������  289

List of Figures

Fig. 2.1 The Anableps’ eye. The left drawing shows the position of the fish within the water column. The upper right drawing shows the direction of terrestrial light (green arrows) and aquatic light (blue arrows) as they travel through the lens of the fish. The bottom right drawing shows a close up of the lens of the eye....................................................................................22 Fig. 3.1 Flower petals under different light. The upper half of the drawing depicts the color scheme of a flower’s petals under UV vision, while the lower half displays the colors humans would see...........................................................................................31 Fig. 4.1 The inside of an insect eye. Inside the ommatidia of an eye with the hexagonal rods that run perpendicular to each other...........................................................................................39 Fig. 5.1 Human and raptor eyes. The upper diagram is an outline of the human retina and lens, while the lower drawing depicts the elongated lens and retina of the much higher acuity eye of raptors......................................................................................47 Fig. 6.1 Owl tapetum lucidum. Owls have an elongated retina that is lined with a silvery layer (tapetum lucidum) that reflects the light back across the receptor cells increasing their night vision........................................................................................53 Fig. 7.1 The amazing stomatopod eye. In the middle of this drawing of the stomatopod eye is the midband where the highest density of different photopigments are located...............61

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List of Figures

Fig. 9.1 A simple hair cell. The basis of many different sensory systems, the hair cell has kinocilia (the longer hair on the right), and a series of stereocilia beside the kinocilia. The hair cell is often innervated by another nerve cell and has no axon of its own.......................................................................69 Fig. 10.1 The elephant’s ear. A fatty deposit (the yellowish orange organ) vibrates in response to low-frequency sound, and this vibration is transmitted through the bones of the feet to the inner ear..................78 Fig. 11.1 The tymbal organ. Many moths have a thin membrane near their wings that functions as an ear. The membrane is part of the tymbal organ that is sensitive to the high-­frequency calls of bats and generates clicks.......................................................83 Fig. 12.1 The fish’s swim bladder. The swim bladder of the fish is a gas-filled sack that vibrates in response to underwater sound. The bladder is connected to the inner ear of the fish which allows the animal to detect sound waves...........................................91 Fig. 13.1 Horns of the butterflyfish. The group of fish known as the butterflyfish have evolved a diverse and elaborate set of horns at the front end of their swim bladder. The distinctive shape allows each species of fish to produce and hear different sounds..................................................................................99 Fig. 15.1 The moth’s search for a mate. Moth’s track pheromone plumes by switching between a surge flying mode while inside of the odor plume (upper drawing) and casting back and forth while searching for the plume (bottom drawing)...............111 Fig. 16.1 The salmon’s choice. Salmon use the smell of their natal streams to return home to spawn. At each juncture in the river, different sets of odors mix creating a difficult choice for the salmon.........................................................................118 Fig. 17.1 The bolas’ chemical plant. While not a very attractive spider, the back of the bolas spider is its chemical factory where it produces the pheromone mimics to draw male moths to their death............................................................................123 Fig. 18.1 The sentinel’s search. Guard ants will chemically pat down approaching ants with their antennae to ensure that they carry the right chemical mixture that tells the guard they belong in the colony...........................................................................130 Fig. 19.1 The chemical intimidation. During social interactions, crayfish release their stored urine toward their opponent and attempt to convince them to retreat from the fight......................139

List of Figures

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Fig. 21.1 Tasty feet. The house fly has taste receptors embedded in its feet and tastes future meals by simply walking around............149 Fig. 22.1 The body as tongue. The body of the catfish is covered with taste receptors (red dots) which allow them to reconstruct a three-dimensional world of taste..................................157 Fig. 23.1 Tasting with an arm. The octopus tentacle has suckers that are ringed by taste receptor cells (red dots). The outer lumen (infundibular lumen) is the part of the sucker that sticks to surfaces and allows the octopus to taste potential meals...............163 Fig. 24.1 The inside taste. Not all taste buds are external to the body. Many animals have taste buds (green cells) located in the stomach and intestines that help mediate the learning involved in food aversion...................................................................170 Fig. 25.1 The forked tongue and VNO. Many reptiles have a vomeronasal organ that is stimulated by chemicals placed on the receptor surface by the tongue. Snakes quickly flick the tongue to chemically sample their world and then place the tips of the tongue on the VNO.....................................................177 Fig. 27.1 Feeling the waves. Water striders place their long legs on the water’s surface to detect the presence of waves. The movement of the leg and the angles between the joints allow the water strider to sense its world...........................................190 Fig. 28.1 The vibration of the ant. Leaf-cutter ants signal to each other by rapidly vibrating their hind end (the gaster). This motion sense vibrational signals through the soil which other ants detect as a call for help...........................................199 Fig. 29.1 Head banger’s skull. While most mammals have a sloped skull that drops from their forehead to their nose, the mole rat has a flattened skull. The unique shape of the skull is used to both generate powerful vibratory signals and detect incoming vibrations.................................................................206 Fig. 30.1 The shaking signal. Related to the famous waggle dance, the shaking signal is used to maintain the efficiency of workers. A bee that is not active is approached by another bee, grabbed, and shaken...........................................................................211 Fig. 31.1 Communicating across plants. The smaller male wandering tiger spider will communicate to the larger and deadlier female spider his intentions to mate. This love signal is initiated on different parts of a plant, and the signal travels down one leaf, through the trunk, and onto the leaf with the female...........................................................................................217

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Fig. 34.1 The loggerhead’s voyage. Traveling thousands of miles to feed, the loggerhead turtle finds its way home by using the earth’s magnetic field. Small-scale anomalies in the magnetic field, like deformations in nets, allow the turtle to faithfully return to the beach where it was born decades earlier....................................................................................237 Fig. 35.1 Sensing the heat. The pit of pit vipers is a highly sensitive thermal organ. The opening at the outside of the pit serves to focus thermal energy on a membrane at the back of the organ and gives the snake the ability to determine the direction and distance of its warm prey......................244 Fig. 36.1 Sensing a forest fire. The black fire beetle has a specialized organ that appears as a series of raised bumps (left-hand drawing). Slicing one of the bumps in half reveals a layered organ that serves to funnel the energy from heat waves to the tip of a dendrite. The heat causes a small-scale expansion of the layered organ which activates the dendrite..............................252 Fig. 37.1 The ampullae of Lorenzini. The electrically sensitive cells of weakly electric fish are located at the bottom of a tube in the skin of the fish. The cells that line the tube are sealed together which funnels the electrical signal down to the waiting receptor cells.....................................................261 Fig. 38.1 The seal’s whiskers. Many marine mammals have whiskers that are located all around their mouth, cheeks, eyes, and face. These whiskers are sensitive to curling water currents known as wakes. As their prey (fish) swim forward, they create wakes of different sizes depending on which direction the prey are turning. The seals can detect these small differences to hunt down their prey.................................268

Part I

The Sensuous World

The truth is that from birth on we are, to one extent or another, a fairly sensual species. —Jock Sturges

Chapter 1

What’s Mine Is Mine and What’s Yours Is Yours

I step out of the van and straight into a real-world approximation of J.R.R. Tolkien’s Lothlórien, which was the famous Elven forest lying in a woodland valley. I am surrounded by large red and white pine trees. Although the pines are clearly dominating the landscapes, there are occasional low-lying cedar trees interspersed with tall ferns and mosses. The dark greens of the needles are contrasted with the reddish hues of the trunks and the oranges of last year’s fallen needles. Shafts of sunlight penetrate the gaps in branches and provide some light to the forest floor. I pause to inhale deeply. The splendor of nature greets my nose, and I am enveloped with a mix of earthen and pine aromas. The damp forest floors emit a heavy and peaty smell that connects me with the earth. The clean air and pine smells create a perception of pure nature. Finally, I listen. Just beyond my vision is a river. I can make out the familiar but distinctive and pleasing sounds of water rushing over rapids and small waterfalls. The sound is subtle, but because I have been here multiple times, I know the sound. As I walk deeper into this mystical habitat and follow the sound of water, the world around me slowly changes. The abundant pine forest is slowly replaced by cedars and mosses. The ground becomes soggy as I approach the riverbank, and the dull greens of the pine trees are replaced with the brilliant greens of moss and fern. The aromas slowly transition from the earthen smells into an interesting set of odors arising from the river. The smells are hard to describe, but I recognize them as coming from a clear and clean river. The babble of a river has transitioned into a low roar of tumbling water. At the river’s edge, I pause a second time. This river is a braided river. I observe the way that the water winds its way around, over, through, and under small islands. The islands are composed of fallen cedars ground over by moss, cranberry, and grasses. As I survey the stream, I see some 20 different small islands inviting biological exploration. With an immense sense of joy, I step from the bank and begin my trek out to the many islands. As soon as my foot plunges into the knee-deep water, I am hit with intense shock and subtle pain. The river is icy cold (close to 12 °C according to my subsequent © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_1

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measurements with sampling equipment), and my leg begins to throb with the sudden drop in temperature. Having explored this river many times, I was expecting that sensation, but my expectations still don’t adequately prepare me for the shock. My other leg follows the first, and another shock to the system is registered. I remind myself of the advice I provide my students when sampling these rivers: “Once your legs go numb from the cold, it isn’t so bad.” With these words echoing in my mind, I press on with my mission to explore. Midway to the first island, I stop to study the streambed. To the untrained eye, there appears to be nothing of significance here. A few pebbles, some gravel, lots of sand, and a smattering of plants are all that my eye captures. I reach in, grab one of the larger pebbles, and flip it over. With some closer inspection, I can see that this pebble is teaming with life. The first thing I notice is a small insect quickly moving across the bottom surface of the pebble. Despite its quick movement, I identify it as a stonefly. One of the larger aquatic insects, the underwater form of the stonefly, is actually a juvenile form called a nymph. Nymphs will live 1–3 years in the water before emerging as an adult. The stonefly is running in between small stone ovals as it tries to escape my field of view. The stone ovals contain another common aquatic insect called a caddisfly. These organisms are the master architects of the world and build their own homes out of wood, stone, and sand and even weave wonderful webs (technically nets) that would make spiders jealous. These two insects may live their entire aquatic life on a few pebbles if the food is plentiful enough. Although these insects are at the larger end of the aquatic insect spectrum in regard to size, they are quite small compared to the fish, birds, and mammals that inhabit this beautiful stream. Yet, stoneflies and caddis flies are significantly larger than insects such as blackfly and chironomid larvae which, in turn, are much larger than algae and bacteria that live on the numerous pebbles in this part of the stream. The size range of life on this planet is immense if we consider everything from the smallest bacteria to the largest marine mammals. The size of an organism and its perspective of the world around it are so intimately tied together that this singular feature (size) shapes how we, and all of life, perceive the world around us. For example, calling the bit of land that I am walking toward an island is probably a stretch of the word island. These small pieces of land vary in size from tens to hundreds of square meters, some of which are interconnected through fallen cedar trees. My fellow mammals, such as beavers and deer, can easily cross them in seconds. The aquatic insects and crayfish that inhabit these streams would take hours to cross them, and, still, other animals would perceive these islands as entire continents. Thus, the usefulness of the term “island” is entirely dependent upon the perspective applied. From my perspective, these parcels are barely larger than stepping stones. For the smaller insects, these islands are an entire world. Perspective is actually determined by the perception of the organism in question. This wonderful habitat is full of sensory stimuli: some of which I am fully aware of and others pass me by unknowingly. The chill of the cold water on my legs, the smell of cleanliness in the air, the vivid green of the moss-covered rocks and trees, and the babbling sound of the water rushing over rapids are my world right now.

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These sensory experiences are my umwelt. This Germanic word means “the world as it is perceived by an organism” and was introduced into our vernacular by Jakob von Uexkull who studied animal physiology and behavior. von Uexkull needed a term to recognize that our perception of the world is different when compared to other animals. Given that animals have different sensory capabilities, their “view” of the world around them, and their behavioral repertoire, is guided by that perception. In my little Tolkien world, my fellow organisms are actually inhabiting different worlds because they have different umwelts. Those larval insects on the bottom of the rock that I grabbed are what scientists call poikilotherms. This is the more apt term for what used to be defined as cold-blooded animals because some of these animals have higher body temperatures than homeotherms (warm-blooded animals). These organisms’ body temperatures are determined by the surrounding environment. Because the body temperature of these insects is identical to the surrounding water temperature, they are unaware of the cold that I feel. Their compound eyes provide them a different perspective of the riverbed, and their noses are tuned to different chemicals than my nose. Thus, all those sensations that I described above are missing from their umwelt and vice versa. This beautiful habitat that I walked into only exists because of the unique combination of perceptual abilities that we have as humans. The beavers, deer, crayfish, hawks, trout, and even the various plants that inhabit this location each have their own umwelts which provides their own individual perspective on the surrounding environment. The purpose of this book is to provide you a glimpse into the various umwelts of the numerous animals inhabiting this planet. This field of scientific endeavor is called sensory ecology, and we have reached a point where we almost fully understand how organisms perceive and react to the sensory signals that are all around us. Thus, I want to share this understanding to you, the reader, such that you may understand what it is like to be an ant, a bat, a shark, or any other organism. My hope is that an appreciation of how organisms perceive this world might give us a fuller understanding of our interactions with nature, and, ultimately, we will become better stewards of this planet. Before moving on, I should address a possible issue that might have given you pause in the previous paragraphs. I subtly used the word “perspective” when writing about how insects perceive the river in which they live. It is possible to disagree with the use of perspective in referring to animals and to argue that this word solely belongs in cognitive heady world of humans. I can hear the critics of this use responding that animals and certainly plants do not possess the cognitive ability to have a perspective. Perspectives require attitudes and complex thought processes in regard to past, current, and potentially future events. I would counter that our understanding of the ability of animals to think and understand complex concepts is still growing by leaps and bounds. We, as humans, have a tendency to want to be a unique species, and as such, we underplay or disregard the ability of organisms to do the same things as we do. Repeatedly, scientific investigations have systematically torn down concept after concept that separates us from other animals. Tool use? Other animals do it. Complex social societies? Nonhuman animals have it.

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Emotions? It’s there. The last bastion of specialness, language, is currently hotly debated as some scientists would claim that animals form and use language, while others would argue that the hallmarks of language (syntax and grammar rules) are absent. Given recent advances in both the experimental ideas of consciousness and more philosophical debates on the concept of consciousness, animals appear to have more mental and cognitive capabilities than what was thought years ago. Thus, I will continue to use perspective throughout this book as a mental capability of animals.

1.1  The Sensuous World The joys of exploring. Whether I find myself in a new city or a stretch of nature, I feel some strange pull that tells me a good old walk is in order. An “explore” is what I call it. During these explorations, I unplug from the electronic world to immerse myself in the natural world. From these walks, I often discover interesting little secrets that provide a sense of wonder. Within urban environments, I am often on the lookout for a good hole in the wall restaurant. I choose ones that are often run by a family that really cares about food more than ambience and delivers authentic, lovingly cooked foods. Another urban find that catches my eye is the small bookstore, but sadly, these are going extinct. Traveling within natural habitats, I often search for the small and unseen. Moss, lichens, and flowers can be hidden among the taller plants but certainly create a distinctive appearance to the forest floor. On forest paths, small mushrooms on the underside of logs are often quite beautiful. I know of several hidden spots on well-traveled paths that have luminescent mushrooms that glow a wonderfully eerily blue or green in the dead of night. Finding these mushrooms requires a strong belief in one’s abilities because the search for these rare treasures involves a midnight hike in the woods without a flashlight. Found in the underbrush or at the base of trees, these mushrooms are a great fall discovery. A hike in the woods at midnight with nothing but a crescent moon and glowing mushrooms to light the path is akin to an out-of-body sensory experience. As humans, we typically gather most of our information about the world from our visual and auditory systems. Nighttime walks in the middle of the woods are often devoid of these two main channels of information. Initially, there is a sense of disorientation until your body and mind adjusts to the situation at hand. While I may be at a loss for typical sensory signals, there is a host of animals that have evolved to live within this habitat. I have often wondered about the role of these cues for the mushroom and what sort of creatures use these signals. One current thought is that nocturnal grazers are attracted to the light and come to the mushroom for a good meal. There appears to be no free meal though, because just like bees and flowers, these grazers will help the mushrooms spread and disperse around the forest. After grazing, the small mammals will transfer the spores of the mushroom that are caught within its coat of fur. Many nocturnal dwellers have adaptations like large eyes or a reflective tapetum that serves to amplify light. A large eye

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is similar to a large F stop on a camera which captures more light. The tapetum lucidum is a reflective structure that sits at the back of the eyes, behind the photoreceptors, of nocturnal vertebrates. Light rays that are not captured as they pass the photoreceptors a first time are reflected back across the receptors which give the receptors a second chance to absorb the light. Given that my own eyes have evolved to be used during daytime, my diurnal eyes struggle to see the otherworldly glow of the mushrooms. I wonder if these mushrooms, while dim for me, stand out as beacons to the nocturnal grazers with their far more sensitive eyes. On one of my more recent hikes to find these mushrooms, I came across an opening in the trees where the faint moonlight shone through to the forest floor. This whisper of moonlight was enough to wash out the green light from the mushrooms, so I turned my gaze toward the skies. This path is located in an area of the country that is devoid of human lights, so the skies are often beautifully lit with the Milky Way, and certain features of the moon can be seen on particularly clear nights. On this night, as I strained to see any craters on the surface, I noticed some quickly moving dark flashes fly across the front of the moon. I recognized these shapes as another favorite nighttime animal of mine, the bat. It appears as if this night has brought out several bats as I could almost follow several different shapes as they zig, zag, and drop chasing insects in the clearing. These creatures of the night, having limited visual signals present, use ultrasonic sounds to hunt down their prey. I can imagine that their world might be similar to my nighttime hunt for mushrooms. They, like me, are hunting for a small prey, whether mushrooms for me or insects for them, in a dark and silent world and sensing reflected stimuli. Their stimulus is the sound bouncing off flying insects, and mine is the light reflecting off trees and being produced by the mushrooms. Unlike my sensory world, these bats are creating their own umwelt by producing the calls that bounce off the prey and echo into their ears. These patterns of echoes carry information that is reconstructed by the bat’s brain to produce a three-dimensional world of objects. Some bats create such precise audio worlds that they can successfully navigate a room containing large amounts of randomly strung fine fishing lines. Many of us would be hard pressed to navigate this room in bright light with our eyes wide open. As I watched the bats dive and weave catching their nightly nourishment, I wondered how my present location would appear to me if I could echolocate. As I scanned my darken surroundings, I caught faint glimpses of tree trunks, a couple of mushrooms on the forest floor, and some small foliage with leafy edges fading into the darkness. As I hiked out to this spot, I had to travel quite slowly so that I would not trip over the occasional tree root or larger rock. What would my umwelt be if I listened with my ears for echoes as opposed to watching with my eyes for reflected light? Could I “hear” the roots as potential tripping hazards and be able to travel must faster? Could I hear the particular shapes of the mushrooms that pop out from the base of trees? Have you ever wondered what it would be like to be another person? Another animal? As a pet owner, I have stared at both of my cats and my dogs and often wondered what they were seeing, smelling, and ultimately thinking. I can say the

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word “out” or “treat” and see my dogs head cock to one side, ears perk up, and a narrow focus on his eyebrows. It is at this moment in time that I would love to hear and smell the world the way a dog does. What is it like to be a dog? Could I walk a proverbial mile in their shoes, hooves, or paws? This is the question that the American philosopher Thomas Nagel wrestled with in his often quoted 1974 essay “What is it like to be a bat?.” This essay is an essential read for any beginning student in philosophy. Within the paper, Nagel argues against what is known as the materialistic theories of consciousness. Materialistic theories state that what we call the mind and consciousness naturally arises from the large number of neuronal connections within the human brain. The same holds true for other animals that have various levels of conscious states. In other words, who we are is nothing more than intricate and detailed wiring within our brain. Nagel argues that consciousness and everything that comes with that consciousness (love, sadness, good, and evil) is more than just the complex wiring of a highly advanced computer (our brain). There is an essential (but unnamed) factor that creates consciousness. To strip away everything that makes us human to merely neural connections misses the essential elements of what consciousness means. These essential elements make the mental state of other organisms unique and inaccessible to us. Thus, to Nagel, attempting to “fly a mile in a bat’s mind” is a fruitless endeavor. I would disagree with Nagel. Let’s try a task that is much closer to our own perceptual world before we jump into a bat’s brain. Consider, for a second, the perceptual world of a red-green color-blind human. Simple tasks that the rest of us would perform one way are often modified by people with these color deficits. Most of us, while driving in any urban environment, would pay special attention to the colors of a stoplight. Red meaning stop, and green meaning go. Other sensory cues are most likely ignored or only play a minor role in our decision on which pedal to press within the car. One of those sensory cues is the location of the lights. Red is on top and green on the bottom. I would imagine that we could flip those locations and probably not cause too much problem for most people. Red-green color-blind people would be at a loss. For them, the colors of the stop and go signals are indistinguishable, and what carries the key piece of information for them is the location of the light. If the top light is on, that means stop. If the bottom light is bright, that means go. While the total sensory image is the same for both people, the color-blind individual perceives and responds to location of light, whereas the normal-sighted individuals respond to which color is lit. This translation in information appears to be an easy step to make. So, is it possible to imagine what the world is like for a red-green color-blind human? Seems like it may be possible. Still, trying to imagine how the mind of a color-blind human works is a small step compared to nonhuman animals. In the small little forest section around me, bats, moths, gnats, owls, deer, moles, and mosquitos are just a few of the animals that keep me company on a dark night. Each of them had different sets of perceptual abilities guiding their movements and behaviors. Beside the sensory capabilities of the bats previously mentioned, the mosquitos, who craved a meal to be siphoned from my arm, searched for little puffs of CO2 that are being exhaled from my

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n­ ostrils. The moles, who built tunnels underneath my feet, used exquisitely tuned vibration detectors on their jaws and feet. I wondered what they sense every time I take a step and send waves of energy through the ground. Called seismic detection, some snakes have receptors in the jaws for sensing animals moving along the ground. A couple of these nighttime denizens were homing in on the heat signatures coming off warm bodies such as my own. This nighttime world, as well as any other habitat, is full of sensory signals that are undetectable to us because we either lack the sensory equipment or the sensitivity to detect those signals. Each animal has its own unique sensory world tuned through evolutionary processes to those range of stimuli that carry important information for them. The sensory signals and the information carried within those signals give rise to the perception and perspectives that is their world. This combination of signals and stimuli is the sensuous world alluded to in the title of this section. A world beyond our ability to comprehend and, because of that failing, potentially inhibiting our ability to understand how other animals interact with the world around them. Our ignorance or woeful neglect of these other sensory perspectives can lead to serious ecological problems. The lights of beach houses cause baby sea turtles to navigate toward beach house lighting, away from the ocean, which is a lethal choice. In high traffic and urban areas, the increase in background noise drowns out alarm calls and, as a result, has caused significant alterations in bird songs. The large number of anthropogenic chemicals that are being infused into the world’s freshwaters is disrupting mating systems in many fish. These are just a few instances of how humans have negatively altered the sensory landscape of other animals.

1.2  The Mind’s Eye Even within our own sensuous world, the importance of our own senses in coloring how we perceive the world is often underappreciated. Our eyes, ears, and nose as representations of our senses are the windows in which our mind perceives the world around us. There is a tendency to think that our senses provide our mind a transparent and unobstructed view of reality. We think the red of the flower is really there and readily apparent to everyone. The call of a mockingbird is equally melodious to everyone that hears it. The smell of a cinnamon roll baking in the morning is equally sweet to every potential customer. The proverbial “seeing is believing” aphorism connotes this very concept. Something is not real unless it is directly sensed, but once sensed, nothing can convince us that it is not real. Unfortunately, this is not the case. Our senses filter and transform much of the world such that we are only aware of a small fraction of reality. To be fair to modern neuroscience, we don’t smell with our noses or see with our eyes. The process of seeing, hearing, smelling, and the other senses arises from the brain. Stimuli are captured and filtered by our noses, eyes, and ears, but putting all those sensory stimuli together into a coherent framework is done by all of the neural connections within our brain. What this means is that the “real” world, the world

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that generates all of those wonderful smells and sounds, is a construct of our mind based off of information that has been transformed, filtered, and, in some cases, rejected by the neural circuitry even before that information reaches our central processing. Remember the kid’s game called “telephone” or “whisper down the alley”? This is a game where one person tells something to another person. This person then tells another and so on. At each step of the retelling, the original information gets slightly altered such that at the end of the game the final sentence is nothing like the original. We play this game as adults, except we call it gossip. The connection from the real world to our brain’s construction of the real world is similar to the telephone (or gossip) game that has been finely tuned by natural selection. Our brain, and those of every animal on the planet, has filters and transformations that supply information to the brain. Except that this information is not what objective reality is; these filters supply what the brain needs to perceive in order to survive which is specific to the individual. This singular idea sets the notion “seeing is believing” right on its head. We don’t see the world as it is, we see the world as we believe it is. How about an example to illustrate this point? Many visual systems have a special set of neural connections that enhances edge detection. Edge detection is performed when animals are attempting to determine where one object stops and another one starts, like a single tree against a forest or the corner of a wall seen against another wall. Edge detection is an important part of our visual world as it enhances the distinctiveness of objects. A moment’s glance around the room or place that you are sitting in will provide you with many examples of edges being artificially enhanced by your brain’s filters. As I type this, I am sitting at my desk and viewing at least 30 different edges around me: my computer monitor, the phone, a stack of sticky notes, a stapler, bookmarks, and all sorts of other objects have a distinct line between themselves and the object next to or beneath them. Edge detection can be performed by a simple process known as lateral inhibition. Imagine a nice neat row of photoreceptors like a line of tubas in a marching band, all of them ready to be excited by light. In addition to this line, each photoreceptor has a neural connection to its immediate neighbors on the left and right. Lateral inhibition works through this connection. When a photoreceptor is excited, it sends a signal laterally through the connection to its neighbors which inhibits them from being excited. In our marching band example, our row of tubas are quietly playing a song. At one point in the song, a spot light focuses on the middle tuba player which causes her to play really loud. In addition to her playing, she throws pieces of foam in the tubas to the right and left of her to quiet them down. Because her neighbors are not playing, her tuba (without the foam) stands out, nice and loud. Her immediate neighbors are very quiet because they have foam (inhibition) in their tubas. Tubas that are two spots away do not have any foam, so their background playing is unaffected. If we were to measure the loudness along our line of tubas, we would detect a medium intensity sound from most of the tubas until we come to the inhibited player. Here the sound would drop to a very quiet level and then jump to loud sound for the tuba in the spotlight. The change in sound between the spotlighted tuba and its neighbor has been enhanced by the lateral inhibition.

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If we widen the spotlight to include other tubas along the row to maybe five other tubas, a second feature of lateral inhibition is found. Again, if we measure the sound of our tuba players from left to right, most of the tubas are playing a medium volume until we get to the first tuba at the edge of the spotlight. The tuba in the dark is being inhibited by the spotlighted tuba as covered above. The first tuba in the spotlight is only inhibited by its neighbor further in the spotlight. The second (third and fourth) tuba is inhibited by both of its neighbors in the spotlight. So the middle tubas are playing loudly, but more quietly than the first tuba at the edge of the spotlight because they receive inhibition by two tubas. The last tuba in the spotlight is identical to the first tuba in that she is only inhibited by one other player. In this scenario, the loudest tubas are in the light at the edge of the spotlight, and the quietest tubas are in the dark at the edge of the spotlight. In our marching band, the spotlight edge is evident by the difference between the loudest and quietest tubas. In vision, edges are enhanced by lateral inhibition, by making the photoreceptors at the edge of the shapes of objects either more excited (if they are in the light) or more inhibited (if they are in the dark). Again, this filter (lateral inhibition) has augmented an important pattern in nature because the detection of edges has survival value. There is more about the different filters that are associated with our visual world (and other sensory worlds) in other chapters. The main point of this description is to demonstrate that our brain sees one phenomenon (enhanced edges) that is not really there. In a way, our eyes and brain, along with the many filters in between, have created a useful illusion of reality. These filters create or enhance one aspect of the world but, by their very design, diminish other aspects of the sensuous world. Given this, one wonders if reality is in actuality possible to perceive.

1.3  The Illusive World Our brains, using the information gathered by our senses, construct a reality. I use the term “a” reality because I will present some evidence that a singular reality that is true for all humans does not exist. Also, given the different sensory capabilities of the organisms covered in this book, one could draw the conclusion that a singular true reality does not exist even for all of nature. This is the illusive world referred to in the book’s title. Our world is full of sensory energies (the sensuous world) that are filtered, transformed, altered, as well as combined with assumptions about how the world works to create a grand illusion that is perceived by our brain. The old adage that “seeing is believing,” within a larger context, makes the fundamental assumption that we have the ability to perceive reality. When I grab a cold iced tea on a hot day, the moisture on the glass is real. The cooler temperature of the glass, compared to the air temperature, is real. The taste of the tea with a subtle hint of lemon, as I drink, is real. The actual truth of the matter is my brain recreates reality using the filtered and transformed sensory information combined with a large set of assumptions about the world to produce my individualistic reality. Imagine ­sitting

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in your car at a stoplight, and the car next to you begins to move slowly backwards. The first instinct that your brain produces is that your car is moving forward, so you hit the brake pedal harder. Another example is the old reliable trick when playing fetch with a dog. The trick where you pretend to throw the ball and the dog takes off after an imaginary throw. In these instances, the brain perceives something other than reality because the assumptions about reality overrule the actual sensory information. If we think that our intelligence would preclude us from falling for the fake throw trick, magicians fool us all the time using this same trick by pretending to either throw a card across the stage or catch just the right card out of midair. Our fallible brain, coupled with incomplete sensory input, constructs reality, and this reality is an illusion. This concept about our ability to perceive reality is clearly demonstrated by peering into the world of magic. Magicians, in general, and illusionists, in particular, are intuitively tuned into how our sensory systems work. They hack our sensory systems and use them against us to entertain, confuse, and delight. One of the major tools in the magician’s arsenal is our sensory expectations. We experience the world based on our expectations about the world (i.e., the thrown ball trick). These expectations are based on our past experiences. For example, imagine that I am standing behind a desk with a basketball in my hands. I tell you that I am going to bounce the basketball off the floor. At this very point in time, your brain begins to develop a series of expectations about what I am about to do and, in essence, primes your sensory systems to perceive the next experience in the way that you want to perceive it. Given what you know about the basketball and floor, you would have some expectation on the height of the bounce. A quick glance at the floor should provide to you some expectation on the sound of the bounce. I can pretend to throw the ball down (but don’t), have a device that produces an appropriate bounce sound, and then pretend to bring the ball up to catch it. If done correctly, I can convince your brain that the basketball was actually bounced despite the fact that it never left my hands. These same set of assumptions or expectations and sensory hacks are used in close up magic using cards and coins. When we see motion (a bird flying or a ball being thrown), our mind quickly sets up a predicted path of motion. Thus, we follow the bird or ball to where we are expecting it to proceed. In sleight of hand (or close up) magic, the magician creates motion in the cards or coins, and our brain begins to predict where that card or coin should go. The magician then interrupts this predicted motion. Our eyes continue along the predicted path, but the card or coin is missing. Thus, the trick is performed and the object has “vanished.” Along with these sensory/brain hacks, the good magician can actually control the attention of the audience. This can be called misdirection, but this type of name really doesn’t fit the processes involved. A better concept would be awareness control. The magician gets you to focus really hard on an object or location and then narrows your awareness so much that the trick can be performed. An excellent, and non-magical, version of awareness control is demonstrated by the famous invisible gorilla trick. This interesting and enlightening experiment was first performed by Chris Chabris and Dan Simmons, and, at first glance, seems unbelievable. I have

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actually seen a subsequent version performed in person and was amazed at the outcome. The experiment can be set up using the following dialogue. You can tell the audience that one sex (say women) is better at paying attention than the other sex. To test this, you are going to have the audience watch a video. In the video, there are six people who are passing and bouncing two basketballs in a hallway. Half of the people are in dark t-shirts and half in white t-shirts. Your job is simple: count the number of times the basketball is passed by the people in the white t-shirt. Finally, you tell your audience to pay special attention to the passes because we want an accurate count for our experiment. Then you start the 1-min video. About halfway through the video, a person dressed in a gorilla suit casually walks across the scene. Interestingly, in the original and many replicated experiments, most individuals are so focused on the people in white and their passes that they claim not to have seen the gorilla. Some participants are quite adamant that the gorilla was not in the original video and claim that when they watch the video a second time, it is a different video. Our visual/brain system has the ability to focus so intently on those issues that are important to us (even if is told to us by a psychologist) that we filter out or ignore other aspects of our visual scene. In part, our brain was primed to focus the visual attention of the participants on the bouncing ball. So, our expectations helped create the illusion of the invisible gorilla. When most of us think about magicians, we envision visual tricks. Yet, these same hacks of our sensory system can be performed using other sensory systems. One of the greatest performers that hacks our other sensory systems for his act is Apollo Robbins, the gentleman thief. Robbins’ act consists of a series of actions that controls your awareness such that he can steal your wallet, watch, or other belongings while he is telling you he is stealing your objects. Robbins will control your awareness by artfully pressing, compressing, or touching parts of your body so that your focus is on one part of your body, while he removes objects on other parts of your body. Thus, the mechanical sensations that he creates by touching your body allows him to control your awareness such that he controls the umwelt that your mind perceives. Taken together, these examples should demonstrate that our sensory systems really perceive a combination of the sensory world and our expectations of the world. But why would our sensory system create illusions of reality instead of any objective reality? The simple and elegant answer is necessity. As you read the many examples of the wonderful and unique sensory abilities of animals outlined in subsequent chapters, it is helpful to keep in mind that these sensory systems are adaptations in response to needs of the individual organism. For our senses, there simply is no survival value in detecting all of the sensory information that is available from the surrounding world. There is, though, survival value in focusing our awareness on that part of the sensory world that can impact us. In addition, being able to predict the world (such as the flight of a bird or the movement of a fish) has additional survival value. Thus, we should not expect that our senses give us an objective reality. Our eyes, ears, and other avenues of perceiving the world gives us a slice of reality that our mind then creates the rest of the picture. This picture is the illusive world, which is just a fraction of the sensuous world.

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1.4  What Really Is Reality? From a philosophical and experimental perspective, many have argued that reality, as defined as an objective perceived world around us, is not even available to our mind. Our reality is one that is reconstructed from our sensory perceptions (along with its biases, filtering, and assumptions), and this reality is our, and only our, reality. This world does not exist for anyone else. Our world is really a subjective world, and this subjective world biases and colors all of our future decisions and interactions with all of the animals and people around us. Despite the solitude the singular reality creates, it might be possible to, at the very least, begin to understand what reality is to other organisms. So, maybe with all of the conceptual and fundamental principles covered in the previous sections, we can return to Thomas Nagel’s famous question of “What it is like to be a bat?.” While it is true that the functioning of the human mind is one of science’s last truly unknown areas, the field of cognitive science has progressed significantly since Nagel first wrote his essay. Today, we understand how many different species of whales produce song and how learning that song with regional dialects occurs year after year. Researchers have solved the riddle of how bats can locate and predict the flight patterns of small moths using ultrasonic sounds. We know the perceptual physics of a fish with its two eyes essentially subdivided so that the bottom half of both can see on land and the top half can see underwater. These are just three amazing examples of how animals have evolved specialized senses that allow them to perceive the natural world in a very different way than humans do. Despite these differences, the science of their senses, the use of information gathered by their senses and, in some cases, how the brain creates perception are all known. The wealth of studies in animal behavior, ecology, neuroscience, and cellular biology allows us to understand how animals perceive their world. If perception creates reality, then this scientific information provides us insight on what it is like to be a bat. To be fair to Nagel’s argument, it is quite possible that there are essential elements to the uniqueness of different organisms that we may be limit to something less than a full and complete understanding of what it means to be another organism. Still, this doesn’t mean our understanding isn’t close to complete. The bat’s (and our own) mind and states of consciousness are heavily influenced by the interactions of those minds with the surrounding world or, in other words, through the perception of the world. For simplicity of presentation, the cognitive abilities of the mind of any animal start with the neural architecture of the brain. This is the “wires and connections” that are initially constructed following the instructions within the genetic code of the animal. These instructions lay down certain specialized neural areas that allow animals to perform amazing feats of detection. In general, these areas can be called glomeruli or neuropils and are dense networks of interconnected neurons in the brain. This is similar to the collection of wires that lies behind any sophisticated home entertainment system, but with a lot more evolutionary selection for organization. One such area, called the mushroom bodies found in the insect brain, plays an important role in the learning and memory

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of chemical signals (olfaction). The exact types of connections that are developed and reinforced are directly shaped by the sensory world in which the insect lives. Although this description is quite mechanical in presentation, the use of powerful computer simulations can put all of these mechanical connections into a perspective that is understandable by us. If we assume, just as a starting point, that the human or animal mind is a combination of instinctual connections and additional connections modified by sensory experiences, then understanding those sensory perceptions can provide detailed insight into how that mind works. As humans, we have a tendency to assume that we perceive the world as it truly is. We assume we see reality. Our eyes, ears, and nose provide us with an accurate record of the world around us. Yet we have a really limited set of sensations. The purpose of the examples contained within the subsequent chapters is designed to provide some insight into the illusive world. This is the world of other animals and their senses, and this is the world that will give us a glimpse of what it is like to be them, even if just for a moment. What follows this introductory chapter is a series of stories: animal stories to be more precise. These stories are organized at the beginning by labels of our own senses: the eye, the ear, the nose, the tongue, and the tactile sense. While these labels are wildly inaccurate when applied to animals, they do provide a familiar attachment to our own world and will hopefully allow the reader to make an intellectual connection to the behaviors and sensory perspective being explained. Within each section, I have placed multiple chapters that include three elements. The first element is a short introductory segment designed to place you, the reader, within the proper sensory context. Within the sensory field, we often use the term landscape with some adjective attached at the beginning to describe the stimulus world. For example, visual landscape describes the surrounding environment that contains stimuli associated with light or vision. The chemical landscape is the one associated with our sense of smell, and the auditory landscape is the one associated with our hearing. As attractive as these terms are, they feel awkward when applied to those senses that are further afield from our own world. Many reptiles have the ability to sense heat, so they would have a thermal landscape. Others, such as spiders, water striders, and moles, can detect vibratory cues, so they should have a tremor landscape. The ability to detect electrical, magnetic, and other signals creates weird sounding and unimaginative landscapes. Thus, the introduction to each chapter provides some sensory context for the reader. The second part of each chapter is a description of the animal behavior or the ecological event that occurs. Since our world is primarily constructed of visual and auditory cues, the descriptions will be forced to use terms associated with those senses. Finally, the last section of each chapter provides a scientific explanation on how animals perform the tasks that were just described. These last two sections will hopefully allow you to enter the perceptual world of the animal, albeit temporarily, to “see” a different world.

Part II

Vision

Vision is the art of seeing what is invisible to others. —Jonathan Swift

Chapter 2

Eyes as Windows to the Soul

Fall in the Midwest is one of my favorite times of the year. There is the return of my favorite seasonal flavors: pumpkin and cranberries. Pumpkin muffins and bread along with cranberry desserts seem to flood the local bakeries, coffee shops, and grocery stores highlighting my seasonal favorites. Cranberries can be found in fruit tarts, breads, and cereals and paired with oranges in muffins. Coupled with corn, apples, and cinnamon, the fall harvests seem to be full of rich and diverse flavors. If one is lucky enough to be in a town with several taverns and local breweries, both pumpkin and cranberries can be found within the local ales and lagers, too. Simply put, fall seasonal flavors mixed with the weather is my definition of perfect. My morning walk or bike to work provides me with crisp morning air that ensures I am fully awake when I enter my office, yet, not cold enough that I need to remove the chill from my body. By noon, the temperature on most days has risen to the point where shorts and a good pullover are sufficient to keep me warm on my travels across campus. Apart from the fall flavors and temperature, the explosion of colors emanating from the deciduous trees is certainly a treat for the eye. Along my route, I have a cornucopia of colors that delight my visual field. One of the most prevalent and noticeable colors is the bright orange of sugar maple trees with their little helicopter seeds scattered around the base of their trunk. A distinctive leaf with either three or five lobes is one of the most recognizable leaves for me to identify. The simple oval leaves of black walnut trees add a dash of yellow to my visual canvas. These colors remind me of the hundreds of walnuts that continuously fall into my backyard. The walnuts contain a chemical that is toxic to grass, so another fall ritual of mine is the constant removal of these nuts from my yard. The reds and oranges of oak trees intermix with the maples and walnut trees to produce a pointillist picture. White oak trees have leaves with smooth lobes (compared to the pointiness of the maples) and can get rather large (compared to the walnut trees). Further down in my route, I walk past the deep scarlets of Japanese maple trees, the yellows of elms and aspens, and the faithful greens of pine trees. Although selecting favorite fall colors may be very different across people, the perception of these colors, despite differences in names, is common across all of us. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_2

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Our ability to see and distinguish colors comes from a set of proteins located in the photoreceptors in our retina. The proteins, sensitive to different colors of light, are called opsins. Despite the plethora of colors in our visual world, humans only have three different opsins in our eyes that are most sensitive to red, green, and blue light. As described in the coming pages, other organisms can have more or less opsins and different color ones. Yet, with only three opsins, how is it possible to see the vast array of colors that humans can see? Our ability to distinguish large variations across the color spectrum is due to a combination of two neural processes: the trichromatic pigments and our ability to contrast opposition colors like red vs blue. Our brain uses these two processes to produce our ability to visualize a literal rainbow of colors. Even though we have three opsins that are most sensitive to red, green, and blue light, the actual sensitivity of any one of these opsins to light is over a range of color. For example, the “blue” photoreceptors show the highest sensitivity to light within the 420–440 nm range. (The unit nm refers to a length measurement where the m is meters and the n refers to nano or one billionth of a meter.) Light can be described by the wavelength inherent in the beam of light. Wavelengths are incredibly small and are measured in nanometers, which is one meter divided into a billion equal increments. The classic rainbow colors can be remembered by the mnemonic device Roy G.  Biv, which stands for red, orange, yellow, green, blue, indigo, and violet. These colors are also in a linear arrangement from longest wavelength (red) to shortest (violet). So, our blue photoreceptors are most sensitive to the shorter wavelength light. Yet, the range of light that activates these receptors varies from 390 to 470 nm with a peak at 419 or from violet to blueish-green light. In a similar fashion, our “green” photoreceptors are sensitive to a range that includes indigo (approximately 450 nm) to yellow (620 nm) with a peak at 531 (green). Finally, our “red” photoreceptors range from dark green (470 nm) to the near red (650 nm). Thus, there is both a range of sensitivity and overlap between our three types of photopigments (opsins). So, one of the ways that our brain interprets different colors is by comparing the amount of excitation from these three color receptor types. A yellow light would not activate our photoreceptors with blue pigments, but would highly activate our red pigments and, to a lesser degree, activate our green pigments. We sense this combination of excitation as yellow. A second process involves the processing of information in an antagonistic way. Our brain compares the excitation due to “rival” colors, black versus white or blue versus yellow. These two mechanisms allow me to distinguish the yellow leaves of the black walnut trees with the oranges produced by the oak trees. Apart from the colors, the shape of the leaves (the number of lobes or the smoothness of the margins) allows me to distinguish the different species of trees that are contributing to my colorful walk. Even though I am not a botanist, I can easily differentiate the five-starred jagged edges of the sugar maple leaves compared to the ornate soft lobed edges of the oak tree leaf. My eyes have three adaptations that enable me to reproduce a robust image of the world around me: a lens that focuses light, a retina that is sensitive to ranges of colors, and a set of neural networks that artificially enhances important elements of the visual scene. The light being reflected from the leaves enters my visual system through a lens which helps to focus the

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light onto a central area of my retina. My retina has an area of densely packed, highly sensitive receptor cells called the fovea, which allows me to see small spatial differences in my visual field (like the multiple ridges on a leaf from an elm tree). Finally, and maybe more brain than eye, I have a set of neural networks that enhances the edges between two objects so that I can distinguish the end of one leaf and the beginning of another when gazing at a pile of leaves. This is essentially the visual system of humans that allows me to enjoy the splendid fall colors. As we shall see in the next few chapters, these three elements (lens, retina, and neural networks) vary tremendously across the animal kingdom. Some animals don’t have lenses at all, while others have thousands of tiny lenses for each separate eye. The shape and number of different types of retinal cells create different abilities (and limitations) for animals, and finally, neural processing allows the brain of an organism to see the world in a way that gathers the most important information for survival. This processing also filters out information that evolution has determined is unimportant for organisms and, thus, limits what any particular organism sees. The stories that follow are designed to show you how the world appears through an organism’s eyes and their other senses. The first step in this strange adventure is to place you in the field observing the organism’s behavior within an ecological context. The words will attempt to provide you a visual description of the scene, whether that is the tops of mountains, the depths of the oceans, or even underground burrows. As the short one act play of life unfolds, I will attempt to capture all the nuances of the behaviors being exhibited with just the words on the page. Your job as reader is attempting to fill in the rest of the sensory scene with your imagination, which is the end point of this entire book. The difficult part will be translating words on a page to an entire sensory landscape. Certainly, imagining a hawk swooping out of the air to capture its prey may be a lot easier than imagining two large fish, say groupers, bellowing at each other at the bottom of ocean. If it helps, you can imagine hearing the words being spoken by your favorite nature documentary narrator.

2.1  Double Vision Our first sensory trip will take place in the brackish waters of South America. The brackish waters (water that isn’t quite as salty as seawater, yet contains more salt than freshwater) are located deep among the mangrove trees and dominate the northern part of the South American continent. One of the most unique features of a mangrove swamp is the aerial root system of the mangrove trees. Looking like giant fingers, the roots are either emerging from the murky water reaching for the sky or, if attached to the main trunk of the tree, appear to be fingers dipping their nails in the water. The roots create a densely packed aquatic forest which serves to dissipate much of the wave action from the open ocean. The surface of the water is as calm and flat as a sheet of glass. Above the water, several insects zip around searching for food or mates. Occasionally, one of the insects will lightly touch down on the surface of the water creating ripples that

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Fig. 2.1  The Anableps’ eye. The left drawing shows the position of the fish within the water column. The upper right drawing shows the direction of terrestrial light (green arrows) and aquatic light (blue arrows) as they travel through the lens of the fish. The bottom right drawing shows a close up of the lens of the eye

extend outward in ever-growing circles. As the ripples speed outward, they are unimpeded until they bounce off what appears to be two small glass marbles floating on the surface of the water. The marbles slowly move together across the water in and around the mangrove fingers. The movement clearly indicates that the marbles are not inanimate features of this small swamp. On closer inspection, a pair of irides behind the glassy exterior can be seen indicating that these must be the eyes of some aquatic creature (Fig. 2.1). The marbles are actually the eyes of a strange fish affectionately called the four-eyed fish. The eyes belong to fish in the genus Anableps who inhabit freshwater and brackish environments from Honduras to the northern part of South America. One of the favorite habitats of the Anableps is the mangrove swamps that border many of the coastal areas in this region of the globe. The fish has a flattened upper body, almost like a submerged aircraft carrier that allows the fish to float right at the surface of the water with only its eyes protruding above the water line. Moving slowly between the roots of the mangrove trees, the fish and its two marble eyes dart forward and then pause. After a short burst forward, the fish pauses again. Clearly, the eyes appear to be searching for something important above the water. A sudden movement on one of the mangrove roots appears to catch the fish’s attention. An orange-tinted object has moved downward on a root and is moving

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toward the water’s edge. The orange is part of the coloration on the front side of a claw belonging to a mangrove crab, and the crab has decided to move toward the water for a drink. This movement has not gone unnoticed by the fish as it progresses toward the crab. Interestingly, while the fish has focused on the movement of the crab above the water, it is also fully aware of any activity beneath the surface of the water. Among humans, this nickname (four-eyed) indicates the presence of another set of lenses to fix poor vision: eyeglasses. Anableps actually have excellent vision, and the four-­ eyed moniker refers to two lenses (and retinas) that create the ability to see above and below the water simultaneously. In some ways, this animal’s vision is similar to many of our office situations where we have two different monitors for our computer. Each screen can display different material granting workers the ability to “see” two different images at once. Unlike the four-eyed fish, we can actually only register and examine one image at a time. We can quickly glance back and forth between the monitors, but our brain can only process each image separately. Anableps and its exquisitely adapted visual system have no need to switch between the two images as they see both simultaneously. Anableps fish mainly consume either algae that grow on the emergent part of the mangrove roots or small crabs and crustaceans that scurry along the roots themselves. Never diving deep, the fish float at the surface to keep their uniquely adapted eyes in the air in search of food. A smaller fish (about 30 cm in length), Anableps is susceptible to the many larger fish that lurk deeper in the waters of the swamp. Having eyes that are constantly observing the terrestrial world while being blind to all of the potential dangers beneath the fish would seem like a poor adaptation. As the fish slowly approaches, the crab is unaware of the danger that lurks beneath the two little marbles moving across the water’s surface. The fish approaches so close that it almost touches the mangrove root. Just as it gets ready to make its lunge to capture the crab, the crab sees the attack and tries to escape. The animal is keeping “two” of its eyes on its prey, the other “two” eyes focused on any potential approaching danger from below. If movement beneath the fish is detected, the animal can make an estimate of the relative distance between its prey and its predator in order to decide whether to continue its hunt or run away. If the potential danger from below turns in to a potential competitor for the mangrove swamp crab, a different decision can be made. The above the water and below the water images are combined into a singular coherent image of the world for the fish. With the ability to see both above and below the water line concurrently, the mangrove crab is still in focus of the Anableps and in striking range. With a powerful lunge from its front fins, the fish launches itself on land toward the mangrove crab. Its aim is true and the crab becomes a hearty meal for the fish. The fish slowly turns around, using its fins as makeshift legs, and dives into the water in search of more prey. In the mangrove swamp, food is almost always above the water line, whereas threats from bigger fish (below) and from the many different waterfowl (above) can come from both habitats. As such, it is important for these fish to not only be able to see these distinct habitats simultaneously but also be able to focus the images clearly in order to make life and death decisions.

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2.2  The Science of the Four-Eyed Fish As stated previously, in its simplest form, a visual system consists of a lens to focus light, a retina to detect intensity and color, and a neural network that extracts relevant information. For the four-eyed fish, the first two elements (the lens and the retina) are where unique adaptations are located, but a basic understanding of how lenses work is needed to understand the uniqueness of this fish’s eyes. For all intents and purposes, light can be considered as traveling in parallel waves from an object to our eyes. The speed of the movement of the light wave depends upon the medium (air, water, or glass) that the light is traveling through. The vacuum of space allows light to travel rather quickly, whereas light travels much slower in water. This is because these two media (air and water)  have different optical densities (which are not to be confused with physical density). Physical density relates the mass of an object to its volumes, whereas optical density refers to speed at which the media or object absorbs and releases electromagnetic energy. Objects like diamonds have a relatively high optical density, and the lowest optical density is found within a vacuum. For perspective, air is only slightly more dense than a vacuum (0.03%), while water is roughly 33% more dense than air. As light travels from one medium (air) into a second medium with different optical density (e.g., the lenses of eyes), the wave front of the light gets refracted which means that the light changes direction. A great example of this phenomenon is a triangular prism sitting on a table that catches sunlight (or on the cover of the Pink Floyd album “Dark Side of the Moon”). The colors that are evident after the light travels through the prism are indicative of refraction. Understanding the process of refraction may be better improved by returning to our marching band from Chap. 1. Now, instead of a line of tubas competing to be heard, imagine the entire marching band line after line after line, marching down a paved street in some type of parade. The lines of the marching band are the wave fronts of light, and the street is representative of the optical density of the medium. As the band progresses down the street, the rows of marchers are nice and neat and remain in a straight line because the street (optical density) remains constant. If we imagine that the street changes from pavement to sand (representing a transition from air to water), the marchers (and hence each row) will slow down because the sand makes marching more difficult. If we were to watch the band from above, we would notice the spacing between lines would begin to narrow as the band moves from pavement to sand. This is exactly what happens to light traveling from one medium to a second one with a different optical density. This description works well except that in many cases the wave front of the light does not strike the new medium perpendicularly. So instead of a change from pavement to sand for an entire row, imagine that the street changes on a diagonal, such that one end of the line hits the sand earlier than the other end of the line. This is the case for light traveling through an angled prism, light hitting the surface of water, or even light traveling through the lenses of eyes. In this case, those marchers that transition from pavement to sand will slow earlier and at a greater rate than the other

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end of the row of marchers. In this case, the row of marchers (or wave front of light) “bend” toward the slower medium and gets refracted. This “bend” is called the angle of refraction and is dependent upon the change in optical density between the two mediums. This is the key to the construction of the lens of the four-eyed fish. To see in air and water simultaneously means solving the problem of two different optical density shifts. As light travels from air to a terrestrial lens, the wave front becomes refracted because lenses are more optically dense than air. As light travels from water to an aquatic lens, the wave front gets refracted, but is refracted less than the transition from air to lens for terrestrial organisms because the water and lens have a closer optical density. Thus, underwater lenses must perform more refraction to focus the light to a central spot on the retina. This difference in the amount of refraction explains why we have difficultly focusing on underwater objects without the help of snorkeling masks. Our lenses are not shaped to focus light that travels from water to our lens. Our lenses are convex in shape to focus light traveling from air to the retina. Interestingly, most fish eye lenses are circular and layered (like an onion), where each layer has a slightly different optical density to focus light arriving from underwater. The circular lens is often quite larger than the convex lens of terrestrial organisms which allows the lens to refract the light even more. The larger lens refraction is needed because the initial refraction from medium to lens is lower in water than in air. So, how does our four-eyed fish deal with this problem associated with two different levels of refraction found in air and water? The lens of the Anableps is neither convex like terrestrial eyes nor circular like most fish lenses. The lens is actually oval shaped with the long axis of the oval along the pathway from underwater light. In addition, the lens has a band of tissue that divides the lens into a terrestrial and aquatic lens. Thus, light traveling from underwater has a longer optical pathway and thus, more refraction is performed. The light traveling from air through the lens passes through the narrower part of the lens and is refracted less. This unique shape with different optical properties performs the task of focusing light from two different media onto retinas. Although this explains the ability to focus light, how does this fish see two different habitats (above and below water) simultaneously? Turns out that the four-eyed fish actually has two different retinas. One retina is located at the top of the eye but receives the focused light from beneath the water’s surface. A second retina is located at the bottom of the eye and receives the focused light from the air. So, two different retinas are situated on the posterior part of the eye to create separate, but integrated, visual images. This aspect is just the beginning of the answer for the four-eyed fish. Light travels through water differently than air. The major difference between these two mediums is how the different ends of the rainbow spectrum get absorbed or scattered. At one end of the spectrum is long wavelength light such as red and infrared. Light at this end of the spectrum, particularly in the infrared zone, can almost be considered heat, and these wavelengths get absorbed rather quickly in optically dense material (i.e., water). Thus, red light doesn’t travel far in water because the energy in this spectral band gets absorbed rather quickly.

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At the other end of the spectrum (blue, violet) is the short wavelength light. Unlike the long wavelength, light within this spectrum does not get absorbed as heat, so this light travels much farther in water than red light. The short wavelengths bounce off of small particles in the air and water in a process known as scattering. The wavelengths are so short that small particles (such as dust, smog, or silt) can cause the light to be reflected off in random angles. Scattering causes these wavelengths to bounce around all of the small particles under the light and eventually penetrates through the air or water. This process (scattering) is why the sky appears blue to our eyes. The short wavelength blue light is bouncing around the atmosphere (by hitting small particles) until it eventually bounces toward our eyes. For the Anableps, not only does the eye have to be adapted to differences in refractive changes in air and water, the color and wavelengths of available light are different between the two habitats. What does this mean for our fish? The two retinas of the four-eyed fish have different visual pigments and are sensitive to two different sets of colors. The “aquatic” retina, located on the top and receiving light from below, has photoreceptor cells sensitive to yellow, blue, and purple light. The “aerial” retina, located at the bottom and sensitive to light from above, has the same blue and purple photoreceptors but has replaced the yellow receptor with a green-­ sensitive one. Scientists speculate that the aquatic eye is sensitive to yellow light because of natural chemicals common in mangrove swamps that tend to turn the water a yellowish tint. The Anableps’ visual umwelt is a split-screen clear vision of two worlds. One world is a terrestrial world dominated by clear surroundings, long vision, and a full spectrum. The second world is one with the absence of red, shortened vision due to increased absorption of light in water and enhanced focusing due to the small differences between the optical density of the lens and water. Although called the four-­ eyed fish because of the appearance and presence of four retinas, I prefer the concept of double vision, as the fish has a clear vision of two different visual worlds.

Chapter 3

The Pollinator’s Garden

The fall colors of deciduous trees are quite beautiful, but pale in comparison to the dazzling colors of a fall garden. Asters provide a range of pastel blues, pinks, and purples to offset the orange and red of the oaks and maples. Mums, which always reminded me of colorful moss-covered rocks, pop up across gardens and decks. The yellows and whites add a little brightness to the seasonal colors. The lilies are standing tall with speckled purple and white flowers. Goldenrods remind us of the last warm sunny days. The purple and red sages blend in nicely with the turning leaves. These late blooming flowers do more than simply supply our eyes with additional color for our homes and gardens. The fall serves as the last time of the year for insect pollinators to gather up pollen and nectar for the creation of honey. Fall is really a critical time for bees because they need to prepare themselves, the nest, and most importantly, the queen for the dangerous cold of winter. Bees are poikilotherms which is the scientifically correct term for what is commonly called cold-blooded animals. Poikilotherms do not have the ability to regulate their internal body temperatures and, as such, have a much more variable core body temperature, up to tens of degrees C. Their temperature is primarily due to two factors: the external temperature and physical activity. Many poikilotherms have much warmer body temperature, even higher than homeotherms (animals with a more constant body temperature), during peak activity time, thus the term cold-blooded is inaccurate. To regulate their body temperature, bees need to remain active or, at least, remain in motion. If their body or hive becomes too cold, they’ll die. Bees have adopted a unique strategy to keep their hive and queen alive during those long, cold winters. To do this, the worker bees form a giant living ball around their queen, and all the worker bees periodically vibrate their wings. This activity generates enough heat to keep the hive from freezing and killing the queen. Usually, the worker bees rotate their position within the giant ball so that any individual bee does not get too cold. To keep this activity up throughout the winter, the colony of bees will consume stored honey throughout the season. One of the key elements of a colony surviving the harsh reality of a cold winter is the storage of honey. Thus, fall gardens, with their colorful flowers, provide important resources such as pollen © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_3

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and nectar to produce the vital honey that will keep the hive alive through the winter. A stroll through a fall garden will certainly show me the colorful resources available to the local hives. In addition to the asters mentioned above, sunflowers provide a brilliant yellow. Purples, whites, and yellows are provided by little crocus. Interspersed are the colors of reds, oranges, and browns that shine through with pansies. Often, we think that spring and summer are the times for colorful and expansive gardens, but fall can bring on a much larger color palette since both the trees and flowers contribute to the visual sensations. I find the purples and reds to be the most visually appealing. The deep colors seem to attract my attention more than the lighter colors. Given the range of colors, I wonder what colors and shapes draw in our pollinators by advertising that last meal before a long winter. It turns out that the pollinator’s garden is very different than the garden I see before me.

3.1  On the Hunt for Nectar As I walk through a local garden, I am surrounded by a sea of pink and purple asters, all in bloom and waiting for their pollinators to come for a visit. Instead of taking in the entire garden in front of me, I can focus on single flowers for inspection. I choose a single pink flower and bend over to get a closer look. What I see is not a single color of solid pink but a menagerie of colors. The outer tips of the petals, called ray flowers, are colored a subtle yellow that bleeds into the main body of pink. These can be considered as a sort of guide lights on the runway for the visiting bees. The central core of the flower head, called the disk, is set in deep reds and brilliant yellows. The base of the inner circle holds the disk flowers which are scarlet in color. Rising out of the disk flowers are the anther tubes that hold the precious pollen which provides the bright yellows. Arising out of the exact middle of the aster is the stigma, and within this treasured location the sweet nectar is found. From a distance, the aster appeared as a singular color of pink, but this initial blush gives way to a wealth of colors, any of which could serve as a guide to bees that are busily visiting other flowers. As I straighten my back to stand up, a familiar buzz alerts me that a visitor is approaching the flower that I was inspecting. Glancing around, I spot the black and yellow markings of a bee which is slowly making its way toward the pink aster. Exhibiting a flight that seems to be haphazard at best, the bee, after initially circling the flower bed, begins its final approach to the pink aster. I imagine that the initial flight pattern around the flower bed is a sort of search behavior that allowed the bee to select the best flower to visit. Some cue is calling the bee to the aster with the pink petals with a yellow tinge at the end and a central core of red and yellow. The bee lands lightly on the pink outer petals and casually strolls toward the red core in search of the precious reward of nectar. Upon reaching the middle of the flower, the bee unfurls its curled tongue and begins to gather the sweet nectar. Of course, on its approach to the treasure in the middle of the flower, the bee had to

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walk through the forest of anthers and is now covered in pollen. This additional payload for the bee is to be carried off to another flower in hopes that floral reproduction will occur. This is a small price the bee pays to the flower for the meal. After drinking its fill from this flower, the bee takes off and renews its haphazard flight pattern in search of its next meal. Although the flying behavior of the bee appears to me as a sort of drunken movement in three dimensions, I know that the bee is using the visual patterns on the flowers as well as the aromas to make its selections on where to land. For this bee, the search doesn’t take long as it appears to spot a crocus close to the ground. This particular flower has deep purple petals that fade into a white center. As with the aster, at the heart of the flower are bright yellow stamens advertising a meal of pollen and nectar. As I watch the bee has begun its landing behavior. I glance up from the bee while it’s collecting pollen and nectar to take in the entire view of the garden one more time. This fall garden is in full bloom, and the colors, although somewhat muted compared to spring and summertime, are varied. The tallest and brightest flowers seem to be the sunflowers against a distant fence. I proceed toward the fence, and the majestic flowers have their faces pointed horizontally as the large bright yellow flowers are bent at right angles compared to the stem. Unlike the crocus and aster, the sunflower contains petals with a singular color of yellow which provides an obvious explanation for its moniker. I hear a slight buzz gaining in volume, and it appears as if our foraging bee has decided to follow me over to the sunflowers to sample their wares. I am not sure what draws the bee into this flower. All I see is almost a monochromatic yellow. Certainly, the petals are a slightly brighter shade of yellow than the middle, but the large “sun” portion of the flower seems homogeneous. Within that large circular part of the flower are disk florets in female and male phases, and the dense inner circle contains unopened florets. Despite my description of the flower, the bee has no problem homing in on the opened florets to feed for its final meal. While I see a garden rich in a diverse range of colors, these colors are my colors and not the bee’s. I know that the garden produces a very different visual landscape for my small companion. Where I see a pink aster, the bee envisions a black and white flower. When I examine the monochromatic sunflower, the bee sees a variety of shades all pointing toward the golden treasure of nectar and pollen.

3.2  The Science of the Bee’s Flowery Vision The pollinator’s view of the garden is different from my view of the garden because the bee (as well as a host of other insects) has the ability to detect ultraviolet radiation. As previously mentioned, the mnemonic device, Roy G.  Biv, listed out the order of colors from longer wavelengths (red, approximately 700  nm) to shorter wavelengths (violet, approximately 400 nm). Of course, this listing is biased because of the ability of humans to see these wavelengths, which have been appropriately called the visible spectrum, quite a human-centric name. In reality, Roy G. Biv lies

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within a much larger spectrum called the electromagnetic spectrum. The visible spectrum is a very small piece of the electromagnetic spectrum which includes radio and TV waves (1–10 m wavelengths), microwaves (1 cm), heat (100 μm), ultraviolet (50 nm), X-rays (1 nm), and gamma rays (0.1 nm). The earth is “illuminated” by this entire spectrum every day, but the human eyes are only sensitive to that little bit between red and violet. Within the basic construct of an eye (lens, retina, network), the bee’s adaptation lies within the photoreceptors of the retina. Most insects have three different photoreceptor pigments, similar to humans, but their sensitivities are shifted from our red, green, and blue to shorter wavelengths. The western honey bee (Apis mellifera) has pigments in their photoreceptors that are most sensitive to wavelengths in the range of 328, 436, and 532 nm (ultraviolet, violet, and green, respectively). This range of sensitivities is fairly common for trichromatic insects. Trichromatic means that the organism has three distinct pigments within the retina which include the human eyes. Some organisms (the common house fly and the Australian swallowtail butterfly) are pentachromatic (five pigments), while other organisms (marine mammals and the owl monkey) are monochromatic. These pigments are embedded in membrane layers within the retina. The actual photoreceptors of invertebrates are fundamentally different in design when compared to vertebrates. The details of these differences and how they lead to seeing the world differently is explained in the animal example that follows this one. In the example above with the asters and the honey bee, UV light is reflected from the aster through the bee’s lens and is focused on a photoreceptor with a certain pigment located in its membrane. When the light hits the pigment, the protein changes conformation and causes that photoreceptor to generate what is called a receptor potential. As more intense light within that wavelength hits the photoreceptors, more energy is absorbed and more pigment changes confirmation, increasing the strength of the receptor potential. If enough light is present, the receptor potential can increase in intensity to cause other neurons in the bee’s retina to fire and send information to the brain of the bee. This information is further processed, but, eventually, the bee will recognize the different colors of light based on what and how many photopigments are excited. Earlier in this chapter, I described how the bee (or butterfly or owl monkey) perceives a different set of colored flowers in our fall garden than you and I do. This is primarily due to the various distributions of pigments in the retina. Some wavelengths (e.g., red) are wonderfully seen by humans but are not detected by the bees. While other colors, the beautiful UV coloration of flowers, are easily seen by the bees (and their fellow insects). They are entirely missed by me as I walk through the garden. At this point, we can wonder what is the real nature of the garden in front of me. Is it the colorful earthy tones of fall that I perceive or the more subdued and darker colors that are present for the honey bees? Or is reality something that combines both the bees and my own perceptions of a garden that would be even more splendid? This visual reality likely exists in a sensory space which is out of reach for our senses and is something beyond what I or the bee can perceive (Fig. 3.1).

3.2  The Science of the Bee’s Flowery Vision Fig. 3.1  Flower petals under different light. The upper half of the drawing depicts the color scheme of a flower’s petals under UV vision, while the lower half displays the colors humans would see

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Chapter 4

Finding the Way Home

When I travel, whether to old or new locales, I like to go on “explores.” When I travel to a new place, whether it is urban or natural, one of the first activities that I enjoy doing is taking off just to explore my new surroundings. One problem with my explorations, at least in the urban environment, is that I have a great difficultly remembering street names. Having lived in the same small town for over 20 years, one would expect that I know the names of roads around my house. Sadly, I don’t. So, for giving driving directions in my home town or returning to my lodging in a new location, I use a series of landmarks to guide both my outward- and homeward-­ bound paths. Although there are no street names in natural settings, I use the same landmark navigation in the wilderness while adding in the location and direction of the sun to help me return home. Knowing the latitude of my current location, I can estimate either north or south from the location of the sun. Knowing the approximate time, I can estimate east or west as a general direction. I can quickly generate a rough map with my starting location by triangulating uniquely designed skyscrapers, elevated transit lines, or other structures within a city. Returning home is just a matter of recreating the spatial arrangement of those structures within my visual field. A recent 3-h sojourn across and around Sydney, Australia, was successfully accomplished by keeping the Bay Harbour Bridge to my north and understanding the spatial location of the different harbors. This navigational method is excellent but depends upon one key element: unique features within the environment. When I used to do oceanic work, my navigational method would have failed me when I was on several cruises. At a large enough distance from shore, the ocean horizon is essentially featureless, and the daytime sky is similarly not helpful. At present, exploring deep enough into a forest can also provide me with some problems. Although definitely not featureless, the lack of distinct and directionally spaced features can cause some mild disorientation during explorations. My reliance on visual features of the environment is limited to those habitats where I can connect a direction relative to my place of origin (hotel, car, or cabin) with a visual landmark that is more or less stationary. (Of course, a magnetic compass would © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_4

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allow me to maintain a constant direction if I wanted to navigate in the open ocean or deep forest). Many other animals utilize the visual navigational trick that I use: landmark orientation. Scientists have an excellent understanding of how animals perform these tasks. Most of these animals can create mental maps of the landscape with landmarks placed on those maps. But, what about those organisms that live in seemingly featureless environments such as a large portion of the world’s oceans (both above and below the surface) or in some of the largest deserts on the earth? For example, imagine that you are suddenly kidnapped and placed on a helicopter. Also, imagine that the helicopter lands in the middle of the Saharan desert and places a large flag which will be called home. Finally, the helicopter flies you 10 miles in some random direction. The pilot unceremoniously drops you off and tells you that she’ll be waiting at the home flag. If you successfully find that flag, she will return you to your previous life. Looking around, you would certainly notice sand dunes of various sizes and shapes, but nothing more. In addition, these sand dunes don’t have a set spatial location as the winds shift and move the dunes around you. Apparently, there aren’t any visual cues to produce a direction home. Certainly, you could watch the helicopter fly off and follow that direction. At some point, you would need some information (like a magnetic compass) that keeps you on the direction back to the flag. A difficult task indeed. This task is not too farfetched for a small little desert ant. The Saharan desert ant, Cataglyphis bicolor, lives in the quite inhospitable Saharan desert where temperatures can routinely climb above 50 °C. Living in burrows, these ants make foraging runs (literally runs because if they stop, they might succumb to the intense heat) where they search these featureless plains for prey arthropods that have died, likely due to overheating. Once they find a suitable meal, they typically head straight back to their burrow following a beeline home (or should it be antline?). The answer for these ants involves visual cues that are, literally right in front of, yet illusive, to our eyes. These cues are the polarized light in the sky and more will be explained after our trip into the ant’s world.

4.1  You Can Go Back Home Again The vast openness of the Saharan desert is bleak and foreboding. Despite the vast images that most people think of for the Saharan desert, most of the terrain is dominated by dark brown hamada which is hardened soil and rocky plateaus. Sprinkled across this landscape are small shrubs and bushes; that is the extent of plant life. Peering closely at the hardened soil, one can see small dots dug into the plateaus. These are the burrows of the desert ant. Under these harsh conditions, the burrows of these ants provide a refuge from the sweltering heat as the underground abode has a level of natural air conditioning. Desert ants are hardy individuals. Even still, if the animals spend too long outside of the burrow, the heat will mean certain death. Its food is located on the inhospitable plateaus above, and the pull of the outside

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draws the animal out into the heat. So, these ants must perform foraging runs that maintain a delicate balance between death from starvation and death from overheating. As the desert ant emerges from its burrow, stepping out into the intense sunshine, it begins the daily search for food. As soon as the first leg hits the hot sand, this ant won’t stop walking or searching until it has returned to this burrow. The treacherous foraging trips have been shaped by evolution and exquisitely tuned to the featureless and deadly desert. The surface temperature of the sand on this particular trip is currently 52 °C and will rise as the sun continues on to its apex. The ant seems to head off in a seemingly random direction but is using its antennae to detect faint smells that will indicate food. Given the vast emptiness of the desert, it is hard to imagine what the ant smells or sees that is worthwhile. On its trip, the ant will make the briefest of pauses and performs a 360° rotation while staring at the sky. Clearly, there must be something in the sky the ant sees that we are blind to. If we examined the bright desert sky, we would see a bright yellow ball of a sun and little else. No clouds, no stars hidden by the bright daylight, nor secret visual images can be seen within the desert sky with our eyes. After these rotations, the ant resumes its journey for the precious food. For this particular trip, the ant initially started walking in a westerly direction. (We know this because our technology would inform us of the direction.) The ant does not have or even need the cognitive ability to tell compass directions. After a few minutes, we can see why the ant went in this direction. The carcass of an arthropod (a grasshopper) lies on sand, probably a casualty of heat exhaustion. What is an unfortunate end for this animal is a bounty for the desert ant. The ant has used olfactory cues from the dead arthropod to locate the unpredictable source of nutrition. The two large antennae on the head of the animal are capable of sensing airborne and contact chemicals. Thus, the ant uses olfaction to navigate through its outbound foraging trip. After arriving to the carcass, the ant has made a successful outward trip. This is only half of the problem of foraging for the ant. Certainly, the location of food is important, but without the ability to return home, the ant will succumb to the same end as its food. What is unseen by any of our observations is that the ant contains a counter in its head that allows it to keep track of how far it has traveled. This trick is similar to the method used in orienteering competition to keep track of traveled distances. Orienteering is a competitive event where participants attempt to locate distant markers using only a compass and a map. By knowing the length of one’s stride and then counting strides, one can get a fairly accurate estimate of distance traveled. For the ant, distance traveled is important, but the length of foraging trips is based on location of food. This is unpredictable. The way home, which is critically important, is a combination of finding the right direction home and knowing the direct distance back to the burrow. The ant pauses to grab the grasshopper. As we watch, the ant begins to slowly turn. The turn is reminiscent of the rotations that it performed right after leaving its burrow. The ant turns in clockwise fashion for about 150° or, roughly, in the direction of where we might think the burrow is located. After performing its slow dance,

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the ant sets off in a straight line. Carrying the grasshopper with amazing strength and performing some unseen calculations, it starts its homeward journey. Amazingly, the ant does not deviate from this straight line path except for the occasional tuft of plants that have managed to emerge from the sands. Even after these small deviations, the ant returns to its line of direction, almost as if there is some invisible track in the sand. Maybe a better thought is that there is some invisible line between the ant and its home, and some machine in the burrow is slowly retracting the line, drawing the ant home. Strings and tracks are just metaphors, but there is no doubt that this ant knows exactly where the burrow is located within the featureless desert. As the ant approaches the burrow, there is a slight decrease in speed. Since the burrow is within sight, it is possible to see that the straight line traveled by the ant was off by just a degree or two. So, some type of correction is necessary. To do this, the ant begins touching its antennae to the ground attempting to detect possible chemical signals leading to the burrow. After a couple of antennae touches, the ant has sensed the burrow opening and heads right for it. The homeward path of the ant was only off by a couple of centimeters. A truly remarkable feat. Imaging the scenario that started off this chapter, while we would be lost and unable to return home, the ant would have no problem.

4.2  The Science of Seeing the Unseen The desert ant, Cataglyphis bicolor, has performed an amazing task by using visual signals that are available to it and are invisible to humans. The homing strategy of the ant, called path integration, is a simple calculation of what is called a “home vector.” If the ant knows the total distance traveled and creates (and updates) a home angle every time the animal turns, then a simple line can be drawn from its current location to its home burrow. The mathematics behind these calculations (distance and angular direction) are simple geometric equations. Yet, the ability of an ant to perform these simple calculations may seem difficult to believe given the computation power and size of its brain. Think, though, of the interesting and more difficult calculations that humans go through to catch something like a baseball or football thrown in their direction. To predict where a baseball, coming off a bat, or a football, thrown by a quarterback, will land and to calculate the speed at which one needs to run to be there when it lands requires advanced calculus. Despite this fact, many non-mathematicians (young kids and athletes) can perform these advanced calculations instantaneously to catch these flying objects. So, the ability of an ant to perform simple geometric calculations, vector math, in order to determine the exact distance to its home burrow seems less cognitively inspiring. Certainly, knowing the distance to a location, such as a burrow, is important, but probably more important is knowing the direction to a burrow. In many of my explorations in novel environments, I use landmarks (such as Sydney Harbour Bridge) to help guide directional decisions for me. Within deep forests or featureless oceanic settings, this method is not possible. Other methods could include the use of a

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­ agnetic compass. Using a compass allows someone to maintain a straight line m (relative to magnetic north) toward some location, like a car or home. The ants don’t have a magnetic compass but do have a visual compass they can see that is invisible to us. This compass relies on something called plane polarized light in the sky. So, what is plane polarized light? Light is a very interesting energy source as it travels both as particles and as waves. For the purpose of our navigating ant (or human), light can be considered a wave, and this wave has something called an e-vector. This e-vector vibrates in 360° in sunlight and many other light sources. To understand this, imagine that you are walking outside, down a city street. As you walk down the street, you pass three kids playing with jump ropes. The first child has tied one end of the jump rope to a tree and is holding the other end of the jump rope. As you walk by, the young child takes his hand and randomly moves it in multiple directions. The jump rope will create waves, but the waves will move in random directions in space. The movement of the jump rope is a simplified version of how the e-vector wave moves in natural light. The e-vector travels in all directions as the wave travels forward. As you continue your walk, you begin to approach the second child. This child has also tied one end of the jump rope to a tree and is holding the free end. As you approach her, she moves her hand up and down in a smooth motion. After a couple of hand movements, the jump rope begins to have a wave traveling back and forth from the child to the tree, but the wave moves only in the vertical direction. This is similar to the types of waves produced by athletes training with heavy ropes. This jump rope is an example of a plane polarized light. The e-vector (jump rope) has a waveform, but the waveform only vibrates in the vertical direction. This is the vertical component of the 360° from the first jump rope scenario. Finally, you approach the third child and she has the jump rope attached in a similar fashion as the first two children. As you walk by, she moves her hand in a horizontal direction. Her motion creates a wave very similar to the second child’s jump rope, but the wave is now moving in the horizontal direction. This is also an example of plane polarized light, but here, the e-vector would be moving in the horizontal direction or the horizontal component of the first child’s jump rope. Light from the sun is scattered by the small particles in our atmosphere similar to the randomly moved jump rope. Think of an old-school disco light that operates on an exceedingly small scale. This degree of scattering that occurs depends on the wavelength of light. Shorter wavelengths (blue and ultraviolet) are scattering more than longer wavelengths (red and infrared). The sky appears blue to us because blue light is scattered around in the atmosphere. As sunlight enters our atmosphere, the e-vector vibration is equally spread around a circle. This is called unpolarized. If this light were to reach our eyes, without scattering, we would see unpolarized light that has an e-vector vibrating in all directions. Because of the composition of our atmosphere (N2, O2, CO2, and other gases), sunlight is scattered, which causes some degree of polarization. If the scattering angles reach 90°, then the degree of polarization is 100%. This would be akin to either our second or third jump rope example from above. In our atmosphere, the polarization of light is less than 100% but greater than 0%. Still, what does this mean for a visual compass?

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Because our atmosphere scatters and creates polarized light, the sky actually has a spatially distinct e-vector. This means that different parts of the sky will have different angles and intensity of polarized light. If an animal could sense polarized light, then the sky could be a visual compass just like the magnetic patterns across the globe creates a magnetic compass. If we can’t see polarized light, how do ants? As noted previously, we can think of eyes as having three key components: the lens, the retina, and the processing network. Vertebrate eyes (which includes human eyes) have two different styles of photoreceptors: cones and rods. Cones are used for color vision, and rods are used for low light vision. The shape of the business end (light sensing) of the receptor is exactly as the name implies. Rods are long cylindrical rods that are transparent. Cones don’t quite come to a point at the end but are definitely canonical in shape and are equally transparent. Within the cones or rods lie a large number of pancake-shaped layers. Think of a flapjack breakfast for a huge gathering of friends. Embedded on both the top and bottom of each pancake are a number of proteins called opsins which are sensitive to incoming light. Light travels through the outer skin of the rod or cone and contacts these opsins, which eventually leads to the detection of light. Unlike the syrup poured on a large stack of pancakes, the light travels through these layers activating any opsins they contact, regardless of whether the opsins are located on the top pancake, bottom pancake, or any in between. An opsin has an orientation that makes it more sensitive to polarized light vibrating in a single plane. In most vertebrate eyes, the opsins are randomly aligned within the pancakes, which makes that cone or rod relatively insensitive to polarized light. To finalize our visualization of the vertebrate eye, all of these cones and rods share a single lens. Insects have very differently constructed eyes. The ants (and other insects) can see polarized light because of the way that the photoreceptor cells in the retina are constructed (Fig. 4.1). Anyone that has taken the time to glance at an insect’s eye (perhaps a dragonfly’s large pair of eyes) will have seen the large number of lenses pointing in a number of different directions. Because insects have multiple lenses within each of its two eyes, they are called compound eyes and each lens forms its own image of a small part of the external world. Each lens (and the underlying rest of that part of the eye) is called ommatidia and has all the same compounds that reside in our single lens eye: a lens, a set of photoreceptor cells with opsins, and neural networks. If we were to examine a single ommatidium, we would see why these desert ants can use polarized light. Imagine that a single ommatidium is pulled out of the eye for our examination. The single ommatidium would be a hexagonal-­ shaped rod that tapers at one end. The larger hexagonal part is where the lens is located. If we were to make a horizontal cut right below the lens of the ommatidia and open up the eye, we would see a structure that looks very similar to an orange cut in half along a line perpendicular to the wedges. The ant’s eye would have a number of wedges that narrow toward the center of the ommatidia. Each wedge is called a retinular cell and this cell is analogous to our photoreceptor cells. Unlike the pancake design in vertebrate eyes, the retinular cell has a very different design. The outer part of the cell (larger end of the wedge) is devoid of any receptor cells but has a series of “bristles” pointing toward the inner part of the cell

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Fig. 4.1  The inside of an insect eye. Inside the ommatidia of an eye with the hexagonal rods that run perpendicular to each other

like a hair brush. In fact, the construction of the entire ommatidia can be thought of as a set of four hair brushes with all the “bristles” pointing inward. Each brush is located 90° relative to the neighboring brushes. This means that the “bristles” are also 90° relative to the other “bristles.” The “bristles” serve the same function as the pancakes within the vertebrate eye. Each individual “bristle” is a tube which has opsins embedded in its surface, almost like the pancakes have been rolled into mini-­ tubes. Unlike the randomly oriented opsins in the vertebrate pancakes, the opsins within the ant’s “bristles” are all aligned and oriented along the long axis of the bristle. Because of this construction, the entire set of “bristles” on a hair brush are sensitive to polarized light in a single direction. Any light that has its polarized vector vibrating in any other direction does not stimulate these set of opsins. The receptor cells that have their “bristles” oriented 90° to this set are only sensitive to vibrations of polarized light along their long axis. Each ommatidium is sensitive to polarized light in two directions that are separated by 90°, because of the bristle and opsin alignment along the bristle. Thus, as a result of two design features, aligned opsins and directionally aligned “bristles” of photoreceptors, desert ants can detect the plane polarized light in the sky in an otherwise featureless sky. These ants carry with them a built-in visual compass that allows them to calibrate their homing direction. By viewing the sky with eyes sensi-

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tive to polarized light, the ants see a range of lightness and darkness that is a f­ unction of the polarized light being detected by directionally sensitive receptors. If the ant rotates in space, the sky’s polarized view stays constant. Just as if we were to hold a magnetic compass in our hand and rotate ourselves in a circle. The little red arrow of the magnetic compass always points toward magnetic north. In the ant’s world, the sky compass remains constant and can provide directional cues to the way home. On their outward journey, the ant has the ability to constantly monitor the direction of its walking by using the sky compass. As the animal moves through the desert, the ant is able to calculate and maintain a straight line vector back home by following the polarized light patterns in the sky. The ants will constantly update their home vector based on their continual reading of the changes in how the polarized light appears on their retina. Despite the invisibility of this compass to our eyes, it is omnipresent for the ants and serves as their beacon to home and safety.

Chapter 5

I Can See for Miles and Miles and Miles

In unfamiliar areas like new cities, using my phone as a GPS is an excellent way to get directions to my destination. Although I prefer my tried and true strategy of landmark navigation to orient myself, this mode of navigation by GPS requires either knowledge of the names of the local roads or clearly marked signage. As my GPS calls out the distance to and name of the next turn, I can get ready by searching the road signs for names. When traveling by car, there is a significant advantage gained by reading and seeing a sign far enough in advance so that any adjustments in speed or lane can be safely made. However, this process was much easier when I was younger when my eyesight was much better. Certainly, the acuity of my distance vision has decreased with age. The ability to detect differences at a distance is called visual acuity. To compensate for this loss in visual abilities, I wear glasses that help improve my ability to detect and read words from a distance. For humans, our best visual acuity occurs when the light from our visual landscape falls on a certain area within the eye called the fovea, which was touched on in Chap. 2. The fovea is the site on our retina that has the highest density of cones. Our eyes contain around 180,000 cones/mm2 (for reference, the thickness of your fingernails is roughly 1  mm). This density drops off considerably outside of the fovea and can be as low as 5000 cones/mm2 on the outside edges of your retina. This difference in cone density is why our peripheral vision is not very good for forming images and why we look directly at objects when we really want to form a detailed picture. By staring at a visual scene, most of the light is focused on our fovea and provides us the most detail detection of the image. My visual problem arises because the lens in my eye has changed shape with age and I have lost the ability to focus my visual world on the fovea. Visual acuity is defined as the spatial processing of the visual system, or in other words, how far apart objects need to be to be detected as two different objects. Of course, this measurement is distance dependent because light enters our eyes at various angles and is focused. To understand this process, imagine that you are sitting in your favorite restaurant finishing up a fabulous dinner. Glancing at the dessert

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menu, you see a delicious pie, raspberry rhubarb, and decide to order a slice or two. Imagine the waitress sets the pie slices down in front of you (with the crust away from you). One slice of pie is directly in front of your left eye and other is in front of your right eye. Your visual field is akin to that slice of pie. Now, imagine that you glance up and see two glasses of water on another table across the restaurant. Your fovea is at the point of the pie and any objects that overlap their positions on the pie slice are detected as a single object by your retina. This situation would occur if the glasses of water are very close to each other or if one glass is directly behind the other. If one of the glasses is on the left eye’s pie and the other is only on the right eye’s slice, then your eye detects them as two different objects. If you were to walk toward the table, both glasses can be located really close together but fall within two different visual fields (right eye vs left eye). You will detect two glasses of water. Walking far away from the table, both glasses can appear on a single eye’s pie slice. Closer to the crust end of our hypothetical pie, the two objects will be scene on the same slice of pie. If we are far enough away (far is really determined by our photoreceptor density), the glasses will merge and be detected as a single object. As the distance from the pointy end of the pie (our fovea) and the crust (our visual target) increases, the distance between these two objects needs to increase in order for us to detect them as two different objects. This is visual acuity, the ability to distinguish two objects as distinct. To continue the analogy, some animals have long thin slices of pie (better visual acuity), and others have short wide pieces of pie (poor visual acuity). What does all this mean for visual fields? If a person has 20/20 vision, they should be able to detect two objects roughly 2 mm apart (two fingernail widths) at a distance of six meters. Certainly, lighting conditions and many other factors determine whether someone can actually perform this well, but I certainly can’t without my glasses. For me, my decreased visual acuity means that I need to be closer to something before I can examine it visually. Although my glasses have helped, I rarely have to read something that is 2 mm apart from across the room. Yet, what if my life did indeed depend upon my ability to discern very small objects at very large distances? I can imagine a sailor’s life at sea, a hundred years ago, where the ability to detect potential landing spots from miles away could be important for survival. Maybe even the ability to see ships and determine whether they were pirates or other vessels from their flags would be a necessary skill. Perhaps crossing large open plains or deserts might call for the ability to find shelter or watering holes at quite a distance would be very helpful. Certainly, the use of modern technology to map unseen areas and store these maps for digital retrieval has made these keen visual abilities obsolete. Yet, what about the animal kingdom, where GPS systems don’t exist? Is there the need for exceptionally keen visual acuity to survive? Instead of needing to read the fine print labels on a box at the grocery store, what if I had to discern the location of a small prey item while soaring hundreds of feet in the air? This is the task faced by most raptor birds. Raptor birds, otherwise known as birds of prey, include eagles, hawks, falcons, vultures, and ospreys. Almost all these birds have keen vision, powerful talons, and sharp beaks. The size of the bird

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determines, in part, the size of the prey that can be attacked. Regardless of this ­relationship, most raptors are hunting smaller mammals scuttling along within brush that are often camouflaged to resemble the background foliage. This is a much more daunting, and important, task than reading the fine print on a can of peas at the grocery store. Imagine attempting to read that fine print on the can of peas from a couple hundred feet away, while the can is under 3 ft of water. Replace the can of peas with a bass, and this would describe the hunting challenge that faces an osprey.

5.1  I Spy with My Little Eye Something Osprey, Pandion haliaetus, are a cosmopolitan bird. When attached to animals or plants, cosmopolitan means that the organisms are found worldwide. The number one environment feature that osprey want is water. Bays, rivers, lakes, and wetlands are all suitable places where ospreys will nest. Water is a requirement because their primary source of food is fish. Ospreys are not very finicky with their meals either. If it has scales and swims, then it is a potential food source. So, a sunny day spent near open water is a good opportunity to see these birds with the exquisite eyes hunting. On a warm and bright mid-day, we head to the shore of the local lake and begin to slowly motor around the relatively shallow parts. Leaning over the boat and peering beneath the surface, small fish, plants, and perhaps even snails and mussels can be seen. Near the shore, pines or other trees provide additional shade, which can enhance our ability to see what is beneath our boat. When the boat travels out deeper, our ability to see the bottom of the lake or even fish moving beneath the surface quickly disappears. On calm days, we might be able to see a little deeper, but even the smallest of breezes creates ripples or waves that disrupt our depth perception. On top of all of those obstacles, we could only be a few feet above the water when our ability to see fish leaves us. The object of our quest, the osprey, begins its hunt at great heights in all types of weather. All of a sudden, a shrill chirping fills the air, which is a sure sign that our guest is here to entertain us. Looking up from the lake into the clear sky, we attempt to locate the source of the sounds. After a couple of other chirps, we both locate the source and see a beautiful osprey majestically flying through the air. Having just cleared the tops of the tallest pine trees approaching the lake, the osprey rises in the air to soar a hundred meters  above the lake. The white head and brown feathers stand out against the blue sky. We watch in anticipation for a hunt and hopefully, our guest will provide us with a visual feast. The osprey is not a deep diving bird. Other hunting birds, like cormorants, gannets, or even shearwaters, are far better adapted to chasing or even swimming underwater to attain their prey. Staying near the surface, the osprey has to ensure that the first strike is true, or else the meal will be lost. A typical maximum dive for the osprey is around 1 m in depth. As such, the osprey tends to focus its visual search on the shallower parts of lakes. The osprey we are watching has decided to cross the

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lake toward our boat to search for any unsuspecting fish hanging out near the shore. A focused examination of its head will show its approach to hunting. Using a much more fine-tuned visual acuity, the osprey searches for movement on the bottom of the lake. The bird has intense flying speed which can peak at 120 kph. Initial aspects of the search can be done at high speeds, but even with its impressive eye, this bird needs to slow on its approach to the kill. The osprey, by shifting its head back and forth, is scanning left and right as it stays high in the air in hopes of seeing a potential lunch. The high visual acuity of the osprey comes at a cost and that is the need for brighter, sunnier days to hunt. Lower light levels would simply not work because the osprey’s eye is densely packed with visual receptors. Given that this day is quite bright, the osprey should have an easy time finding prey in this abundant lake. Changes in the bird’s flight pattern and a subtle slowing of its speed is a clear sign that a prey has been spotted. The great vision of the osprey, along with the ability to accurately judge distances, has allowed this animal to set up a fierce attack run. Given these visual abilities, perhaps we should replace the phrase “eagle eyed” with “osprey eyed,” although the latter one is quite a bit more awkward to say. The osprey puts in a couple more wing beats before it lines up the attack run. The osprey has now slowed down and stopped flapping its wings as to glide. The eyes have focused on the bottom of the lake, indicating that the bird has definitely found something. Its head remains stationary, and both eyes are focused on the fish. So much so, one could draw a straight line from the tail through the beak and right to the fish. As the bird locks in the targeting parameters for the fish, the osprey will switch from a glide to a headfirst dive, initiating its attack. The osprey has begun to attack as it begins its dive. Counterintuitively, the wings stay unfurled. The osprey attacks over water and, unlike hawks, won’t land to take the prey. So, the wings stay open to control the descent and to begin a quick climb after snatching its prey. Despite the wings, its beak is aimed right at the prey and the feet are held back to become as aerodynamic as possible. The osprey drops at an amazing speed. As mentioned above, the wings are held parallel with the body during the steepest part of the dive. During the osprey’s approach to the water’s surface, the tremendous vision coupled with quick calculations of distance and speed, the bird knows exactly how far the lake and the fish are from its current and rapidly changing position. On the final descent to the water’s surface, the hunter opens its talons for the first and final strike. Right at the last second, the osprey brings talons forward, almost directly next to its beak. The bird is directly above the lake’s surface. Its talons are wide open, and its feet are directly in front of its beak. In an instant, right through the surface of the water and onto its prey, the talons find their mark. Pulling upward, the osprey was successful and captured a large bass. Immediately, lifting skyward, the osprey flaps its wings and climbs through the air. Its legs are back in flight position with the prey firmly grasped in the talons. After a little height is gained, the bird will shake off the water just like a dog shakes after getting wet. It was a successful catch and beautiful display of accuracy and precision striking, even from 20 to 30 m in the air.

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5.2  The Science of Precision Talon Strikes The ability of the osprey’s precise aerial strikes is a result of four very specific adaptations: depth perception, high flicker fusion rates, increased visual acuity, and large eyes. Together these adaptations give the osprey’s visual system the ability to detect and identify objects from great distances and through layers of light absorbing water. Most raptors, or birds of prey, have similar adaptations as the osprey’s visual system. Thus, much of the following can be generalized across hawks, eagles, and falcons. Ospreys, because of their excellent visual system, are some of the best fishing animals in the world, and their catch rate can vary anywhere from 25% up to as high as 70%. That rate is certainly something to think about the next time out on a lake and casting a rod in the water. The first adaptation, depth perception, is a fairly common adaptation across the vertebrate animal spectrum. Depth perception is the ability to determine the relative distances between objects in a visual field including the organism itself. Depth perception is critical in organisms that run, swim, or fly at high speeds and is the difference between a two-dimensional and three-dimensional visual world. Moving quickly through a dense forest without good depth perception would be quite hazardous to one’s health. Each eye of any organism has a visual field. The visual field consists of a cone shape radiating outward from the lens of the eye. An object or movement within that cone is detected and processed by that particular eye. Many animals, particularly smaller prey animals, have monocular vision. This is a situation where the visual fields project out sideways from the animal and the visual fields do not overlap. Most fish have monocular vision due to the location of the eyes on the sides of their body. The advantage of this configuration is that since the visual fields do not overlap, each singular eye (and its visual field) covers a larger and unique area of the surrounding environment. Movement (such as from a predator) can be detected from a larger area which gives the animal an increased chance of escaping. Conversely, predatory mammals, many birds of prey, and of course humans have evolved to where the eyes are no longer on the sides of the head but are moved forward such that both eyes are essentially looking ahead of the animal. The forward placement of the eyes causes the visual fields (cone shapes) of each eye to overlap. While this forward placement provides the animal with less visual detection of the entire environment, the overlapping section provides the animal with binocular vision. Within this overlapping area, an object is perceived by both eyes, but the relative placements of the background and the object are different. A simple test can demonstrate this. Stare at an object in the room that is approximately halfway between you and some steady background (a wall, tree, or some other stationary object). Now, close your left eye and notice the distance between the object of interest and your steady background. Switch which eye is closed (close your right and open your left eye) and notice how the distance between the object and the background has changed. This is due to the angle between your open eye, the object, and the background. If there is a large distance between the object and the background,

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then the spatial change as you switch which eye is opened will be greater. Conversely, the closer the object is to the background, the smaller this spatial change will be. This difference between the left and right visual fields allows an organism to detect the relative distances between objects and creates a three-dimensional view of the world. Ospreys and other birds of prey have forward looking eyes with a large overlap in visual fields which gives them excellent depth perception. Besides depth perception, ospreys have higher flicker fusion rates, especially compared to humans. Flicker fusion rate is defined as the frequency at which the display of separate images appears to be a continuous motion. An elegant example of flicker fusion rates are the old stop-motion cartoons drawn on consecutive pieces of papers. Imagine a drawing of a stick figure walking across a page from right to left on a stack of one hundred pieces of paper. Each individual page has a single image of the stick figure at some location on the page. If you “flip” through these pages rather slowly, the stack of 100 images will appear as 100 separate images, and there will be no “motion” seen in our stick figure. Flip through the pages fast enough, the stick figure will come alive and steadily walk across the page of papers as if in a movie. This analogy is especially appropriate because even modern movies are a series of single images shown fast enough that the appearance of seamless motion picture is perceived. For humans, flicker fusion rates are approximately 50–60 hertz (Hz). Hertz is a unit of measure that would be frames per second. Think of the old childhood game of drawing stick figures on a pad of sticky notes and then flipping through the cartoon. If you flip the pages slowly (lower hertz or pages per second), the stick figure appears as separate drawings. Flip the pages faster (by increasing the hertz), and you’ll be watching a little cartoon movie. This means that images flashed across our visual field slower than 50 Hz will flicker and appear to be a sequence of single images. Think of watching someone dance using a strobe light. The perception of the scene is a series of single body positions visible when the strobe is on. Yet, when the strobe is off, the motion that creates the different body positions is lost. Conversely, showing images faster than 60 Hz will produce a movie or continuous motion effect. If motion appears fast enough (as in race cars, airplanes, or even the pitch of a baseball), then individual movement is lost, and the image becomes a blur. For the osprey, a very slow flicker fusion rate means that the prey (some 40 m away) will jump or move between positions which would inhibit the precise nature of the aerial strike. Thus, raptors have flicker fusion rates that hover around 100 Hz or about twice that of humans. These higher flicker fusion rates allow the osprey (and other raptors) to track the location of the prey at a higher rate. Changes in attack angles or attack locations can be made more continuously on a much smaller scale which increases the overall success rate of very long attack flights. The next two adaptations (higher spatial acuity and large eyes) are connected in that the larger eyes compensate for lost visual sensitivity due to the higher spatial acuity. As stated above, the highest visual acuity is located in the fovea of the eyes. The fovea can be thought of as the focal point of the lens and contains the highest density of photoreceptor cells. As light passes through the lens, the shape and composition of the lens serves to focus essentially parallel rays of light onto a singular

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point on the retina, just like the hand lens of a magnifying glass can be used to focus sunlight onto a single point. The number of receptor cells located at this point determines the visual acuity of the organism (or determines the minimum distance two objects need to be spaced apart to be considered two distinct objects). Increasing the density of receptors means that each individual receptor gathers information from a smaller slice of pie of the visual world (which increases visual acuity). Again, humans have around 200,000 receptors/mm2 in the fovea. Estimates for the density of receptor cells in raptors are difficult to perform, but several reports have estimated that raptors can contain up to 1 million receptors/mm2 in their fovea. This is a fivefold increase in density and acuity over the human eye. Yet, this is only part of the story (Fig. 5.1). Raptors have two other adaptations as regards to their fovea that increases visual acuity. First, they have a second fovea, in the lateral regions of the retina, which increases the acuity of their peripheral vision. Second, raptor eyes have a structure called the pectin oculi. This is a highly vascularized structure that serves to provide nutrients to the retina and maintain the ionic nature of the fluid between the lens and the retina. So, a second fovea produces better image forming peripheral vision and a special structure that feeds and maintains all of these dense photoreceptors ensures that these eyes are operating at their peak efficiency. The downside of having dense photoreceptors, high flicker fusion rates, and excellent visual acuity is the loss of sensitivity. Increased visual acuity means that individual or a very small group of receptors are responsible for sending information to the brain about the visual field. As mentioned earlier, visual sensitivity to low light situations is improved when the light intensity is combined or summed across

Fig. 5.1  Human and raptor eyes. The upper diagram is an outline of the human retina and lens, while the lower drawing depicts the elongated lens and retina of the much higher acuity eye of raptors

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a large number of receptor cells. Yet, this summing eliminates the individuality of the image sent to the brain by photoreceptors. So, increasing visual acuity means a loss in light sensitivity, and increasing light sensitivity results in a loss of visual acuity. Turns out that an eye just can’t do both. One adaptation, seen across many different animals, for the increased detection of light is the construction of large eyes. Nocturnal animals, such as the owl or the tarsier, or deep oceanic animals, such as the giant squid, have evolved larger eyes to capture as much light as possible. Diurnal raptors, such as our osprey, eagles, or hawks, have eyes that are larger than expected for their body size up to 50% larger than a mammal of comparable size. This increased eye size allows for more light to enter the lens and strike the retina to produce visual images. Thus, the osprey eye is large, able to see a small-scale and a three-dimensional world, moving at high speeds with sharp visual acuity. All of these spectacular adaptations produce an eye that provides the raptors (and in particular the osprey) the ability to discern and locate prey that could be hidden beneath dense underbrush or layers of water in oceans or lakes. This would be akin to a human strapping on a pair of high-powered binoculars and speeding across the lake at 90 kph looking for minnows in the shallows. Luckily for us, ospreys and other raptors are more focused on smaller mammals, so we have very little to fear from these farsighted predators.

Chapter 6

Peering into the Darkness

My favorite research organism is the crayfish. This animal has a wide range of interesting behaviors, and their aggressive interactions are far more entertaining than anything seen on nature shows. Crayfish, and generally most crustaceans, seem to always be in a fighting mood. So, they are excellent models to study social and fighting behaviors. The reason I chose to start working on crayfish was the immense role that chemical signals play in crayfish behavior. These animals use chemicals to make just about every decision that an animal needs to make. Hunting, fighting, and avoiding predators all depend on a suite of chemicals put forward either by themselves, their opponents, predators, or prey. Mating and finding shelter are also heavily guided and influenced by subtle chemicals in the lakes and streams in which crayfish are found. Instead of using daylight, these tremendous chemical detection capabilities give them the ability to extract environmental information in the absence of light. Their “noses” are as superior to dogs as dogs’ noses are to our own olfactory sense. Often found in the depths of lakes, in various rivers, or even wetlands, the availability of light to detect objects in their environment is often limited. Obstacles in the water, such as heavy plant growth, downed branches and logs, or even silt and sand can make the use of light nearly impossible. If the crayfish live in a lake, light penetration can be limited, and the bottom of a lake can be quite dark, even in shallow areas. Thus, the use of chemical signals is an ideal way to go about one’s nightly activities. Despite all these advantages as a research organism, one of the disadvantages of using crayfish as a research model is that I have to go out at night to either observe their behavior or collect large numbers of organisms for research purposes. Working primarily in the Midwest of the United States, my lab and I typically head out around 11:00  pm to one of the local lakes or rivers for collections or research. Besides delaying our sleep, the lack of light is a severe detriment to any research or collecting activities. Our eyes are perfectly adapted to work during the diurnal hours under a vast array of lighting conditions, but at night, we are literally lost unless we create our own artificial light. Driving to our sampling locations, we have the h­ eadlights on our cars that light our way. Even then, everyone in the vehicle, especially the person © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_6

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in the passenger seat, is on high alert for the random deer, skunk, porcupine, or bear that may quickly emerge onto the road. When we get to our sampling location, we can use headlamps to make our way through forests to the water’s edge, and finally, once in the water, we can use underwater flashlights to spot and locate the different crayfish species we need. In our region, the crayfish appear to be far more active during new, rather than full, moons. The absolute darkness that occurs during a new moon in the wilderness makes our hunting task even more difficult. Of course, we aren’t the only hunters out during these nighttime hours. Within the same areas where we hunt our crayfish, we are sharing the night with raccoons, porcupines, does, wolves, and owls. They have no need of headlamps and flashlights to see enough to find and capture food. Unlike us, our fellow companions of the night have special adaptations that allow them to move around, hunt, and forage during the darkest of nights. One of the most common adaptations that nocturnal animals possess is exceptionally large eyes. The tarsier, mentioned previously, has large eyes. In fact, related to its body size, the tarsier’s eyes are the largest of any animal in the world. Each eye, approximately 16–18 mm in diameter, is around the same size as its brain. For comparison, the human brain is around 140 mm in diameter. If our eyes had a similar eye to brain size as the tarsier, each eye would be six times larger than their current size or about the size of a tennis ball. The larger eye allows more light into the lens to be focused on the retina, just as a photographer would open the aperture of a camera to take pictures under low-light conditions. Although the tarsier is an extreme case of this, most nocturnal animals have larger eyes than their diurnal cousins. Large eyes, while beneficial for night time vision, do come at a cost, which will be covered later in this chapter. One of my favorite nocturnal hunters can be considered the ninjas of the deciduous forest. The owl is a predator that hunts on the wing and flies silently through the forest hunting small terrestrial mammals scurrying along in the underbrush. The wings of owls have special feathers that allow them to fly almost completely silently. The leading edge of the feathers have structures called hooks and bows that break up turbulent air as it moves over the wing. The trailing edge has flexible structures that serve to absorb this turbulence which dampens the characteristic sounds produced by air flowing over wings. Flying silently is useless unless the owl can see both their prey and the maze of branches that inhabit its hunting territory. This is where a spectacular set of visual adaptations allows the owl to be such an effective hunter. If we were to put away our artificial lights and attempt to catch our crayfish on moonless nights, we would be facing the same challenges as the owl.

6.1  Seeing in the Absence of Light Although walking through the woods at midnight might be a nightmare to some, this is the best way to see the silent hunter at work. A quick walk deep into the dark woods is the best place to see our next creature. The barred owl, Strix varia, is a

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nighttime hunter found in the dense forests of the Midwest of the United States. On the search for an owl at night, using red lights or no lights at all allows our own poor night vision to adapt to the low-light conditions without alerting the owl. This “dark adaptation” enables our eyes to be tuned to the low levels of background light. Despite our limited nighttime capabilities, our eyes have an amazing ability to detect light over nine orders of magnitude: from the brightest days to the dimmest nights. Unfortunately, our eyes can only detect about three orders of magnitude at any one time. So, our eyes can either dark adapt (going from a brightly light outdoors scene to a dark movie theater) or light adapt (reversing the trek listed above). Once our eyes have adjusted, we see a typically dense deciduous forest. Oak, maple, and aspen trees are intertwined with red and white pines. The forest floor is cluttered with last year’s leaves, broken twigs, fallen trees, and ferns. Even with our dark-­ adapted eyes, the current light levels would only allow us to see objects that we may stumble into. Reaching the pre-designated spot, waiting for the appearance of an owl is a patient game. This area, a fairly undisturbed second growth forest, is a known territory for the barred owl. A beautiful bird, the feathers, and darkened stripes, from which its name is derived, can range from a brown to gray and even a whitish color. A rustling in the leaves will tell us a potential prey item (mouse or vole) is near, but the owl’s hearing is far more sensitive. Coupled with its vision, any small mammal that wants to forage at nights with owls present is in for trouble. With our eyes having fully adjusted to the darkness of the forest, a distant darkened shape can be seen about 10 m up in a distant oak tree. The barred owl majestically sits and waits for any telltale sign of food walking around on the forest floor. Peering the darkness, I can just make out that the upper part of the bird swiveling to the left and the right. Seems like the owl is searching. If we had night-vision goggles, we might be able to see what the owl sees. Images received from night-vision goggles are often green because human vision has the most sensitivity within the green spectrum. Our goggles might allow us a small glimpse into the owl’s visual field, but the coloration of the objects for the owl would be very different. Although dimmed, the owl sees an enhanced picture of the world at night, unlike the gray or black and white of our nightly world. By turning its head, the owl keeps both of its eyes pointing in the same direction as its ears. Almost like a periscope with a radar attached, the owl is scanning its hunting grounds for both sound and visual images. The owl’s head continues to move slowly back and forth. Very small turns of the head means that the animal is fine-tuning the location of the sound and will quickly switch its search to its eyes shortly. As the owl’s head freezes, it appears to have clearly spotted something. Extend an imaginary line from the animal’s large eyes to the forest floor, a spot about 15 m away seems to have gathered the owl’s attention. I can imagine that the owl can see this spot clearly, but we would see nothing but darkened blobs of leaves, branches, and potential prey items. The head of the barred owl has not moved at all, indicating that the hunter has locked onto to something moving among the leaves. The small sounds of a scurrying animal finally reach our ears. We’ll have to wait for the owl to take flight and

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we’ll use its flight path to guide us to the unknown location of the would-be prey. When the owl has determined the exact location of the prey, it slowly unfurls its wings and gently lifts off the branch. We see the distant owl move but hear nothing. It is gliding silently through the dense branches of the forest. Even when we see the wing beats, we hear nothing from the silent bird. After a couple of wing beats, the owl does a slight course correction and banks noiselessly to the left. The owl must feel it is getting closer because it has stopped its wing beats and switched over to simply gliding down to the forest floor. We still cannot see what has gathered the attention of the owl, but the hunt is on, regardless of our own poor vision. The hunter knows the location of its prey. Like a fixed wing glider, the owl descends toward its victim. Everything is motionless as it flies straight toward the unsuspecting prey. Since it took flight, the owl’s head did not move at all. The eyes are glued on the target and will remain so until after the attack. Because of the darkness and the silent approach of the owl, the poor prey has no idea of the danger that is rapidly approaching from above. Subtle changes in the owl’s posture and wing position indicate a change from flight to strike. The wings are opening up to slow the descent of the animal, and at the same time, the talons rise upward. Opening wide, the sharp claws of the bird are readily apparent. As the end of the hunt approaches, the predator has changed its body position from an aerodynamic horizontal to almost a vertical position. The talons are poised and ready for the final strike. Even in this darkness, we can see the changing shape of the owl as it quickly approaches the forest floor. The entire body is in attack position, and as the owl closes the final distance to the prey, the talons quickly close around the small animal. The final strike was viscous and fast. The prey never heard or saw any threat, and yet, the barred owl was aware of its prey during the entire flight. After the attack, the owl quickly flaps its wings to gain altitude. Between its talons lies a mouse that will serve as its meal. The owl leaves the scene just as quietly as it hunted and is probably off to its nest to consume its prey.

6.2  The Science of Nighttime Vision Since we are diurnal animals, most of us are unaware of just how active nature is during the night. A walk through the woods, a field, or even a late-night swim would provide a glimpse, both literally and figuratively, into nature functioning in the absence of light. Truly one of the great hunters of the night, owls are exquisite examples of animals adapted to hunting in light conditions such as these. Just like the osprey in the previous chapter, owls have a number of different adaptations to their visual system that allow them to effectively forage. For the osprey, those adaptations were brightly lit conditions, but the owl can hunt as effectively even under the darkest of nights. As with the osprey, some of the owl’s adaptations have other costs associated with them, so the interplay of adaptation and compensation is interesting to note. When

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Fig. 6.1  Owl tapetum lucidum. Owls have an elongated retina that is lined with a silvery layer (tapetum lucidum) that reflects the light back across the receptor cells increasing their night vision

examining the owl’s ability to perceive prey under dim lights, three different adaptations stand out: enlarged eyes, a greater density of rods (low-light photoreceptors), and a special reflective layer called the tapetum lucidum (Fig. 6.1). Earlier in this chapter, the tarsier was used as an example of a nocturnal organism that has evolved large eyes. In a similar (but less extreme) fashion, owls have evolved larger eyes and pupils that can open to a larger dimension than what would be expected for the size of the animal. The larger eyes create a greater opportunity to capture more light under darken or dimmed conditions as explained above. Yet, this isn’t the only adaptation owls have. Unlike our eyes, which can be thought of as roughly spherical balls, the eyes of owls are more tubular in shape. The tube shape allows for a larger lens and pupil (which improves sensitivity at low-light conditions) to fit within the head of the owl and maintains the appropriate focal length which improves resolution. These two functional abilities need to go hand-in-hand for the owl. Larger lens and pupils are needed for low-light sensitivity, but the overall size of the lens and pupil is restricted based on the size of the owl’s head. To solve this problem (larger eyes, smaller head), the retina is placed farther away to allow the high resolution that is necessary for hunting small mammals in a forest. Despite the overall difference in body and head size, the eyes of owls are roughly equal in size to our human eyes. The downside of large eyes and tubular shape is that the eye is not moveable. As any parent of a teenager knows, human eyes have the amazing ability to roll around in their head without the head moving. This allows us to focus our visual field up, down, left, and right without moving our heads. The owl’s relatively larger eyes are immobile, so they have compensated for this immovability by having an amazing ability to rotate their heads. Owls can turn their heads an incredible 270° to survey their visual environment. For humans (180° max), we can easily focus on an object by “looking sideways” at it, but owls always directly face the objects they want to focus on. The second adaptation involves the relative distribution of cones and rods within the retina. As discussed previously, cones are the photoreceptors used for color vision, and rods are the photoreceptors designed for low-light detection. While rods

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are the dominant receptor type in most vertebrates, the density of the rods to cones changes among diurnal and nocturnal animals. In some diurnal birds, the ratio of rods to cones can even be less than one indicating that cones are more numerous than rods. Diurnal birds with such ratios would have excellent color vision but have really poor night vision. Conversely, some nocturnal birds can have ratios as high as 100 rods for every single cone which would greatly increase the ability to see under low-light conditions. In particular, these nocturnal birds tend to have very densely packed rods which further enhance nighttime visual capabilities. The barred owl has a ratio of 35 rods for every cone within its retina. This heightened ratio allows owls to detect and form images at much lower light levels than their diurnal relatives. The final adaptation present within the owl’s eye should be quite familiar to anyone who has a pet cat. House cats are descendants of the hunting cats of the wild, like lions and tigers. A significant portion of these predators are nocturnal hunters and face many of the same hunting challenges as owls. As such, these ancestral cats have passed along a specific trait to our pet cats, and this trait is quite evident when taking a photograph of a cat. Often in these pictures, the cat’s eyes have a reflective glare. The same phenomenon occurs when attempting to photograph owls. This glare is a result of a reflective structure at the rear of the retina called the tapetum lucidum. As a side note, one can identify animals at night by the color of the “glow” of their eyes due to this structure. As light enters the eye, the lens focuses the rays onto specific parts of the retina, particularly the photoreceptor cells. As previously noted, these cells come in two shapes (rods and cones), but for low-light vision, the cones are the receptors being used. In the cone section, there are stacks of pancake-­ shaped membranes that contain the opsins that respond to the light. After light is focused and aimed at the photoreceptors by the lens, a significant portion of the light passes through the outer membranes of the photoreceptors and is absorbed by the opsins. The light that is not absorbed by the opsins on the outermost pancake passes through to the next pancake. Some light travels through all of the opsin-covered pancakes and never gets absorbed by anything in the photoreceptor cells. In human eyes, this light hits the back of the retina and is absorbed without activating any of the opsins. So, this light is lost. For owls (and cats), the light that passes through all of the densely packed photoreceptors without getting absorbed bounces off of the tapetum lucidum like a mirror and travels back through the photoreceptors. This gives the opsins a second chance to absorb and detect the light. The reflective surface effectively increases the visual capabilities of owls in low light by capturing additional light that is lost for diurnal hunters. The reflective glare that becomes apparent when photographing cats and owls is this reflective light that has bounced off the tapetum lucidum and is traveling outward from the animal’s eyes. Taken together, these three adaptations (recall: large eyes on a swiveling head, higher ratio of rods over cones, and a reflective membrane) provide the owl with a visual system that makes it an exceptionally effective nocturnal hunter. With these adaptations, flying through a midnight forest, avoiding branches, while in search of mammals, and running through the brush become an easy task. Our eyes, placed in similar conditions, would have us bumping into branches and tripping over roots on the forest floor. The midnight world of the deciduous forest is only available to us if we light up the night with our own artificial sources.

Chapter 7

Technicolor Dreamcoats

More than just about any other animal, we like to decorate ourselves. Our coverings (clothes) are more than just functional to us. The selection of style, color, and even fabric is used to send messages about who we are. Clothes are used to signal group membership, and t-shirts can be used as walking billboards for companies or causes. These selections (either by free will or by dress codes) are designed by cultural norms to express ideas of maturity, creativity, or individuality. Walking through large metropolitan areas, those individuals working within certain business cultures (say, corporate world) can be seen by identical suit styles among the men and women. Subdued colors such as blues, blacks, and grays dominate the visual landscape. Splashes of colors are only seen with the occasional scarf or tie. Within the artistic centers of cities, the opposite is true. Individuality and expressiveness dominate, as the style of clothing varies as much as the coloring itself. Within sporting cultures, kits and jerseys, along with their associated colors, indicate inclusion as a fan or player. The red and blue of Barcelona, the pinstripes of the Yankees, and the black leaf of New Zealand signify a group membership for elite athletic teams. Unlike other animals, we can drastically change our appearance at a moment’s notice. The business woman, who returns home from work wearing a gray suit with a bright red scarf, can quickly change her appearance by swapping her daytime clothes for a complete Manchester United kit. In doing so, she has transformed herself from corporate membership to football membership. It is true that animals can change plumage or fur colors depending on the season. Other organisms, such as the famous chameleon and equally dazzling cuttlefish, can alter their outward appearance quite impressively, but are limited in range of these changes compared to our clothing options. Within these decorative additions or changes, color plays a central role. It’s the color of an object that contains the messages of identification more so than the shape or size of the object. A Real Madrid fan can easily spot the rival Barca fan by the red and blue stripes whether those stripes exist as a full kit, face paint, or simple patch on the breast of a t-shirt. The color of the “M” is a better indicator of a team © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_7

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for Maryland, Michigan, Minnesota, and Miami (of Ohio) in American college football. Outside of our cultural experience, color is central to our decision-making. The color of a banana is used to determine ripeness, the color of a patient’s face can determine wellness, and the redness of meat will provide information about the age. We are entranced by the colorful world so much that even our technology reflects the importance of color to us. Modern TVs boast an ability to project a 4K image with over 1 billion different colors. One company has trademarked their own version of the spectrum as if they created something unique. Some estimates of our ability to differentiate colors place that number to be around the seven million mark; however, I wouldn’t put much stock in that number as it has yet to be verified experimentally in a controlled fashion. In addition, the ability to differentiate colors is different than the ability to recognize colors. To differentiate something in a psychological experiment is simply to determine that color A is not the same as color B. To label, recognize, and use these colors to carry distinctive messages is an entirely more complex issue. Still, if we functionally operate under the concept that seven million colors is reasonable, this number is amazing given that we only have three pigments. The sensitivity of these pigments to different colors is a graded response. This means that the receptors for these colors aren’t turned on and off once a color is presented. The receptor slowly increases its response to the peak sensitivity as the color is slowly changed. Thus, the different and graded responses of receptors with our three pigments give us the ability to see many more colors than just three. We tend to believe that the colors we see are real and true, but they are only real to us because of the number of pigments we have. An excellent example of the illusions that our senses create for us can be demonstrated by comparing the visual world of animals with varying numbers of pigments. Imagine a world where stop lights have no color. The confusion that would arise from drivers might cause some considerable number of accidents. We might be able to manage with some of the traditional designs with three vertical lights, but what about singular blinking lights? This is the world of people with red-green color blindness. Even something as simple as picking up your favorite apple from the grocery store becomes a challenge. How do you tell the difference between a green Granny Smith apple and a Red Delicious? For these people, reds and greens simply don’t exist. Moving outside of the human realm, dogs only have two pigments and as such their color world is quite different from our own. Across the animal kingdom, animals (just like the bees of Chap. 3) have the ability to see a colorful world quite differently than our own. We think that our three pigments display the world quite nicely because that is only world we know. So, while having a TV that displays 1 billion colors may be interesting or a show of your wealth, the additional 993  million colors (beyond our 7  million that we might be able to see) are quite useless. However, there is an animal that might be able to use that TV. This animal is the champion of the color world in both vision and appearance. Stomatopods (or mantis shrimp) are a benthic marine crustacean often found in and around coral reefs. A diverse array of organisms, the mantis shrimp are known throughout the aquaculture world as a beautiful, yet frustrating,

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organism to keep within aquaria. The name mantis comes from the appearance of its front legs, which they hold folded and in front of themselves, as well as their quick strike abilities. In the terrestrial world, praying mantids are the world champions in speed of their strike. Keeping their arms fold in a praying position, they remain stationary until an unsuspecting insect ventures near. In one of the fastest reaction times ever recorded, they quickly unfold their arms, strike out to kill the insect, and draw it back in to their mouthparts. Stomatopods behave in an identical fashion. Unlike the mantids, the stomatopods have diversified the ends of their arms to different types of weapons. Most have hardened balls at the end of their arms which can deliver crushing blows to prey, enemies, and the glass of aquariums. The latter one leads to broken glass, water, and animals all over the aquarist floor. Some mantids (shrimp) have adapted their arms into spears in which they pierce their prey. All this is done at amazing speeds and with immense power behind the attacks. With such weaponry and brutality available to these animals, it is no wonder that they are quite aggressive and territorial. The other amazing aspect of stomatopods is their exquisite beauty. Their bodies appear to be a canvas for a 1960s psychedelic artist. Brilliant hues of red, greens, and blues merge, blend, and flow along their body. Some of the stomatopods also have tails that are filled with dots and splashes of different hues. Their colorful shells would cause any peacock to close its tail and hide in shame. These descriptions and any pictures of these animals fall woefully short of their entire beauty because we are viewing them with our measly little three visual pigments and seven million colors. As described later in this chapter, the mantis shrimp can see a much richer world than we can. They use this enhanced color vision in a number of different ways, but the most important one is to control the potentially lethal use of the weapons at the end of their arms.

7.1  The Different Hues of Aggression From a behavioral point of view, crustaceans are quite an interesting group of organisms. Most of them have some sort of weaponry, like a claw, which is primarily used in acquiring food. Some crabs and lobsters use these powerful claws to open up oysters, mussels, and other shellfish. When not hunting, the claws are quite effective at dismantling a potential competitor. With such deadly tools at their disposal, it isn’t too surprising that crustaceans are quite an aggressive group of organisms. Like some grumpy old men, they seem to waken in the morning looking for a scruff or a fight. For science and even school demonstration purposes, this is great. Just place two crayfish, lobsters, or crabs in a tank, and eventually they’ll begin a set of maneuvers that often lead into some sort of fight. The down side of having these claws is the potential that even winners of fights will leave a match quite injured. Given the lack of serious medical care at the bottom of the ocean, even small injuries can weaken the victor and eventually become lethal. As a result, many crustacean fights have

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become ritualized where a series of visual displays coupled with more gentle pushes and boxing with chelae are used to signal levels of aggression between combatants. Through these ritualized displays, fights gradually increase in their levels of aggression until one of the opponents decides to quit. Fights are often decided at lower levels of aggression and rarely lead to the unrestrained use of claws. In addition to the ritualized nature of fights, crustaceans have an amazing ability to remember previous opponents or even the ability to detect an opponent’s win-loss record before engaging them. This is where the colorful body plan and exceptional vision of the stomatopods become important. Stomatopods are commonly found around coral reefs and will make their homes in the natural crooks and crevices that are found everywhere within a reef. These burrows provide protection against predators and are as highly prized as the best castles in medieval times. Unlike castles, crustacean burrows tend to be rather cramped and tight-fitting. This design ensures that the owner, and only the owner, can fit in the burrow. Any unwanted access to the burrow has to go through the owner and face those powerful piercers or punchers at the end of their arms. Stomatopods defend these burrows quite vigorously. One such stomatopod, Neogonodactylus oerstedii¸ lives among the reefs on the Caribbean from Florida down to Panama. Commonly referred to as the rock mantis shrimp, this particular species is mostly green or brown with bands of lighter color along the back of its carapace. The underbelly is a little more colorful with iridescent blues. Although it is quite drab compared to other stomatopods, the animal is largely sensational compared to the rest of the animal kingdom. Stomatopod researchers and enthusiasts often classify the shrimp based on the type of weaponry, and this particular species is categorized as a “smasher” (as opposed to a “spearer” or “hatchet” type). This animal finds cavities in coralline algae, which is a type of algae that secretes a calcium skeleton that resembles a coral head. The animal is quite active and often leaves its home in search of food. It is likely during these trips that the rock mantis shrimp encounters other rival stomatopods. If two rock mantis shrimp were to encounter each other during their daily hunts, a series of aggressive interactions will take place. The rock mantis guards its shelter with intense determination. All intruders will be rebuffed with intensity and swiftness. The smasher appendage is cocked and ready as the animal waits at the entrance to its burrow. Its eyes, located atop of stalks above its head, look like enlarged balls sitting at the end of short straws. Although watchful, the eye doesn’t swivel around as if it is searching for potential conflict. The compound eye gives the appearance that a fine mesh covers the entire structure. In reality, the mesh is an illusion created by the individual ommatidia, which were briefly described in the chapter about the bee’s eye (Chap. 3). The ommatidium is the optical unit of the eye and gives the animal an ability to have a lens focused on different aspects of its visual landscape. Though the eyes are not darting back and forth, as ours would during an intense search, they are quite aware of the surrounding environment. Off in the distance, the animal catches sight of the briefest of movements and slowly shifts its body in the direction of the motion. It is another rock mantis shrimp

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that has entered its territory. To the first animal, the appearance of another rock mantis is a threat. The new animal is a competitor for the food resources in the area and may even attempt to take over its burrow. The first animal stays close to its burrow, but slowly draws its body out of the cavity in preparation for a fight. The intruder is also cautious. It must know that it is in a foreign territory and is attempting to size up the current owner of this part of the reef. The intruder slowly extends its weapons outward. Within crustaceans, this is called a meral spread. It is seen in lobsters, crabs, and crayfish during agonistic encounters. The exact meaning of the spread within the context of the fight varies across the different crustacean species. For some (lobsters and crayfish), the spread is supposed to communicate size and strength. By displaying the full glory of their weapons, these animals seek to end the aggressive encounter before the need to use those very weapons. Although the exact meaning within mantis shrimp encounters is unknown, a very conspicuous-colored circle on the weapons is commonly seen within the mantis shrimps. Research has shown that these circles are important sources of information during these contests and that the colored spot carries a wide variety of fluorescence in the visible light spectrum as well as in the ultraviolet spectrum. In response to the intruders meral spread, the owner also creates its own meral spread to ensure that the colorful spot is visible to the intruder. The intruder gives pause in response to the display and appears to be taking in the visual scene in front of it. The colors, shades, and hues in the spot carry information about its opponent including information on its social status, fight history, and even familiarity to the intruder. After the pause, the intruder approaches a couple of steps closer while maintaining its display. Here the intruder is testing its opponent for responses. Will the owner leave its burrow or stand its ground? Does the owner want a fight or more displays? The burrow owner watches the approach of the intruder warily. Turning its body to face the opponent head on, this mantis shrimp leaves its burrow and closes its meral spread. After taking a couple of steps to close the distance between competitors, the owner reopens its meral spread. Raising its raptorial appendage upward and outward, the animal is attempting more displays before committing itself to a full-­ out battle with powerful and lethal weapons. Approaching the intruder with renewed intensity, the rock mantis is clearly not going to give up its shelter easily. The intruder somehow senses this commitment upon the owner of the territory. The meral spot (accompanied with unseen chemical signals) has convinced the intruder that there is no easy meal or burrow to be stolen this day. The intruding animal lowers its body to the ocean floor and tucks its tail beneath its body. As a final act of contrition, the intruding animal stops displaying and begins its retreat out of the contested territory. The owner of the territory, through its use of signals, has demonstrated that on this day and in this area, it is the victor and will get to keep its burrow.

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7.2  The Science of Multicolor Worlds As mentioned, mantis shrimp are exquisitely colorful. Amazing shades of purples, red, greens, and blues can be found throughout the mantis shrimp family. Despite all these brilliant colors, the most important location and color is found on the base of what is formally called the raptorial appendage (its weapon). These colors carry special meaning within the fights of mantis shrimp, but the meaning is carried beyond just the visible spectrum. As explained in Chap. 3 on bees, several species can see within the ultraviolet spectrum of light. Mantis shrimp are unique in the animal world in their ability to see colors and even detect light outside of what is considered the visible light spectrum. Stomatopod eyes can be divided into three distinct regions, the dorsal (or top) end, the midband, and the ventral (bottom) end. The midband is where all the highly specialized adaptations are located. Within the midband, the stomatopod eye has densely packed rows of ommatidia. As a reminder, an ommatidium is a hexagonal tube that houses a single lens as well as six to eight receptor cells. These tubes make up the basic design of a single compound eye, because of their vast quantity. These animals, as well as countless others, have compound eyes. Each ommatidium has a unique angle or view of the world, and the animal’s brain seamlessly knits together all these views to produce their visual landscape. In the midband of the eye, the ommatidia are packed together in parallel rows, and most stomatopods have around six rows in the midband. So, the first layer of organization is top, middle, and bottom, and within the middle section, there are six rows of ommatidia. A single ommatidium consists of the cornea (lens) and a section that houses the functioning receptor cells called rhabdoms. As an analogy using the direction of light to guide the explanation, the human eye consists of a lens which encounters the light first. The lens filters and focuses the light as it passes through the fluid within the eyeball (vitreous humor). Finally, the light connects with the retina which is lined with two types of receptor cells: cones, sensitive to color, and rods, which are used for low light conditions. The stomatopod eye has an ommatidium where the light passes through the cornea into the rhabdom, which has the receptor cells (Fig. 7.1). Within the midband of the stomatopod eye, each ommatidium will have different light filters that reside just above the receptor cells. These filters act as sunglasses and only allow certain wavelengths of light to pass through the receptor cells. Similar to having different colored sunglasses, one pair would block out blue light and another would block out red. For the stomatopods, the ommatidia have filters that are unique for each of the rows. This single adaptation would provide the animal with a much richer experience of the visual world than almost any other animal. Yet, there are even more layers of complexity. Within each ommatidium, the receptor cells are stacked on top of each other in layers or tiers. The lower tiers of receptors are sensing light that has already passed through the upper tiers. This design enhances the ability of each ommatidium to capture more light and to allow the unique filters above to influence the type of light being passed along to each of the tiers.

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Fig. 7.1  The amazing stomatopod eye. In the middle of this drawing of the stomatopod eye is the midband where the highest density of different photopigments are located

Yet, just like in a bad, old late night commercial, the phrase “But wait, there’s more” is appropriate. As noted above, humans can supposedly sense seven million colors with our three visual pigments. Sadly, dogs only have two different pigments, and thus, their color world is less rich than our own. Stomatopods can have up to 16 visual pigments, more than 5 times the number of pigments that humans possess. These visual pigments are spaced between the short-wavelength light (ultraviolet, violet, and blues) all the way up to long-wavelength light (red and infrared). The exact number of colors and color variation that stomatopods can detect with 16 different pigments is orders of magnitude beyond what we can do with our measly three pigments. Now, the true complexity of the stomatopod eye can be appreciated. Thousands of different ommatidia are located on eyes raised above their body. Within the densely packed midband of the eye, the ommatidia have different “sunglass”-style filters that limit and tune what each particular ommatidia is sensitive to, and within each of the ommatidium are tiers of receptor cells being turned on and off by the various colors emanating from the body of other stomatopods. Finally, 16 different visual pigments further parse out the color world into detailed slices that allow the animal to see amazingly large ranges of color. With this highly complex eye, the animal can focus in on the fine-scale color patterns on the meral spot of competitors, opponents, or even potential mates. This is done with such precision that these animals probably are aware of subtle color deformations in the meral spots and may be able to identify individuals based on these color patterns. This is why the stomatopod is known as the champion of eye design.

Chapter 8

The Eye as a Window to the World

Because of the central role that vision plays in our daily lives, we have developed an artistic and spiritual connection to our eyes. Such concepts as “eyes are the windows to the soul—English Proverb” or “Poets are damned… but see with the eyes of angels  - Allen Ginsberg.” Deeply emotional attachments are linked through the world by the eyes that allow us to experience life visually. One can stare deeply into the eyes of a loved one. We can flirt with our eyes or we can emote an everlasting kinship when good friends say goodbye. People’s intentions can be “told” with their eyes whether intention is disapproval by throwing shade or empathetic connection by a soulful stare. Between these two extremes, we find that we can smile with our eyes and give approving looks, or with an intense glare, we can flash red hot anger. These are just a few examples that demonstrate the importance that we attach to vision in our daily lives. It is not a stretch to conclude that vision is our primary sense and plays a predominant role in developing our umwelt. The eye has also played a critical role in the understanding (or misunderstanding) of evolution. Most vertebrate eyes, including ours, are quite complex in design and function and are a wonder of evolution. Darwin, in his seminal book, On the Origin of Species, also recognized the complexity of eyes when he wrote: To suppose that the eye, with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree.…If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down. But I can find out no such case.

Despite the intricate designs, which were explained earlier in this section, Darwin also recognized that the diversity of eyes and their design can easily be explained through the process of natural selection. Let me also insert a caveat here. When I refer to “eyes,” I am really referring to the entire visual system from lens to neural processing. Many of the features of the world around us are “seen” by the brain and

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not by the lens, retina, and nerve cells contained within our eyeball. Thus, although the word “eye” is a scientifically inaccurate term, substituting visual system for the eye is easier for the flow of this book. Keep in mind that natural selection does not create perfect eyes, and instead the process of natural selection creates functional eyes whether for a four-eyed fish, honey bee, ant, or owl. The concept of functionality depends upon the habitat an organism (and its eye) finds itself (day or night) and the role that vision plays in an organism’s life (hunting underwater or foraging for nectar). For example, the eyes of frogs have an inordinate fondness for dark rectangular objects moving quickly across its visual field, which indicates food as small insects flying in the visual field of the frog. Frogs have no need to form a detailed visual image that might allow them to identify the species of insect, thus becoming an amphibian entomologist. The most salient features of the visual world for frogs are insects, and insects can appear to be small rectangular objects which does not affect the functional ability of the frog to visually locate its prey. This system can be easily fooled by substituting a small black rectangle for food is functional enough for frogs. Eyes are adapted to the most salient features of the world around us and as such; eyes also ignore those features of the world that are unimportant for the survival of the owner of the eyes. This singular concept, paying attention to only salient features, is behind the illusive world. Although we like to think that seeing is believing, magicians and natural selection say differently. We visually experience only a fraction of what the visual world offers up for sampling. The nighttime world of the owl is a series of black blobs to our eyes. The ultraviolet pattern on flowers, which is meaningful to bees, is replaced by colors and patterns (which are meaningless to bees) in our world. Illusionists make us believe that we see something that isn’t real, and natural selection makes us ignore aspects of the world that are quite real for other animals. Just as an illusionist should make us question visual reality during their show, an improved understanding of the visual world (and how it’s seen) should make us question whether we see a complete version of reality.

Part III

Audition

Hearing is a form of touch. You feel it through your body, and sometimes it almost hits your face. —Evelyn Glennie

Chapter 9

The Music of Nature

For some, almost mystical reason, I am drawn to water. During my graduate school days in Woods Hole on Cape Cod, I used to walk down to the beach at night for some serenity and peace after hectic days in the lab. With a cold Rolling Rock beer in hand, I would walk out to the end of a rocky pier and just sit. Staring out into the vast ocean, I was alone with my thoughts and the sounds of the waves gently crashing against the pier. The silence of the calm nights was rhythmically interrupted by the waves, and a feeling of peace would settle upon on me. Now, in the latter half of my career, I work primarily in the freshwater systems of lakes and rivers. Despite the change from salt to freshwater, I am still clearly drawn to the water. My oceanic rocky piers have been replaced with hammocks hanging near the shore, but the sound of waves breaking upon the beach provides me with that same peaceful feeling. One of the benefits of moving from a marine to a freshwater habitat for my research is the ability to sit aside the small rapids or waterfalls on the different rivers I have explored. A different sound than waves on a beach or pier, the gurgling of streams, or the unique sounds of water rushing over rocks and falling down rapids provide me with the same level of satisfaction. Maybe it isn’t the water that draws me in but the natural music produced by the moving water that creates the magical environment full of musical spells which envelopes me. Nature, imagined as a sentient artist, knows the right sets of tones and rhythms to produce hypnotic sounds. The rustle of leaves due to a gentle breeze, the drumming pattern of rain drops on a roof, and even the mystical quiet of an evening’s snow fall display the full range of musical abilities of nature. In the wizarding world of the Harry Potter series, the students gather in a great hall on the very first day of classes. During this gathering, the headmaster of the school, Albus Dumbledore, has all the students stand and sing the school song. Although every student sings the identical words of the song, in a whimsical twist, each student can choose their own melody. What emerges is a cacophony of sounds, words, and melodies that finally ends as the last two students, who have chosen a funeral march, finish their version of the school’s song. Dumbledore, tearing up, quietly states “Ah, music. A magic beyond all that we do here!” This line resonated © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_9

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with my aquatic life filled with the songs of breaking waves and rippling rivers. I have carried this need for music during my non-field days. The life of a scientist at a university is quite variable. Depending on the day, I may be teaching; writing books, such as this one; marching through wetlands, lakes, or rivers; meeting with students; constructing experiments; chatting with colleagues; or quietly reading the latest journal articles. Despite the variability of my days, the singular constant throughout my work is the presence of music. There always seems to be some form of music playing, regardless of my location. This is particularly true if I am deep in thought or in the midst of writing. In fact, most of my previous book was written while listening to a single artist’s album. One would think the monotony of the same set of songs over and over again would dim the bulb of creativity, but for me, their album energized my bulb such that the creativity burst through any haze in my mind. On the days that I didn’t feel creative or really didn’t want to sit down and write, I would start playing that artist’s album. As the familiar strains and words began to emanate from my speakers, I would be visited by some invisible muse and the words would flow. Some sort of magic in the music seemed to envelope my mind, and I would enter a state of being where the world would melt away with nothing existing but my book and the music. Despite the power of human-created music in my life, I prefer the presence of nature’s music during my hikes and explorations through either urban or natural landscapes. The sounds generated by the denizens of the surrounding habitat can provide so much information to us. If I am hiking through a previously unexplored forest area, the pulsation of waves on a beach or the rushing of water of a river can often be heard long before the water can be seen. Thus, I know I am approaching an aquatic habitat. The crunch of the forest floor underneath my foot informs me on the types of leaves, branches, and soil that comprise the habitat. As my birding friends would point out, the calls and chirps of many feathered creatures are often the only piece of information that tells someone that a particular species is present. For me, the sounds present during my hikes are far more enjoyable than the sights of the trees, flowers, and other forest plants. We rely so heavily on vision to understand the outside world that we often relegate our hearing to a distant secondary role. We think that sound is only useful for interacting with other people (or listening to music). This is readily apparent for anyone that has walked on a college campus. The moment that classes are dismissed and students are free to walk around to their next class, an interesting phenomenon occurs. Earbuds and headphones are instantly donned as students turn on their music and shut out the sounds of the outside world. The sounds of their fellow students are ignored as their sight is focus on finding their way to the next classroom without running into someone. The ability to hear the complex and varied sounds within the music of humans or nature fundamentally relies on a very simple and yet powerful cell: the hair cell. Our ears contain a complex mixture of structures that include the eardrum, three little bones (the hammer, anvil, and stirrup), vestibule, cochlea, and tectorial membrane that all serve to either amplify or differentiate sound waves for us to hear. Despite all of these various physical structures that help condition the sound, the structure that translates the pressure waves into electrical signals for our brain is the hair cells.

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Fig. 9.1  A simple hair cell. The basis of many different sensory systems, the hair cell has kinocilia (the longer hair on the right), and a series of stereocilia beside the kinocilia. The hair cell is often innervated by another nerve cell and has no axon of its own

A hair cell looks like the capital letter D rolled over on its rounded edge (Fig. 9.1). Human hair cells in our ears are a very elongated or a stretched D that is tubular in shape. At the top of the D are a series of hairs that give the cell its name. There are two types of hairs at the top of the cell, stereocilia, which are shorter and more numerous, and often a single kinocilium, tall and lonely, at one end of the bunch of stereocilia. If viewed from the side, the hairs increase in length, almost like lining up the children of a middle school class by their height, with the much longer kinocilia at one end, like the single teacher of the class. Why is this detail important? Hair cells show a directional sensitivity to sound waves. If the bunch of hairs are stimulated and bent toward the longer kinocilia, the hair cell is activated and sends signals to the brain. If bent away from the kinocilia, the cell is inhibited or turned down. This simple design, directional sensitivity, along with a host of morphological structures, allows the human ear to experience the wonders of Mozart, the beauty of a mockingbird song, or the natural lullaby of a gentle rain. The very simple hair cell, along with morphological adaptations, is the basis of just about every animal’s hearing or even sensing sound (or pressure) waves. What really differentiates how various ears work is the morphological structures that interact with this very simple hair cell. For example, if one were to place a blob of jelly on top of the hair cell and place this combination in a canal on the side of a fish (called a lateral line), a flow sensor can be built. Change the configuration of the lateral line, and a pressure sensor is constructed. Conversely, that same hair cell is found within a structure called a cochlea. The cochlea is inside of our ears and is constructed from three circular tubes all placed at right angles to themselves. This hair cell and structure gives us the ability to detect our equilibrium, a sense that astronauts and roller coaster enthusiasts are intimately aware of.

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Is an equilibrium a sense of hearing? In most cases, the answer to this question would be no. Equilibrium senses are attuned to position and gravity and are not responding to sound or pressure waves. Yet, at the base of many different species’ abilities to sense motion and up versus down is the simplistic hair cell described previously. Despite the similarity of the underlying sensory machinery, our cochlea does not hear, but does provide a caution against defining a sense based solely on how humans detect and use that sense. Thus, a very narrow approach to explaining the world of sound would focus only on vocalizations and their detections. A broader approach would include all the various ways in which organisms have used the simple hair cell (or other sensory machinery) to detect different stimuli in nature including motion, speed, and directionality (up from down). Of course, the broader approach will enable our intellectual trip to include some interesting adaptations and functions, so the more abstract approach on “hearing” will be used here.

Chapter 10

All About the Bass

In a previous chapter on vision, the description of light energy was placed upon a spectrum. At one end were the long wavelengths of infrared and red, and at the other end were the short wavelengths of violet and ultraviolet light. In the middle of this spectrum was human vision extending from 390 (red) to 700 (violet) nm. In a very similar fashion, sound can be placed along a scale, but with frequency instead of wavelength as the measurement. Sound waves are pressure waves and can be visualized as a slinky stretched out on a flat surface. If one were to just casually lay out a slinky on a desk or table, the rings on the slinky would likely be randomly spaced out along the toy. Some of the rings would be jammed closer together, and others would be pulled or spaced apart. The same type of distribution occurs with sound waves. When the rings of the slinky are closer together, this would represent what is called a compression in the sound wave. This is a higher pressure point on the sound wave. A rarefaction occurs where the slinky’s rings are spaced further apart and is associated with a lower pressure. In a different view of the slinky, the compression of rings can be considered the “crest” of a wave (despite the height of the slinky remaining constant), and the rarefaction is the “trough” of the wave. Just like the slinky, the sound wave is a series of crests and troughs traveling through space. Sounds can have intensity and pitch. The height of the crest of the sound wave determines the intensity or loudness of the sound, and the number of crests that occur within a second determines the pitch of the sound. This last measure (crests that pass by per second) is called frequency, and unlike light (which is measured in wavelength or the distance between two crests), sound is measured in frequency. Typically, most humans can hear sounds that range from 20 Hz up to 20 KHz. This is a large span of frequencies, but we are most sensitive to sounds within the 1–4 kHz range. As with the ends of the visual spectrum, the prefixes ultra- (as in ultraviolet) and infra- (as in infrared) are added to the ends of the sound spectrum. Unlike the colors of light, there are not unique names for different frequencies of sounds. Thus, only the ends of the sound spectrum have the very pedestrian names of ultrasonic (very high frequency) and infrasonic (very low frequency). From an evolutionary perspective, our visual spectrum is most sensitive to those colors that played a © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_10

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s­ urvival role, such as the identification of appropriate food that is ripe. The same is true for our auditory system. Those sounds in that 1–4 kHz range are important for our survival as well as the social aspect of our lives. Human voices fall within this range as well as many sounds associated with predators and prey from our evolutionary history. If biological evolution moved more rapidly than it does, I wonder what our hearing would look like given our modern technological habitat. At one end of the auditory spectrum of a modern hearing range would be the mosquito ringtone. This ringtone has a dominant frequency of around 18 kHz. This is a favorite ringtone of teenagers because most people, over the age of 25 or so, cannot hear this ringtone. As we age, our hearing degrades, and we tend to lose more sensitivity in the upper spectrum of sounds more quickly than the lower spectrum. At the lower end of the modern hearing spectrum would be the low-frequency sounds produced by the movement of large and heavy trucks within a city or the loud bass on a car with intense speakers. These low-frequency sounds are an interesting case because they can be sensed differently than most other sounds. Imagine strolling along a sidewalk enjoying the fresh air, when a car turns the corner and starts to drive down the street. From a distance, you can tell that the car has been modified to include heavy duty speakers in the trunk. Although, you cannot make out the music that is playing, you can certainly hear the bass pounding away in a rhythmic fashion. At this point in time, you are perceiving the pressure waves generated by the cone of the speaker. The vibration of the cone, which is controlled electronically, produces the pressures waves that you perceive as sound. As the car slowly approaches, the intensity of the very deep sound increases, but something else, some other feeling, is emerging. As the car comes next to you, certainly, the deep bass is still present, but your entire body seems to feel the sound and you find yourself in some state of unease. Two things are occurring during our imaginary example. First, the intensity of the bass is such that you are probably both sensing the pressure waves through your normal hearing channels (your ears), as well as your body being moved by the pressure ways themselves. This secondary sensation adds to the intensity of the auditory response. Second, it is entirely possible that the vibration of the speakers in the car has passed through the tires into the ground and then transmitted to your body. This ground vibration is certainly not hearing as detected by the ear, but it is a type of sensation. Think of the classic scene in the original Jurassic Park, where the T-rex is approaching our heroes. Every step is heard, felt, and visualized as rings created within a cup of water. (As a related side note, intense low-frequency vibrations have been known to heighten fear, stress, and anxiety in humans.) These vibrations, whether from speakers in a car or an imaginary T-rex, have the potential to carry valuable information over very long distances. Certainly, these distances are much longer than we would normally think about for acoustical communication. Old American western movies frequently portrayed one of the characters laying their ears to the ground to “hear” distant horses or wagons following their trail. Periodically laying an ear to the ground would be quite cumbersome for many different organisms, evolving the ability to hear with something that already is in constant contact with the ground may provide a much easier solution. For land

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animals, that structure is their feet. If it was possible to “hear” with feet, organisms could communicate using infrasounds at a distance far greater than visual communication. It just so happens that elephants have this exact form of communication. They have the capacity to produce low-frequency sounds as well as detect them with their feet.

10.1  Hearing the Earth Move Under Your Feet The majestic African elephant (Loxodonta africana) can often be found in the open savannahs and on the edges of forests in the mid-to-lower latitudes on the continent of Africa. Highly social and intelligent creatures, African elephants live in social systems across the savannah. Their social systems are often centered on a matriarch and several other mothers that will vary in relationship to the matriarch. Sociality is somewhat fluid throughout the year, especially when females become reproductively active. Even over the course of a day, two family groups may join together and break back up later on. Beyond this family unit are several other levels of organization, but for the purpose of this chapter and behavioral description, it is only important that these higher units can be dispersed widely across the savanna, facilitating the need for communication over long distances. The large creatures roam these habitats in search of vegetation to consume. Elephants are such an interesting animal to humans that they have been the subject of a large number of studies (both formal and informal). Young reproductively active males often live alone, even during the reproductive season. When these young males come into musth, they are ready to find females for mating. Male elephants in musth are quite aggressive, yet they tend to avoid each other during their search for mates. This dynamic social and mating system is where elephant infrasound is a fascinating topic. One of the most common places in which family groups will gather and join into larger groups is the watering hole. A precious resource during the dry parts of the year, many groups of animals will be found around water and form a tentative unspoken peace agreement to share the water. As one group of elephants use the watering hole, several other groups will wander in. This is when periods of communication can take place. Even on cool days, elephants enjoy splashing around in the water, and this is especially true for juvenile elephants. For elephants, a nice drink of water and a bath is a great way to spend part of the day. If the watering hole is large enough, several groups of elephants will appear. The largest female in each group is the matriarch and the natural leader of this family group. She’ll watch over the herd and greet any groups that want to temporarily join them at the watering hole. Always vigilant, she is probably listening more than looking for other elephants. As groups approach her herd, she’ll turn her attention to the approaching herd. The other herd will have its own matriarch, and these two leaders will slowly approach each other and begin their communications. When they are spaced about 50 m apart, they’ll stop and begin listening to each other.

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Although infrasounds are a form of communication, the ability to detect and recognize the very low frequency of sound can also be used to monitor movement of herds across the savannah. The powerful steps of the elephants will generate vibrations that travel through the hardened soil. This vibration moves through the soil as a wave, outward from the footfall, and is detected by mechanisms that couple the foot to the ear in the receiving elephant. In our example, the two matriarchs walk ahead of their group to greet each other. While it appears as if they are just staring at each other, they are actually developing an important conversation. The “words” can be measured by using special microphones that are sensitive to low-frequency sounds. The matriarch of the initial group would normally begin the conversation by emitting a deep and low rumble. The ground beneath the calling female shakes as a result of the greeting call. If we were standing close enough to the call, we would feel the rumble through our feet. This would be similar to standing on a sidewalk while a large dump truck drove past. We would feel the sidewalk vibrate, but we would be unable to determine a meaningful information from the vibration other than a large object passed by. One of the ways we can tell that the elephants are communicating is that both of their front feet are planted firmly on the ground. This is critical for the reception of these signals. After the initial call, the lead female of the approaching group will let go with her own version of a greeting call. The call, which feels like another dump truck rumbling by, varies between 18 and 25  Hz. Human hearing diminishes in sensitivity around 20 Hz. This is why we would sense the call as a movement of the ground as well as vibrations in the air. These calls are just at the edge of our ability to hear using our ears. The matriarch will respond rather quickly after the approaching group’s greeting call. As the matriarch responds to the approaching group’s call, she increases the intensity of the call. Perhaps to establish her dominance to this other group. The call is similar in frequency, but much louder. This is a fully loaded dump truck driving by and we can feel the fill strength of her call. These elephants are calling with their vocal cords even though most of the signal is being transmitted into the ground. The elephants are actually using two mechanisms to listen to these calls: one involves the feet and the other involves the detections of vibrations in the air with their ears. Both large females have opened up their massive ears in order for the sound to penetrate to their ear drum. Their feet are still firmly on the ground. The feet are sensing the lowest frequencies as vibrations in the earth. As the females call back and forth, the intensity gets varied as well as the frequency of the calls. At this point, the greeting communication will continue using multisensory signals. Chemical signals produced in facial glands as well as urinary signals will accompany the continued rumbles until the group decides to join up for some larger-scale playing and splashing. If the right signals are produced, the matriarch will move forward to invite this other group in to share the watering hole. This is part of the dynamic and fluid aspect of the social system within elephants. Although protected by a matriarch, bonded groups will come together to play or forage and then break off into their family groups. This ritual of calls (or seismic communication) helps groups recognize each other and send communications of

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intentions or familiarity. Elephants have a wide range of low-frequency calls that function within both social and reproductive situations. After an extended period of play and interactions at the watering hole, the initial matriarch begins to slowly move away from the herd. As dominant individual, she has determined that it is time to leave the watering hole to forage. To announce this to the rest of her herd, she’ll move away and generate a different set of calls. During these calls, she raises one of her feet off the ground to change her level of sensitivity to seismic communication. These calls are a softer, but constant, rumble. Barely audible to us, the call is still a low-frequency call but has a softer edge to it than the greeting signals. These calls are a lower amplitude than the greeting calls that were used earlier. These calls are around 15  Hz and are repeated every few minutes, almost like a parent standing at a doorway, repeatedly calling for their kids to come in for dinner. The matriarch will stand still and repeat her calls until one by one the family members gather around her. As family members join the matriarch, they will also join in the calling. As a second female approaches near the first, she will raise her foot also as a clear sign that she has joined in the calling. These calls, since they are lower than the greeting calls, are primarily heard through their feet rather than their ears. The final family members are gathering, and the matriarch is probably giving her last call. As they gather, the family members will stand still and face the matriarch. This gives them the best chance to sense the call and understand what the matriarch is telling them. She is signaling that play time is over and it is now time to move on to forage.

10.2  The Science of the Distant Rumble of Words The elephant communication system provides an excellent model to explain two different aspects of auditory communication. The ability to produce such rich and low-frequency sounds requires some specialized adaptations based on the interaction of air and vocal cords. Also, given the human auditory system as a reference, we tend to focus on the compression and rarefaction of air to produce pressure waves as the system of communication. Elephants certainly perform this style of communication, but also send waves through the ground to other elephants. This requires a new and different listening mechanism than an ear drum, some smaller bones, and hair cells. As mentioned above, this is called seismic communication, and elephants “hear” these energy waves through their feet. Formally defined, seismic communication is vocalization or energy waves that travel through solid substrates like the ground rather than through the air. Now, it is certainly possible for us to sense shifts in the ground (think earthquakes, powerful thunder, or large moving vehicles such as trains or trucks), but sensing shifts in the ground is different than extracting meaningful information from these signals. The elephant systems are designed to gather information from the movement of waves within the ground they are walking on. First, let’s turn to the vocal communication.

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Terrestrial vertebrates produce vocalizations by forcing air through the vocal cords. The vocal cords are two membranous tissues found in the larynx. The tissues form a slit and vibrate when air is forced through the slits, which is similar to the sounds produced when air is released from a balloon. The two halves of the rubber balloon vibrate as the air passes through the opening. If one controls the tension on the rubber balloon, it is possible to create different types, pitches, and frequencies of sound. In a similar fashion, control of the tension and position of the vocal cords allows a person to create different sounds. The pitch of a person’s vocalizations is determined by the fundamental frequency of the larynx (which is, in turn, dependent on the size of the larynx) and the length, size, and tension on the vocal cords. A smaller larynx or vocal cords will produce higher pitched sounds. Conversely, a longer and larger larynx and vocal cords will produce lower pitched sounds. The sounds produced by elephants are called infrasounds because the frequency of these sounds is very low. The concept of low is very subjective, but infra- and ultrasounds are defined against human hearing. Ultrasonic communication occurs at frequencies above what humans can hear, and infrasounds are lower than the 20 Hz baseline that humans can detect. The sounds produced by elephants across their wide array of vocalizations are all infrasonic in nature. Elephants produce their sounds in a similar fashion to how humans talk or sing. They force air from their lungs through their vocal cords which causes them to vibrate. This vibration produces a host of frequencies that we would recognize as sound, but because the elephants are performing this task at a much lower frequency, we sense this as vibrations. Elephants can produce such powerful and low-frequency sounds because their vocal cords are so long. Human vocal cords range from 1.25 to 2.5  cm in length with males typically having longer cords and deeper voices. Elephant vocal cords can be as long as 10 cm in length. This increased length allows the elephant to produce such low-frequency calls. Elephants have a large nasal cavity, much larger than expected even for something the size of an elephant. Other mammals have adaptations that allow vocalizations to be focused which helps produce louder sounds. Dolphins have a structure called the melon that allows them to focus and intensify their communications. The elephant’s nasal cavity also has layered cartilaginous structures that could function in a similar fashion as the dolphin’s melon. Thus, the elongated vocal cords, large lung capacity, and nasal cavity create a series of structures that allows the elephant to produce intense low-frequency signals. Another beneficial factor for seismic communication for elephants is that seismic waves travel further without degradation than sound waves. Sound waves travel outward from their source as an increasing sphere. Think of blowing up a balloon. As you blow more air into the spherical balloon, it expands equally in three dimensions. As sound is generated, the sound waves travel outward in all three dimensions equally. Because of this spherical relationship, sound intensity drops significantly with distance. Intensity of sound is often measured in decibels. Decibel (dB) is calculated as the log of the sound intensity divided by some reference intensity. For most calculations, that reference intensity is the threshold of human hearing. The log function means that every 10 units of decibels mean a tenfold increase of

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i­ntensity. For example, a sound that has an intensity of 50  dB is 10 times more intense than a sound of 40  dB, 100 times more intense compared to a sound of 30 dB, and finally, 1000 times more intense than a sound of 20 dB. For sound waves, the intensity drops off at about 6  dB for every time the distance from the sound source is doubled. Conversely, seismic waves are traveling through material that is often a bit denser than air. Ground, wood, or even concrete has a higher density than air, and sound waves travel faster in objects that are acoustically dense. In addition to this density difference, seismic waves travel in increasing circles propagating outward from the source rather than the spherical mode for sound waves. These two factors, when taken together, mean that seismic waves only drop by 3 dB, which is half of the decrease seen in sound waves. This fact explains why we “feel” seismic waves (like strong thunder or a car with a large bass) long before we would hear the sound from that source. Still, being able to produce sound that travels through the ground is one thing, but how do elephants hear these sounds when their ears are several meters above the ground? At this point, it is important to note that sound waves are translated into vibrations as the pressure waves hit our eardrums. The internal structure of our ears is actually capable of hearing vibrations (and translating this vibration into sound) that are conducted through the bones of our jaw and skull. Modern headphones can be used to conduct vibrations to our ears allowing us to hear music while our ears remain open to external sounds. One of the ways to improve sound reception in people with certain types of hearing loss is to use hearing aids that transmit vibrations through the skull right behind the ear. A similar mechanism appears to be in place for elephants as they detect seismic waves with their feet. Elephants have a fatty deposit or cushion at the base of their feet. All other fatty deposits within the elephant’s body fluctuate in size based on the food intake and storage of the elephant, similar to how mammals “fatten” up before the winter or how certain parts of our bodies fluctuate in size as we increase or decrease in weight. However, the fatty cushion in the elephant’s foot stays the same size throughout the seasonal variation in the elephant’s body fat. This cushion rests just below several bones in the elephant’s foot and can resonate as seismic waves travel past the foot. This is a similar mechanism to how the vibrations in our tympanic membrane (ear drum) are transformed as movement of the inner ear bones in our ear. The vibrations in the fat body would create vibrations in the bones of the feet. Consequently, these vibrations would progress from the foot to the legs and up to the shoulder of the elephant (Fig. 10.1). Bone conduction of seismic waves in elephants is further supported by the construction of the inner ear bones. Within humans, these three ossicles (small bones) are called the hammer (malleus is the technical name), the anvil (incus), and the stirrup (stapes), which are all connected together in a way to transmit vibrations of the tympanic membrane (ear drum) to the cochlea of the inner ear. The size of the bones is exceedingly small to help transmit higher frequencies to the ear. Within the elephant, these same bones have grown quite large which would make them more sensitive to seismic waves. On the behavioral front, elephants turn to face the source

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Fig. 10.1  The elephant’s ear. A fatty deposit (the yellowish orange organ) vibrates in response to low-frequency sound, and this vibration is transmitted through the bones of the feet to the inner ear

of the waves, spend more time freezing their movements, and keep their feet on the ground during artificially produced seismic waves than for vocalizations. In addition, the elephants place more weight on their front feet during the detection of seismic waves, which happens to place their front limbs in a direct line with their ears. By standing still and facing the source of the ground waves, elephants can “hear” over very long distances. Instead of putting their ear to the ground (as shown in old western movies), these elephants literally walk with their ears (feet) to the ground.

Chapter 11

The Sound of Fear

Within human society, vocalizations (words, sounds, and songs) are used to convey information or thoughts from the sender to the receiver. Just as surely as the elephants created seismic waves for greeting family and friends, we use words in an identical fashion. A friendly “hello,” “what’s up,” or “nice to meet you” are used as greetings and undoubtedly depend upon the familiarity of the two parties. Aside from these phrases, we use words and sounds to engage in two-way dialogues. Constructing sentences out of a series of vocalizations has the ability to powerfully transfer the feelings and objects in one person’s brain into the other person and vice versa. A back and forth of words can create structures for deep thought and is really the basis of modern human sociality. Even beyond words and thoughts, sounds can be used to evoke certain feelings. As mentioned previously, whenever I write, I have a certain style of song playing in the background. The music and words create an emotional setting within my mind that allows me to be creative in both my thinking and writing. Within the commercial advertising world, the use of sound and music can be used to convince the consumer to get up and dance with happiness or be introspective about their lives. For wedding ceremonies, the bride and groom often spend significant amounts of time choosing particular sets of songs to be played at pivotal moments. In their mind, they hope that the songs will create an emotional environment for themselves and the attendees in which love and hope are strongly felt. Sound producers in the movie industry are intimately aware of the ability of sounds or songs to evoke the right feelings at the right moment in time. Some of these reactions are innate, and others are learned based on a connection between the movie scene and sound. Powerful low-frequency sounds often evoke anxiety or fear for humans and even some animals. Maybe the deep hum creates the idea that some large (and potentially extraterrestrial) object is nearby or that strong seismic signals are connected to disasters like earthquakes. One of the more notable examples from movies includes the repeated two-note beginning to Jaws. Although over 30 years old, this sounds is ingrained in our cultural knowledge and still creates a sense of trepidation in the listener. The Imperial March (Darth Vader’s theme) created by © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_11

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John Williams for the Star Wars franchise creates a combined sense of power and evil. Even just simple cords or an increase in the intensity of background music can heighten the sense of anxiety in movie goers. In many horror movies, subtle and not-so-subtle changes in music create the sense of impending doom. This can be easily demonstrated by listening to the same movie clip with the sound off. Under these silent conditions, the scene is far less menacing. This effect is so commonly known that several horror movie satires have characters break the fourth wall to warn the audience of impending horror because of the change in sounds. Unfortunately for animals, there is no artificial soundtrack that plays during their daily routines that could warn them of a potential predatory attack. Animals have to rely on the sounds (intentional or unintentional) that the predators make. Movement of the predator toward the prey often generates unintentional sounds that can be heard and tracked by prey. These sounds can be pressure waves from swimming predators, the sound of wind rushing over feathers from flying raptors, or even the footfalls of terrestrial predators. As much as predators attempt to mask these sounds, many of them are unavoidable, and the auditory systems of prey can be finely tuned into these exact sounds. A few predators (e.g., bats and dolphins) actively create sounds that help them either find their prey or stun them once they are found. These active hunters use the return echo off their prey to help them hunt effectively. As a consequence of this sonic hunting, the prey have a “movie soundtrack” that can tell them if and when a hunter will strike. For insectivorous bats, ultrasonic vocalizations are a key to their hunting success. Eschewing visual and olfactory cues, these bats create high-pitched sounds during their flights. These sounds have very small wavelengths that bounce off smaller objects in the air, which tend to be flying insects. The bats then use these echoes and differences in the time of when they arrive at the right and left ears to locate their prey while flying. The bat’s sense of hearing is wonderfully adapted to this mode of hunting, and the science behind their amazing abilities has been aptly studied for years. What is even more intriguing about this predator-prey relationship is what the prey have evolved in response to this ultrasonic hunting. Some species of insects have evolved ears in response to this predation pressure. Instead of just listening for the presence of bats and hiding, these moths take an active role in their defenses.

11.1  The Song of the Flying Tigers Despite its name, the tiger moth, Bertholdia trigona, is not the orange and black you would expect. This species is brown and red with some colored spots on their wings. Tiger moths are found across the globe in a wide range of habitats, but for this tiger moth, it is the co-occurrence with bats that is the focus of this story. The vocal dance between these moths and the voracious bats occurs at night and with excellent night-­vision cameras can be easily captured. Most of the science about the interactions between the bats and this moth is done within controlled laboratory settings, so that excellent video footage can be captured. In addition to the video equipment,

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sensitive microphones are needed to explore the interaction between hunter and prey. The bat vocalizations occur between the frequencies of 20 and 100 kHz. At younger ages, humans can detect up to around 20 kHz, but that ability fades quickly with age such that even most 25 year olds are unable to hear these bat calls. As the sun begins to set, the tiger moths take flight in search of food or mates. Night-blooming flowers and calling females are just a couple of the denizens of the night that produce fragrant calling cards for the moths. Compared to other flying insects, moths do not appear to be the most graceful fliers. Their relatively large and hairy bodies are bulky compared to most flying insects. They are slow and always seem to be struggling to stay aloft. This appearance is deceptive because the moths are strong fliers as will become evident in their interaction with their predators. Once the night fully takes over from the day, the sky is filled with tiger moths. The dark, small objects are gently flying around in search for a quick meal or a female to mate with. By straining the eyes and examining parts of the sky that are clear, larger and quicker darks spots can be seen. These are the nocturnal hunters of the tiger moths, the bats. Their speed and agility clearly outclass the moths, and just by comparing the flying abilities of these two species, the hunter appears to dominate the prey. What is unheard by us are the ultrasonic clicks of the bats. The high-­ frequency calls are being sent out by the hunters in hopes that a return echo will indicate the presence of prey. Most of the tiger moths are unaware of the presence of the bats. It is only when the bat’s ultrasonic click bounces off of a tiger moth that the moth is aware of the hunter’s presence. Of course, as the echo returns to the bat, the bat is aware of the prey. This is where the interesting dance begins. The bat, upon recognizing the moth, will begin a series of clicks that will allow the animal to focus its flight path on the moth. In ecological terms, the bat is an intercept hunter. It is using the echoes to determine distance and direction of the moth as well as predicting where the moth will continue to fly. Once this is calculated, the bat doesn’t chase the moth, as a cheetah does to its prey. The bat attempts to arrive at the same location in space as the moth and, by doing so, capture it in flight. From an evolutionary point of view, the moth is aware of this hunting technique and is preparing its own calculations. The moth won’t go into defensive mode until just the right moment in time. That moment is the split second before the bat makes its final capture move. The moth is alerted to these final moves of the bat, based on what the moth hears from the bat. The bats actually have a range of calls adapted to specific habitats or insect types. Bats that forage among trees have different calls than the ones hunting out in the open. Even within a single bat, the call is modulated in order to locate and hunt the insect. Changes in these calls as the hunt progresses provide possible information to the moth about the level of danger. As the bat circles around, the predator appears to be aimed at a distant point on the flight path of the moth. As the bat begins its final approach, there are subtle differences in the ultrasonic clicks. In hopes of acquiring a good meal, the bat alters its clicks because the distance between predator and prey is closing quickly. The bat needs to update its flight path quickly. Just before the bat makes its final capture move, the moth responds with its last second, life-saving maneuver.

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At this time, the moth has initiated two important defensive measures. First, the moth has stopped flapping its wings and dives straight to the ground. This alone might be enough of an evasive measure to escape predation, but it is possible that the bat could follow the emergency change in flight plans. The second behavior is its own set of clicks. These clicks are generated by the moth to jam the ultrasonic sonar of the bat. So, the moth hacks into the bats own hunting channel and produces a counter set of clicks. This new sound startles the bat and throws it off from following the diving behavior of the tiger moth. The startled bat was not expecting a last second jam of its own signal which has cause the bat to temporarily stop hunting.

11.2  The Science of Jamming and Diving Insects are arthropods, and as such, they possess one of the most prominent features of the arthropods: a hard exoskeleton. This exoskeleton is composed primarily of chitin and offers a protective outer layer for this group of animals. Despite this fairly widely known fact, there are a large number of aspects of the insect’s armor that are unknown outside of the science world. First off, the chitinous exoskeleton is not one continuous piece of skeleton. Rather, it resembles the classic medieval knight’s armor in that the body is made up of different sections or pieces of exoskeleton. In between the pieces, very flexible skin exists. The harden pieces of the exoskeleton exist where the insect needs the greatest protection and the least amount of flexibility, like the head capsule. Elsewhere on the insect body, like the abdomen, flexibility is needed where different body parts need to move (like the wings) or distend after feeding. Here, the armored pieces are connected by membranes. The second misconception is that the exoskeleton is completely solid although there are many different holes that exist within an insect’s exoskeleton. The most prominent holes are the spiracles. These are small holes, usually located along the abdomen, where oxygen is exchanged between the inside and outside elements of the insect’s body. Just behind the spiracles exist the respiratory tissue of the insect called the trachea. Between the holes (such as the spiracles) and the membranous sections of the exoskeleton, the insect’s external body has a great deal of flexibility and connection to the outside world. Finally, on the inside, the insect has numerous stretch receptors connecting the hard outer skeleton within the inner workings of the nervous system. These stretch receptors provide feedback to the insect’s brain on the movement of different body parts and how those movements supply stress and forces to their hard exoskeleton. So, the exoskeleton is extensively wired with thousands of receptors providing continuous feedback to the animal. Thus, the exoskeleton isn’t just a hard outer shell for the animal, and in these terms, the analogy to a medieval knight’s armor fails. The exoskeleton is a living, flexible, and vital organ for the animal as it goes about its daily labors. Tiger moths (in a subfamily Arctiinae) have evolved ears that use the hard exoskeleton as anchoring points. The ears of these animals are actually not found on the

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head but on the side of the body between the thorax (front segment of a moth) and abdomen (hind end of a moth). Located between two chitinous elements, another hole (similar to the spiracles) is located on either side of the moth. Instead of an open hole, the tiger moths (and other moths with ears) have a thin membrane stretched across the opening. In this construction, the basic elements of the ear are similar to that of our own ears. Depending upon the exact species, the neural configuration is different. For a closely related family of moths (Noctuoidea), two sensory cells are directly connected to the tympanic membrane. Thus, when the membrane vibrates in response to the bat calls, the sensory cells are activated. These moths are most sensitive to sounds in the 20–100 kHz range. The champion for insect hearing is currently the waxwing moth which can detect sounds as high as 300 kHz in range. In tiger moths, the ears are called the tympanal organ and are located on the thorax itself. The ears on all of these moths are tuned such that they can detect the ultrasonic sounds of hunting bats. Yet, hearing the sounds of an oncoming predator (like the music in a horror film) is still not enough to save these moths from becoming prey. The tiger moths have another organ specifically designed for sound production. This organ is called a tymbal and is found on the metathorax which is closer to the head than the tympanal organ. Similar in shape to the tympanal organ, the tymbal organ is a flexible membrane that sits on the exoskeleton of the moth. Unlike the tympanal organ, which is innervated by sensory cells, the inside of the tymbal membrane has a connection to the tymbal muscle. This muscle serves to vibrate the membrane to produce the moth’s anti-bat sounds. A large number of insects, including the cicadids that produce their characteristic sound, have different types of tymbal organs. Some organs have a smooth surface which produce single clicks. Others are striated, with structures called microtymbals, and produce a rapid series of clicks in response to bat vocalizations. The size and structure of the tymbal organ determines the frequency of clicks produced (Fig. 11.1).

Fig. 11.1  The tymbal organ. Many moths have a thin membrane near their wings that functions as an ear. The membrane is part of the tymbal organ that is sensitive to the high-­ frequency calls of bats and generates clicks

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What is even more fascinating about the tiger moths’ response is how they couple the detection of bat signals with the production of their own sound. It appears as if the moths jam the bat’s echolocating ability. In order for the moth to do this, their own sound production has to be intense enough and quick enough to arrive at the bat’s ears the same time as the returning echo from the bats own sound. This has shown to be the case. Tiger moths produce an intense sound upon hearing the bat’s calls, as loud as 90 dB close to the bat. In horror movie terms, that means the hero or heroine would scream at the movie monster from a distance of 200  m. This scream would be so loud that the monster would be stunned and possibly temporarily deaf. If the monster was listening to your footsteps in order to track you, this would be the perfect time to escape. This is exactly what the tiger moth does. So, the moth has evolved the ability to hear sounds in the ultrasonic range produced by the bat and send its own loud “scream” back that temporarily stuns the hunter. Quickly following this, the moth stops flapping its wings and goes into a dive. Thus, taking itself out of the original flight path of the bat and onto freedom.

Chapter 12

Sound Beneath the Waves

Crayfish are wonderful organisms for science. As a keystone species, the crayfish plays an important role in the ecosystem of freshwater bodies and has an amazing set of behaviors primarily driven by their sense of smell. The downside of these organisms is that they are aquatic and nocturnal. Given my current research location, the Upper Midwest of the United States, this often means late-night dives to the bottom of fairly cold lakes. My usual location of these dives is Douglas Lake at the University of Michigan Biological Station. I have worked at the station for over 20 different summers. I am lucky enough to teach a summer limnology course and then perform my research activities on days that I don’t teach. This arrangement affords me a small, but sufficient, cabin on the shores of Douglas Lake. The cabin sits about 50 ft from the shore and is an excellent makeshift dive shop for my research team. Inside the cabin, I store the regulators and flashlights, while the scuba tanks are chained against the back of the cabin. Near the shore, we have a homemade scuba rack that holds all of our wet suits, fins, and masks. Finally, about 20 ft from the scuba rack is our trusty research “vessel,” the Black Phoenix. The Black Phoenix is really nothing more than a 30-year-old pontoon boat consisting of a wooden platform sitting on top of the two pontoons with a small engine attached to the back. Not much of a boat, but it is our boat. Most of our research dives entail one of two objects. The first is to take down handheld video cameras to document and monitor crayfish behavior in their natural settings. The second, and more time-intensive task, is to place a stationary underwater camera on the bottom of the lake over active crayfish burrows. The camera is powered by a series of batteries that sit on shore and feed the camera through a 150 m underwater cable. Finally, the video images captured by the camera are sent back to shore and recorded on a DVR enclosed in a waterproof case. This last task takes a dedicated and well-trained team of researchers to pull off. Research nights often start with a gathering of the team at my cabin to assign the tasks and get the equipment ready. One person needs to stay on shore with the batteries and DVR in order to communicate to the field team on the quality of the video images. Usually two people are assigned the above-water tasks of driving the boat, © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_12

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communicating with shore, and prepping the divers. On good nights, we have three divers who start getting ready during the short boat ride out to our research site. The goals of one of these trips are to, first, find an active crayfish burrow and mark it. Second, move the boat to this location, and give the three divers the heavy metal quadpod that holds the camera above the burrow. Once this is placed above the burrow, the dive team returns to the surface to get the camera and cables and attaches the camera to the quadpod. The reason that three divers is ideal is that one diver stays on the bottom with a powerful flashlight to guide the other divers to the underwater research location. Finally, once the camera is attached, two divers stay on the bottom, while one diver surfaces to talk with the boat team. In a series of rapid communications, the boat team calls the shore to check on the video image. The shore person then supplies commands to the boat team on how to move or focus the camera image. This command is relayed to the diver, who, subsequently, returns to the bottom to work with the rest of the dive team to move the camera into the proper position. Unfortunately for the dive team, this last bit is often repeated several times until we get just the right image. Communicating underwater is a particularly tricky thing while setting up our underwater research. Certainly, our ability to produce sound is limited to banging on tanks with the end of knives. We could use Morse code, but this would be an extremely slow process under frigid conditions. So, we resort to our own style of hand signals that contained a set of pointing at people or directions, hand waves to signal swimming, and mixtures of other gestures. While this works for our needs, the method is cumbersome and less than clear. We don’t have any predefined set of gestures that everyone is familiar with as we make the language up on the fly. A far more efficient method would be the ability to generate and receive sound waves at the bottom of the lake. Human vocal cords just aren’t designed for use in a dense medium like water. Any attempt results in a series of bubbles that do little to carry the intricacies of human language. There exists underwater microphones and speakers that can produce and receive sounds at depth, and these systems work fairly well. If we had the money to purchase this equipment, we certainly would have. Although, we could not use sounds as a source of information for our camera setup, this doesn’t mean that the use of sounds underwater is ruled out. Most people are familiar with the ability of marine mammals to use sounds and songs as means of communicating throughout long distances in the oceans. Dolphins and porpoises use clicks, squeaks, and other sounds to communicate during hunting and for social situations. The champion of underwater sound production has to be the humpback whale. These whales actually produce songs that last over 30 min and are heavily used during mating seasons. Male humpback whales will use these long vocalizations to woo females or even compete against other males for a female’s attention. The details of the whale song are quite complex and can exist of an underlying theme that is often repeated. This theme can be overlaid with multiple phrases that are strung together to complete the entire song. These songs can have regional dialects, and the exact structure of the songs changes or evolves over time.

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The toothed whales (orcas, dolphins, and porpoises) produce clicks and whistles and do so by moving air around a complex system of air sacks and some specialized tissues that vibrate. These sounds are focused through a large fatty mass located within an organ called the melon of the animal. The melon is the rounded shaped organ above the mouth that is most prominent on dolphins. The melon functions in a similar way to the fatty tissue located on the bottom of the elephant’s foot. The baleen whales produce sound much differently than their toothed cousins. Inside of their larynx is a rigid U-shaped fold of tissue. This tissue operates very similarly to the vocal folds of terrestrial mammals and our own vocal cords. Next to the folds is an inflatable balloon-like structure called the laryngeal sac. Baleen whales have the ability to inflate this structure with air from their lungs and then force that air through the U-shaped folds. This causes the folds to vibrate, transferring those vibrations to the laryngeal sac. From here, the vibrations are sent out into the water and form the songs of these whales. Marine mammals evolved from terrestrial mammals, so the similarity in the production of vocalizations can readily be seen. The clicks, songs, and sounds of marine mammals are well known, but there are thousands of fish species that also produce and hear sounds underwater. Just like the whales, fish can produce sounds to frighten off potential predators, to lure in potential mates, and in response to being frightened (potential warning calls). The interesting way that fish produce sounds is tied to their swimming. Living in a truly three-dimensional world, many fish need to be able to control their buoyancy. If they are too buoyant, they’ll rise to the surface of the lake or ocean and eventually be stuck there. If not buoyant enough, they’ll sink to the bottom. Neither of these situations produce a good outcome for the survival of the fish. Human divers face the same problem. Luckily for humans, we have invented a device called a BCD (or buoyancy control device) that we can inflate with air from the scuba tank or deflate with release valves. This allows experienced divers to control their depth rather precisely. Fish have a very similar device which may have served as the inspiration for the human device. A large range of fish have swim bladders. These are essentially inflatable bladders in the middle of their bodies. With a series of biological inputs and valves, fish can control the amount of air in the bladder which maintains their buoyancy and hence changes their depth within a lake or ocean. If you have ever played with any inflatable object (or a solid object with a flexible membrane on top of it like a drum), you might have noticed that striking the object or membrane creates vibrations. These vibrations are amplified by the inflated object or the walls of the drum. The degree of the inflation or size of the object can determine the frequency of the vibrations and hence the types of sounds being produced. A fish with a swim bladder could create sounds by causing vibrations to form within the organ. One species of fish from the Caribbean that does this is none other than the red grouper.

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12.1  The Keith Moon of the Deep The red grouper, Epinephelus morio, is located within the warm waters of the Caribbean and can grow to a moderate size, roughly 25 kg. Highly territorial, the red grouper engages in a large number of social interactions throughout the year. These social interactions, including staking out territories, are where most of the acoustical communications take place. During these interactions, especially when there is a mixture of males and females, different types of sounds can be produced that are supposedly used for communication between and across sexes. Although we are just beginning to understand how these fish use sound within their habitats, they provide an excellent example of the adaptations that have evolved for both sound production and reception within the aquatic realm. Thankfully, the red grouper is not found at great depths, so we have a clear view of what these animals are doing during their social interactions. Likewise, because of their size, the sounds that they produce can be both felt and heard while diving with them. The warm Caribbean waters make observing the grouper a pleasant experience. Diving under clear and warm conditions, one can get a sense of what it means to fly as you gently float over the reefs. Groupers inhabit slightly deeper water than the surface and can often be found at a depth of 50 or more meters. Swimming between and among the reefs, the groupers are gentle creatures and can be found rather easily. The large-bodied fish can grow over a meter long, and they generally do not run and hide from lurking humans. Approaching the bottom of the ocean, it is possible to see more than a dozen red fish moving slowly around the coral heads. These groupers are setting up and defending territories around the reef heads. The territories are primarily used as mating grounds, and the groups will defend their territories vigorously. Despite the intensity of the interactions, the aggression groupers show to each other rarely rises to the level of physical violence. These animals use their “voices” to resolve their conflicts. Focusing on a singular large male will provide some insight into their use of sound in social situations. Within the behavioral sciences, when we watch a single animal and track its behavior, we call this animal the focal animal. In many cases, focusing on a single animal allows us to observe the evolved rituals which are just sequences of behaviors that minimize the potential for physical harm. In the case of these groupers, when another fish approaches our focal animal, we can record and track the vocal interactions. Thus, our cue to really listen in on the groupers begins when an intruder approaches our focal animal. As the intruder approaches, the focal grouper will generate a loud warning call. We wouldn’t actually hear it as much as we would feel it, as the water surrounding us would vibrate. The focal grouper begins to generate its calls to establish a territory with the other grouper. Upon closer inspection of the grouper’s belly, we would notice a slight and quick tremor of belly during the call. This is evidence of the call being sent out. The fast calls last only a few seconds and range anywhere from 40 to 200 Hz. So, the sound production is within the range where we can detect it as well

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as deep enough that we’ll feel the call as a vibration. We hear the calls as short booms, thumps, or even grunts because of the low frequency with short durations. Imagine a drum filled with air that is hit once or twice in rapid succession. This analogy is similar to what is occurring inside of the grouper to produce this sound. For the focal animal, this is the first step in establishing a territory for spawning. The focal grouper feels as if this other grouper has infringed upon his territory, and as a result of this aggression, the focal group starts a series of acoustical calls in order to determine who will finally gain ownership of this territory. Depending on the intensity and type of signals being produced, the intruding groupers will make decisions on whether to retreat from this territory or continue to fight. In essence, these two animals are sizing each other up by the nature of their calls. If the right call is produced, the eventual loser will slowly swim away. If not, the calling will continue until one animal decides that they have had enough fighting for the day. If the intruder choses to stay and fight, it will begin a series of response calls. In this case, the intruder has decided to take up the fight and produces a different call. The red grouper can generate a number of different calls. They can alter the fundamental frequency of the call between the ranges that written above. They can also alter the duration of each call between 1 and 4 seconds. Within each call, the animal can produce a series of thumps or booms that vary in number from as short as three individual sounds to pulse trains of thumps that can number in the teens. We don’t understand the meaning of these individual calls, but we do know that these various structures of calls play a large role in both territoriality and courtship behavior. As these two groupers continue to fight for this territory, they’ll display a wide range of calls, thumps, and other sounds. If the match continues, the calls will increase in intensity and sometimes duration. It is the grouper’s way of increasing their aggression. The focal animal has responded to the challenging male. This time, the focal grouper has increased the frequency of its sound. In addition, the intensity of the call and the number of pulses have increased. It appears as if the focal grouper feels that it owns this territory, so he has increased the level of aggression reflected in the new calls. He is attempting to firmly establish he is the dominant animal here and the intruder needs to leave. Now, the intruding animal has to make a decision of whether to increase his return call or back off. Most likely, the challenger male has a nearby territory and is trying to extend the boundaries of his territory into this area. This fight has escalated to a critical juncture: to end or escalate the aggressive interaction. The challenger shall determine this now. Without waiting too long, the focal grouper begins another set of calls in response to the challenger’s last call. Maybe the fish has noticed that his opponent has hesitated in responding and produced a less robust call. If so, the additional calls should signal the end of this interaction. The first call, by the challenging male, was a weak response to the focal male’s intensified call. This means the challenging male is likely getting ready to retreat and concede this interaction to our focal animal. The focal animal, in response to the weakened call, has further increased his intensity.

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The changes in the call structure and intensity, the challenger is weakening and focal animal is still increasing, clearly signal that this fight is coming to an end. Most of these types of socially aggressive interactions are solved by a ritualistic series of displays or calls. Even the winner of an intensely physical interaction could receive grievous injuries, so across the animal kingdom, it is possible to see these types of interactions solved before they escalate into physical battles. Today, our focal grouper has established his territory boundaries through the series of calls and responses.

12.2  The Science of the Fishy Sound Fish have a number of different mechanisms in which they produce sound and calls underwater. These include stridulations (rubbing two hard and serrated structures together like crickets and cicadids), hydrodynamically (swimming with fins produces pressure waves), and drumming. Despite the diversity of mechanisms, this section will focus on the way that a large group of fish have evolved to produce a wide array of sounds: underwater drumming. Of course, if drumming produces sounds, there has to be a drum and a drummer. The large number of marine and freshwater fish can be primarily divided into two groups of organisms. Other groups exist, but are relatively depauperate. The first group of fish contain those animals with cartilaginous skeletons: the Chondrichthyes. This group contains the sharks and rays of the aquatic habitat. The larger group of fish are called the Osteichthyes. These animals have a bony skeleton and include most of the other fish in the marine and freshwater habitat. These two groups are divided by a number of different adaptations, but for the purpose of our discussion, the most important adaptation found only in the bony fish is the swim bladder. The swim bladder is an organ that is like an internal balloon. If the organ is inflated, the fish will rise in the water column, and if deflated, the fish will sink. Depending upon the species of fish, the connections to the swim bladder differ, but there is usually a gas gland that is highly vascularized. Another organ, the rete mirabile, also participates in the control of gas entering and exiting the swim bladder. Oxygen (and some other gases) in the bloodstream, gathered from the surrounding water via the gills, is pumped into and out of the swim bladder depending on the depth that is desired by the fish (Fig. 12.1). One reoccurring theme within the evolution of life is either the repurposing of or additional use of organs for other functions. The swim bladder’s primary function, for most fish, is to control the depth at which the fish is located. Yet, a gas-filled, flexible organ is also perfectly adapted for the generation or reception of vibrations (i.e., sound). As previously mentioned, a balloon or really any gas-filled object like the lungs or drums can produce vibrations if struck properly. In addition, the size or inflation of the object can influence the frequency of the sound being produced. A large set of tom-tom drums demonstrates this effect quite nicely. A quick search for

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Fig. 12.1  The fish’s swim bladder. The swim bladder of the fish is a gas-filled sack that vibrates in response to underwater sound. The bladder is connected to the inner ear of the fish which allows the animal to detect sound waves

the drum set of Neil Pert from the Canadian rock group Rush is an excellent illustration of the range of sizes and sounds that different-sized drums can produce. Thus, fish with swim bladders have a built-in drum right in the middle of their bodies. Not only is the drum there, the ability to modulate the level of inflation of the swim bladder gives the animal the potential to modulate the fundamental frequency being produced by the bladder. Still, even the best of rock drummers (like Neil Pert or Keith Moon) are useless unless they have ready access to a set of drumsticks. The drumsticks for many species of fish that produce sound with their swim bladder are a set of muscles that run alongside the bladder. Appropriately called the sonic muscles, the contraction of the muscles acts to vibrate the swim bladder, just as surely as striking a tom-tom with a wooden drum stick. The exact mechanism by which different fish create vibrations varies among different fish species. Some species (like the toadfish) insert the sonic muscles onto the surface of the swim bladder and create vibrations. Some species (like the thorny catfish) have the muscles attached to a thin bony plate that is used to strike the surface of the swim bladder. Other species have tendons or muscles that stretch across the swim bladder. Regardless of the exact structure of the muscle and bone, the functionality is the same. Control of the contraction of sonic muscles creates the fundamental frequency of the sound by vibrating the gas-filled swim bladder. The contractions and expansions of the swim bladder are incredibly small, yet powerful enough to create a pressure (sound) wave that travels outward from the animal. The speed of these contractions is incredible even with the low-frequency calls of the groupers. The lower frequency of calls (40 Hz) means that these drumming muscles are contracting at a speed of 40 times a second. The higher-frequency calls described in the scenario above (180 Hz) is 4.5 times faster! Now that is a rhythm that even the most

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ardent fan of speed rock would find incredible. The production of underwater sound is only half of the scientific answer. Once something is produced, how do the fish hear the sounds? The problem with detecting acoustical signals underwater is that most fish have the same density as water. Thus, the pressure wave created by contracting swim bladders quickly passes through the fish as if it wasn’t there. In terrestrial environments, animals have a much higher density than the surrounding medium (air); thus, sound waves move our sensory hairs in our inner ear, while our bodies stay stationary. Sound waves, in water, move the fish and hair cells in a similar fashion, so it seems like detection of the sound is not possible without some modifications. The ear of fish is remarkably similar in design to the part of our inner ear. As a reminder, our inner ear contains two sensory elements. The first is the cochlea which is a spiral-shaped bone that contains a membrane and nerve cells responsible for the hearing of sounds. The other sensory part of the inner ear is the semicircular ducts. These are three loops that are at right angles to each other and are part of our vestibular system. The vestibular system is designed to help us detect the directions up and down, motion, and acceleration. Each loop is sensitive to motion in one of the three planes that are part of our three-dimensional world. The fish’s ear is composed of two different parts. One part contains the three semicircular canals, and the other part is the utriculus. These two parts of the inner ear are responsible for encoding information about equilibrium, similar to the canals in our ears. The second part of the ear (the utriculus) also has two parts, the sacculus and the lagena. These two parts play a role in sound transduction for the fish. Yet, the problem of acoustical density still exists because all these parts are roughly the same density as the surrounding water. Inside each of these structures, a separate type of bone can be found called the otolith. The otolith is composed of calcium and other minerals and, as a result, is much denser than the surrounding water. The otolith rests on a membrane that can be described as a bed of spikes. The spikes are thousands of hair cells arranged in a number of different directions. As a reminder, hair cells have a series of cilia that are aligned from the shortest to the longest. This alignment provides directionality to the hair cells. If a sound stimulus causes all the cilia to bend toward the longest, the cell creates a positive response. If bent to the opposite direction, the cell creates a negative response. The otolith, being denser than both the fish and surrounding water, moves more slowly and less intensely than the fish or water. Thus, the differential movement of the otolith and the fish (with its bed of hair cells) allows the animal to detect sound from the excitement of all those hair cells. All the hair cells that are excited send their signals to the brain of the fish which is processed and received as sound waves. Thus, the vibration of one grouper’s swim bladder creates motion in the surrounding water. This motion travels through the water, and when it arrives at the receiving fish, the movement of the otolith (relative to the hair cells) creates the perception of sound in the fish. The prominence of the swim bladder in the production of sound is really only half of the story though. The swim bladder can actually be involved in the reception of sound. As another comparison, the human ear is the tympanic membrane (eardrum) that is connected

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to the three little bones of the inner ear. This design allows for the tympanic ­membrane and bones to amplify the sound for the inner ear. Without these structures, our ears would be far less sensitive than they currently are. Although fish don’t have eardrums, they do have something that can act as a drum as noted above: the swim bladder. The sensitivity to sound of different fish correlates quite nicely with the inverse of the distance between the inner ear and swim bladder. In other words, if the inner ear is close to the swim bladder, then the fish have an excellent sensitivity to underwater sounds. Conversely, if the inner ear is located far away from the swim bladder or completely absent (as in sharks and rays), the sensitivity of the fish to sounds decreases dramatically. The swim bladder, filled with gases, is considerably lighter in density than either the fish or the surrounding water. Thus, as sound waves move through the fish, the swim bladder vibrates quite readily. The vibration consists of rapid contractions and expansions as the sound (pressure) waves moves through the animal. Some species of fish have internal bones that connect the swim bladder to the inner ear in much the same way that the tympanic membrane is connected to our inner ear through the three little bones mentioned above. As the swim bladder vibrates, the bones move in conjunction with the swim bladder and transfer that motion all the way to the inner ear. These bones are actually a modification of the fish’s vertebrae. The first three parts of the backbone have been shrunk and modified by the forces of evolution to function as part of the hearing system of fish. In many ways, creating sound waves to protect territories and court females is so critical that two structures have been modified from their original function to help these animals produce and receive sounds. The swim bladder originally evolved as a tool to help fish maintain and control their buoyancy, but now creates and responds to sound waves as well. The backbone, which protects the spinal cord and provides stability for the skeletal structure of the fish, has lost its first three vertebrae to help amplify important underwater sounds. As we shall see in the next chapter, the incredible evolution of the swim bladder has resulted in an amazing story of underwater love.

Chapter 13

The Lover’s Voice

During my more intensive writing sessions at a local bakery, I am surrounded by sounds. My most creative periods tend to be in the morning. It seems as if my muses leave me around 2:00 pm, so I make sure to set aside at least an hour of writing every morning. The morning crowd at the bakery contains a set of regular patrons gathered in small little groups. The conversation in these morning groups tends to be quite casual. After having listened to their words and studied their gestures on numerous occasions, it appears as if the conversations are about the previous day’s events or some local issue. The largest group, usually about ten older gentlemen, are typically located near the middle of the bakery. A smaller group of women sit themselves near the window and occasionally find themselves conversing about the people walking by the windows. Finally, the third group sits near my favorite writing spot. I try to locate myself off to the far side of the bakery. Away from windows and the central area of the bakery, my choice of writing location is based on minimizing visual and auditory distractions. This third group sits behind me, and their conversations are focused on religion. A dedicated Bible group, they meet almost daily to quietly discuss issues regarding their most recent readings. Thankfully, a good set of headphones, background music, and a focus on my computer screen are enough to separate my mind from the events and conversations of the bakery. During any momentary period that I happen to be stuck on a certain idea or sentence, I’ll take my headphones off and surreptitiously listen into the conversations. I’ll even walk over to refill my drink to get up and hear different conversations. These brief distractions are often enough to get my writing flowing again. I have been writing and listening at this bakery enough that I can recognize the voices of many of the groups’ participants. The most recognizable voice happens to be the leader of the Bible study group behind me. The gentleman leading the discussion is always dressed in jeans and typically has a plaid shirt on. A small baseball cap is either on his head or on the small table next to his chair. I am not sure I could recognize his face, as he and his group are usually behind me. However, I am pretty positive I could recognize his voice if he randomly called me on the phone. His voice is a little deeper than a baritone, but not © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_13

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quite a tenor. He is probably one of the few Americans left that actually pronounces a hard “t” as opposed to letting the “t” fade into the end of a word. If I hear him pronounce the words “tight,” “left,” or “might,” the characteristic “click” of the last “t” is clearly evident. Finally, if I really listen closely to his speech pattern, I think I can detect a hint of New England accent on certain words. I have spent much more time listening to their voices and creating a similar set of descriptions rather than studying their faces. They could all probably walk right past me and I would not recognize any of them. If they happened to be standing behind me in a checkout line and started talking, I would recognize most of them fairly instantly. Despite our heavy reliance on visual cues to perform facial recognition, we can, and often do, also use the unique tone, speech patterns, and dialectical differences in word choice to perform this same recognition task. This is obviously important when listening to podcasts, music, or talk shows when a visual image of the speaker is impossible. Just listening to few words of a song, we can easily discern the name of the singer. The voice of an old friend over a cell phone call will be recognizable despite long years apart. As an example of my own life, my office door is usually open for students to pop by with their questions. Yet, if I have a lot of writing or editing to do (and I am not at my morning bakery spot), I’ll close the door for some solitude. Even with the door close, I often get graduate students who will knock and ask if they can come in. The sound of their footsteps and the unique rhythm and intensity of their knock are excellent clues to the person behind the door, even before they announce their presence. The use of sound to recognize individuals has a much deeper evolutionary root than listening to modern media or identifying individuals on the other side of a door. Throughout evolutionary history, biology has been awash with mechanisms to determine group status. Groups could be as large as bacteria colonies and animal troops or as small as a mating pair. The importance of establishing whether an individual belongs within or outside of a certain group is tied to resource and reproductive effort. The “end game” of evolution is to pass along your set of genes in as high of an abundance as possible. Your own offspring are the best vehicle for passing along your genes, but brothers and sisters also contain a significant duplication of your genetic makeup. A little less related, cousins, aunts, and uncles carry some of your DNA. Thus, reliably identifying those individuals who belong in your family group is important when deciding whether to share resources like food and shelter. On a broader scale, determining those individuals that belong to larger social units is also important. Whether the unit is called a troop, pod, tribe, or some other name, the procurement of resources, defense of the unit, and shared reproductive effort is often associated with different levels of sociality. Thus, in-group members benefit from the efforts of other members. Interlopers, who would benefit from the shared resources of the group, but do not contribute, are the bane for sociality. As such, vocalizations, such as the songs of marine mammals, have evolved to detect which individuals really belong inside the group and are deserving of benefits as well as which individuals are out group members. Within our own lives, the recognition of family and friends through their individual voices carries with it a deep emotional attachment. The deepest of these

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c­ onnections is to our lovers and companions. A soft whisper while lying in bed, even in some half dream state, comforts us because of the emotional association between the sound and the whisperer. When times are bad, this same voice can supply us with a calming reassurance that they’ll be there through thick and thin during our entire lives. This long-term relationship creates a bond that is quite difficult to break. A number of different animals are monogamous and will mate for life. Here too, just as in humans, the “voice” of a mated partner can carry great significance. One such interesting example is the brightly colored butterflyfish. Their moniker is due to the resemblance to butterflies in their color and diversity. These animals are small marine fish that range between 10 and 20  cm in length. They live in and among the coral reefs of warm climates. Found in the shallower regions of the coral reefs, butterflyfish usually lead a quiet, solitary life until they find a mate. Predominantly peaceful creatures, the butterflyfish can get quite aggressive when attempting to court. During this period, males will create a variety of sounds through different mechanisms as warning calls to other males. These sounds are used to create and defend territories in order to impress female butterflyfish in hopes of mating. During the mating process, a different set of sounds are created and used to bond the pair for life. If successful, the mating of the two butterflyfish will create a monogamous relationship that will last their entire life, and this relationship is filled with vocalizations that serve to identify each other. Once bonded, these fish are inseparable. They travel and hunt as constant companions.

13.1  Kiss the Girl Like the red grouper, butterflyfish are located within the warm coral reef habitats across the globe. Coral reefs are the home to many different species of organisms and can be considered an oasis surrounded by a desert (as far as productivity  is concerned) of an ocean. The abundant and diverse set of organisms that call reefs home creates a noisy habitat. Swimming fish, breaking waves, and vocal calls all create a sound party that can elevate background noises. Because of these loud background noises, fish that want to communicate with each other using sound have evolved special mechanisms that allow them to tune their sound production and hearing. Butterflyfish, as we shall see, have unique structures that allow them to create a large array of sounds. These sounds carry critical information that is used for territorial defense, mating cues, and other aspects of their behavioral ecology. One such fish is the pebbled butterflyfish, Chaetodon multicinctus. This particularly vocal species has vertical stripes that are brownish yellow on the dorsal and fade to white toward the ventral part of the animal. Characteristic of most butterflyfish, these specimens have a black vertical stripe that stretches across the eye. Fiercely territorial and monogamous, the male fish defends its territory and communicates with its mate using sound. As with the groupers of the previous chapter, intruding butterflyfish are seen as potential threats to both territory and mates.

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Once mated, the pair of fish are inseparable. Whether the daily activity is foraging, defending the territory, or tending to the nest, the pair are constantly with each other, communicating their needs and wants using a diversity of sounds. One of the most visually obvious forms of communication are head bobs. Males and females will move their head up and down to create small pressure waves that are detected as sound by the mate. The head bob produces a pulse train of pressure waves around 70 Hz and is mainly a form of communication between mates. It acts as a sort of greeting between lovers as they perform their daily chores. As the mated pair move around their territory, an intruder has entered their part of the coral reef. Once spotted, the pair of butterflyfish will drop everything that they are doing and immediately start defending their territory. As they move toward the intruder, the pair continues to stay close to each other. Strength in numbers is probably the guiding factor in their close grouping. In addition, two animals can generate more sounds than any unmated individual. While the head bobs are usually for intrapair communication, this pair needs some type of sound that is more intense. For this, the male generates what is called a tail slap. The higher density of water (compared to air) creates the perfect medium for these types of signals. The tail slap is one of its most aggressive sounds. The male quickly moves its caudal fin (tail) against its body producing a sound wave from the slap. This is a loud warning call to the intruder. The second most aggressive call is a body pulse. The body pulse produces a singular powerful wave traveling outward from the male butterflyfish and is produced by the swim bladder of the animal. The body pulse and tail slap are more “shouts” or warnings to intruders. There isn’t much complexity to these signals. The purpose of these two sounds is to create a powerful and loud pressure wave to intimidate intruders. These signals work quite well as intruders are scared off rather quickly. After successfully defending their territory against an intruder, the pair will return to their private conversation. Primarily using the head bob, the animals can uniquely identify each other. Subtle differences between the cadence of the bob, the intensity of the signal, and even frequency could be used to identify individuals. This is the sound of their lover’s voice. The intensity of each of these signals is correlated strongly with the fish’s body size. The larger individuals produce more intense sounds, but the cadence and frequencies are signatures of their mates.

13.2  The Science of Singing Silly Love Songs The butterflyfish interaction outlined above requires two distinct and related components. First, the animals need a number of different mechanisms to produce a variety of sounds. Second, these animals require a sense of hearing tuned to these different sets of calls and sounds. One of the best researched examples of underwater communication, the butterflyfish provides an excellent example of how the evolution of hearing and sound production can produce a detailed communication system. As mentioned in the previous chapter, many teleost fish (bony fish) have swim bladders

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that allow them to control their buoyancy in the water. Also covered in the previous chapter, this swim bladder has also evolved into a resonance structure for underwater sound. As sound (pressure waves) arrives at the swim bladder, the inflated organ begins to vibrate in resonance with the pressure waves. This intense vibration is then transferred to different structures within the fish to be detected as sound. While some fish have the ability to vibrate the swim bladder to produce sound, butterflyfish appear to lack this ability. Thus, for this group of coral reef fish, the bladder serves as a specialized organ for the detection of sounds as well as other functions (locomotion, buoyancy, and even feeding behavior). For many fish, the swim bladder is a rather pedestrian structure simply shaped like a tubular balloon. In the butterflyfish, many of the different species have unique swim bladders with extensions called horns. These horns are located on the anterior portion of the swim bladder. These swim bladders resemble a Mickey Mouse balloon that has been really stretched and elongated. The variety of horns regarding to their shape, length, and position is immense among the butterflyfish. Some of the horns split off into a “v” and others form a more “u” shape. Still, the main characteristic shared across the butterflyfish is the close proximity of these horns to the ear of the fish (Fig. 13.1). The horns sit very close to a structure called the otic capsule. This capsule is a bone that surrounds or contains the sensory structures of the inner ear. In butterflyfish, the otic capsule is very thin and is close to the saccular macula. The thinning of this usually thick bone would facilitate the transmission of pressure waves across the bone. The saccular macula contains sensory cells that are sensitive to sounds or pressure waves. So, the location of these extended horns places them right next to the sensory hairs that detect sound. The much smaller horns of the swim bladder likely amplify the vibrations being produced in the larger portion of the swim bladder, which in turn is transmitted quite quickly and efficiently to the inner ear structure of the fish. As such, these fish should be far more sensitive to sound than fish without swim bladder horns and have a much greater frequency range over which they are sensitive. The butterflyfish, as a large and diverse group of fish, do indeed Fig. 13.1  Horns of the butterflyfish. The group of fish known as the butterflyfish have evolved a diverse and elaborate set of horns at the front end of their swim bladder. The distinctive shape allows each species of fish to produce and hear different sounds

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have higher sensitives and broader frequency ranges than other fish. Yet hearing sound is only half of the story, these animals also have a wide diversity of sound production too. Because of the increased density of water (compared to air), the production of detectable sound waves has a much greater diversity of mechanisms than what is usually found on land. Even the simple action of swimming produces a pressure wave that can be detected as “sound.” Instead of just using vocal chords (as terrestrial vertebrates do), underwater animals can produce sounds with fins, tails, body shakes, and even head bobs. The butterflyfish have certainly taken advantage of these mechanisms. Each of these sound-producing mechanisms has unique and special meaning to the mated butterflyfish, as evidenced by the type of behaviors that are exhibited as a result of hearing different sounds. The exact language or code of signals has not been entirely worked out. Imagine attempting to understand a foreign language by just watching two people interact. A tough task indeed, but behavioral biologists have been working on that task for a long time. Head bobs are a common behavior and are used in communicating to mates and intruders. Tail slaps, though, are most closely related to aggressive interactions with intruders. In addition, these animals can create pressure waves using their swim bladder, body shakes, and other fins, like the pectoral fins. Having a large diversity of sound-producing mechanism creates the possibility of language or at least the rudimentary beginnings of a language. In the butterflyfish, it appears as if that language reinforces the monogamous mating that these species form. The horns on the swim bladder and their ability to tune the ears of the fish to these sounds are an excellent example of natural selection. The ability to recognize and respond to a lover’s and companion’s voice, whether human or fish, is critical in monogamous species. The head bobs and body shakes are the butterflyfish’s whisper of “I love you” and shows that we aren’t all that different in many ways.

Chapter 14

The Power of Sound

Despite the preponderance of visual stimuli in our world, we use sound and words as the primary mechanism of communication between each other. From the powerful speeches of Martin Luther King Jr. and Abraham Lincoln to the pillow talk between lovers, we create sound to carry our hopes, dreams, and desires. Whether we are greeting each other after a long absence (like the elephants) or calling out to our significant other (like the butterflyfish), it is our words that carry information and emotion to each other. Even when we are not talking to each other, we fill our world with songs, videos, and movies that challenge us to think, console us when we are sad, fill us with joy, or even cause us to dance in celebration. In other ways, our words are how we define who we are. With words, our promises create an ethical bond with those to whom we make promises. In marriages, a simple nod in response to vows is not sufficient; the words “I do” must be acknowledged and spoken to create that relationship. For many personal dealings, verbally accepting a deal finally seals the relationship. Thus, sounds, either spoken or sung, are a central and fundamental structure of our society. Beyond social aspects, the world of sound is an essential aspect of our survival. The presence of a snapping twig tells us we are not alone on a hike. The sound of birds singing provides us with a reassurance that we are safe in an outdoor world. The bubbling of rivers or the calm crashing of waves are clear indicators of water. Even within our urban habitats, the honks of vehicles, the shouts of pedestrians, and the calls of street-side merchants allow us to navigate our world in a successful way. These same types of sounds are just as important within the animal world, but we are oblivious to those sounds that are outside of our capabilities. The nighttime struggle for existence between the hunting bat and the fleeing moth is played out in sounds inaudible to us. The deep rumbles of the savannah or low-frequency calls under the waves play an important part of the social aspects of elephants and butterflyfish, respectively. These four animals are not the only ones that rely on sounds to manage their lives. The entirety of nature is filled with animal music that we fail to hear. This is particularly true for those habitats that lack visual signals, which includes the majority of habitats on this Earth. Over seventy percent of Earth’s © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_14

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s­ urface is covered with water, and some of these aquatic habitats extend for miles deeper than light penetrates. Terrestrial habitats, such as caves, dense forests, and underground habitats, often exist in the absence of light as well. If we include nocturnal organisms, the number of environments devoid of visual signals increases tremendously. However, all of these habitats have sound. The organisms that live within these lightless environments have developed keen senses of hearing, and some have even developed a sort of protolanguage that uses a number of different sound-generating mechanisms. This acoustical language of animals is in trouble because of human activities. We have developed a society that creates a background noise that makes these natural sounds difficult to discern. Our urban centers are rarely absent of traffic, airplanes, or other human activities that generate sounds that unintentionally disrupt animal communication. Bird populations that live in or around cities have learned to alter their songs in response to this background noise. Even in aquatic habitats, boating, drilling, and shipping activity creates increased noise that has been shown to cause problems when animals try to communicate. Animals are faced with situations that are akin to having a meaningful conversation while stuck inside a Las Vegas night club. We have the choice to simply leave the night club and maybe head to a coffee shop to continue our talk. Unfortunately, animals aren’t simply able to leave their habitats and find nature’s equivalent of a coffee shop. The stories covered in this section of the book are only a small sample of how animals use acoustical signals to communicate. Hopefully, these stories can shed some insight into that part of the soundscape that remains elusive to our ears, and we can use this information to manage or even eliminate the production of our noise.

Part IV

Olfaction

For the sense of smell, almost more than any other, has the power to recall memories and it is a pity that we use it so little. —Rachel Carson

Chapter 15

The Smell of Warm Bread

I do most of my writing in my favorite bakery. Using headphones to channel a carefully chosen set of songs, I drown out the small din of conversation around me. Once I get my computer running and fan out my papers, the words seem to flow almost effortlessly at the best of times. Of course, there are other times that producing words on paper feels like pulling teeth, but these times are fairly intermittent. In part, the familiarity of the visual scene and the music helps me ignore the extraneous stimuli and write. I can find other locations that will provide me the visual and auditory solitude in order to write, but the last missing sensory piece is the olfactory system. My best writing times are usually in the morning, and the aromas of a morning bakery are a Mozartian symphony of odors. As a side, we perceive odors more akin to hearing than vision. In detecting visual signals, we blend the underlying singular signals together into a new gestalt. For example, blue and yellow paint, when mixed together, produce a green color. Try as we might, we cannot see the original blue and yellow pigments. When listening to a piece of music, say Bargain by The Who, we can focus our attention on different elements of the underlying individual instruments. The wonderful bass by John Entwistle and the fabulous drumming by Keith Moon play against the vocals of Roger Daltrey or the guitar riffs by Pete Townshend. We can also selectively choose to listen to the compilation of sounds as a single gestalt. My morning bakery is a complex aria of different olfactory stimuli. The olfactory bass, which provides the underlying rhythm to the song, has to be the different brews of coffee waiting to be consumed by the customers. This bakery usually has three blends out during the morning rush. The first tends to be a hearty and aromatic dark roast. Next is a lighter breakfast blend, and finally, there is usually a flavored coffee such as hazelnut or French vanilla. Even sitting in my far-off corner, a deep breath will allow me to relish the interplay of these odors. The syncopated beat of the drums is represented by the different breads that they are baking for the day. Every time the oven is opened and a new batch is drawn out to cool, the smell of warm bread is released to the bakery. The aromas of coffee and bread would be © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_15

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enough on their own to create a wonderful sensory landscape. Of course, the morning clientele of the bakery are coming in for a breakfast as well as coffee. So, the odors of eggs, bacon, and soufflés are added to the olfactory landscape in a similar fashion that guitar play is placed on top of the bass and drums. The final pieces, the vocals of my morning olfactory landscape, have to be the sweetness of the bagels and pastries that line the front counter. Closing my eyes, I can take an olfactory stroll around the room and visit the coffee, cooling breads, breakfast food, and pastries in turn. At each stop, I can focus my attention on each individual set of odors to fully appreciate the feelings and sensations created by the chemicals swirling around in the air. Opening my eyes and breathing deeply, I can now combine all of these odors into a singular perception called the bakery. The fused nature of these odors creates a set of perceptions that seem to stimulate my writing. Even on those days when I am not “feeling” the writing, a trip to the bakery seems to remove any temporary writer’s block that I might have. The information gathered through our olfactory system is systematically processed differently than the visual and auditory signals covered in the previous two sections. Those signals are sent directly to our cortex in order to be processed by the cognitive parts of our brain. This means that we think about these signals first and then attach emotional responses to the stimuli. Conversely, olfactory signals are routed through the limbic system of our brains which influences or controls our emotional responses. After a visit to this part of the brain, the olfactory signals are sent along to the cognitive part of our brain. Thus, we “feel” aromas first before we begin to think about them. This seemingly simple twist in processing sequence is why olfactory memories, as well as our emotional responses to odors, are more powerful and less controllable than our responses to either visual or auditory signals. Humans are not the only animals that process odors in this fashion, as a large and diverse set of animals receive odor signals in a similar way. In addition to evoking feelings, during the reception of odors, many animals have their physiology heavily influenced by the reception of different chemical signals. Within mammals, many different aspects of reproductive physiology are altered by the presence of chemical signals. Within rodents specifically, spontaneous abortions can be induced when a new dominant male (and his odorous urine) arrives to a nest. The estrous cycle of primates is influenced by dominant female and male odors. Outside the group of mammals, the queens of different social insects create odors that stop the reproductive cycle in other females. Just the presence of reproductive pheromones will drive male moths into a sequence of behaviors designed to locate and copulate with female moths. I frequently refer to chemical signals as the ninja signal because these signals can sneak their way into the nervous system of the receiver and alter physiology without the receiver being aware of the changes that are occurring. Even with humans, studies have shown that odors can alter the physiology of the receiver without them being aware that the odors are present. In sheep, certain odors connected with the birth of the lambs reinforce the maternal connection by altering the neurochemical oxytocin in the mother’s brain. Shepherds, even without knowing the underlying mechanisms, use this phenomenon to get sheep to adopt lambs

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whose mothers have died during childbirth. The smell of the baby’s head evokes emotional attachment within females, and this attachment is stronger for women than men. This emotional attachment that is associated with our chemical senses is probably part real and part developed from our fascination of pheromones. First discovered in insects, the concept of a sex pheromone has been promoted by shady businesses for centuries. Our search for that one smell or drug that will make us irresistible to the opposite sex probably lies within the need to reproduce as one of the driving factors of natural selection. The misplaced concept of the pheromone is that a single rare sniff of a magical compound produces a “love zombie” in the receiver where they think of nothing but their attraction to the owner of the scent. In reality, insect pheromones, which are the most studied and understood of the many different pheromones, create a cascade of behaviors in the males that still depend on decision-making within the male moth. First the male decides to start to warm up its flight muscles by flapping its wings. Next, it takes to the air and begins its search pattern. The pattern is a combination of straight upwind surges followed by a side to side casting behavior. This behavior is repeated until the male hones in on the female, which can be many kilometers away. Once the female is found, the male lands on the tree, bush, or twig that the female has called from and begins a specific walking pattern until the female is found. Then, and only then, can the reproductive event take place. Each of these steps involves decisions, which need not be conscious, but rarely turned off until mating occurs. Thus, even in the insect world, pheromones don’t produce the same types of behaviors portrayed in popular media. Pheromones are deeply involved in the development and attachment associated with relationships, even in the insect world. For many moth species, the relationship is often a long distant one. Except when mating, moths are not very gregarious and spend most of their time feeding. Eschewing the social life, moths live a lonely existence with very little interactions with the opposite sex. When mating time rolls around though, moths are a model system of hunting for and acquiring a mate at whatever cost. Far more gallant than any medieval tale of knights and damsels, male moths will fly heroic distances to find their distant love. Luckily for moths, pheromones are carried by the surrounding winds for miles, and the males are quite sensitive even to small concentrations of the female’s perfume. Females of many different species of moths will often climb trees or tall plants to get a high vantage point in which to release her sexual signals. Once the pheromone production has started, the female releases her signal in pulses into the prevailing winds. The winds, themselves, pick up this pulsed delivery to further break up the pheromone into wisps or filaments that travel downwind to the waiting male. The male must follow these filaments effectively in order to mate. This task sounds simple, but it may be the most challenging sensory task that any animal faces. As odors move down wind, the filaments of pheromones are stretched and torn such that there is no distinct concentration gradient of pheromone. Imagine trying to find that one hidden smelly sock that is causing a malodor in your room. The odors move around the room in varying concentrations and don’t necessarily point directly to the sock’s location. Male moths are faced with this same challenge, but on a much grander scale. To provide

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an example of this long distant love, we can travel to the southeastern part of the United States to visit the tobacco budworm, Heliothis virescens, in its native habitat. An unassuming creative, this moth is rather dull in coloration, being a brownish white in color, but is a champion at flying great distances to mate. Since they are often found in open fields and agricultural environments, watching these animals find their mates is a relatively easy behavior to track.

15.1  Long-Distance Relationships We can most likely find the tobacco budworm in fields that contain the plants that gave this moth its moniker. The large open fields of tobacco farms provide ample opportunity to find the males. The females, once mated, will lay their eggs on the crop plants where the larvae can cause tremendous devastation. So, the females find suitable habitat for oviposition (egg laying) and will begin their pheromone calling to the males. After finding a suitable plant, the female will climb up to the top and begin to exude the pheromone gland from the base of her abdomen. Here, she’ll pulse the release of the pheromone and advertise her readiness to mate. From there the wind takes those precious molecules to any males that happen to be waiting downwind. Walking through the tobacco fields, there are rows and rows of plants with large leaves. The leaves are green, rich, and really close to harvesting. The large, broad leaves hold themselves almost vertically on the plants that can reach over a meter in height. At this height, it might be difficult to see the romantic interplay between the males and females, but the moths are quite visible against the brilliant blue sky that lights the field. The males are tannish in color and can get as large as 3 cm. Their normal flight path is somewhat erratic and watching them makes one wonder if these animals may have imbibed a little too much alcohol. Neither moths, bees, nor butterflies are particularly graceful fliers. There are graceful insect fliers (dragonflies are one example), but most of the beautiful fliers are of the bird variety. Given the budworms flight behavior, the bobbing moth will be easy to spot on a day like this. On a tobacco plant, a female has made the long and arduous climb to the top. The top of the plant is where the wind velocity is highest. Chemical signals are unique among the senses in that the mechanism of dispersion is independent of the stimulus itself. Sound and light have energies that move them through the environment to their intended targets. Pheromones, as well as all other chemical signals, rely on wind or water to scatter them to their receivers. The pheromone is carried to the male on the tendrils and wisps of wind. While the common thought is that a smooth concentration gradient exists between the female and male, the reality is that the odor signal that the male moth is attempting the follow is quite chaotic. Turbulence and the twisting and turning of the wind mix up the odor and move it downwind in concentrated filaments. So, the male moth has quite a difficult task ahead of itself. He needs to use a signal that fluctuates in space and time to locate his mate. It is akin

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to finding a lost wallet on the dance floor of a night club with chaotic strobe lights in use. To perform this task with amazing efficiency, the male moth essentially has two flight modes. One mode is a straight upwind flight that is triggered by the detection of the female pheromone. This mode is called surging. A second mode is what the male is performing right now. The moth is flying across the wind, back and forth. The male performs this maneuver when he has lost the scent or if the scent isn’t arriving consistently at the antennae of the male. This mode is called casting. Being primarily visual creatures, we find it quite difficult to imagine what the moth is sensing. Most of our signals are fairly consistent. Lights don’t flicker on and off, and sounds don’t normally cut in and out. Yet, every single odor signal is periodic in nature. This means that even scents that are constantly being produced (perfumes on a person, scented candles in your home, or the warm, just out of the oven, chocolate chip cookies) arrive at our nose in pulses. For the male moth, this means that the pheromone smell is constantly on and off. In some ways, the male has to be constantly searching for the scent trail being produced by the wind blowing by the calling female. Watching the male fly, it is possible to see the switch between these two strategies. As the male stops the casting behavior, it makes a large and relatively fast movement straight upwind. This behavior means that the female pheromone is stimulating him at the right frequency. Imagine walking into a hot kitchen where someone is cooking with a lot of garlic and is using fans to cool themselves off. Initially, you would smell a large dose of garlic as you enter the kitchen. Then, when the fans change direction similar to the random action of wind gusts, the garlic is gone. As the fan returns to its original position, the breeze picks up the garlic scent, and you are awash with the aroma. These are the fine and pulsatile wisps of pheromone that the male is sensing. A requirement of this chemical interplay between the female pheromone source and the male antennae is the wind. Without it, the female’s pheromone would go nowhere, and the male would have nothing to guide him. For the male, the ebb and flow of the wind is a gift and a curse. The wind brings the precious scent of the pheromone, but can also blow the animal off of the scent trail. Even though these pheromone flights occur under windy conditions, the moth can keep itself on track because it uses visual cues from the moving image of the ground to measure its speed and direction. As the images of the other tobacco plants move past its eye, the moth can quickly calculate its flying speed and any crosswind offset. A big breeze has the potential to blow the odor plume away from the moth. As it does, the male switches its behavior. The moth has lost the odor again and has switched to this zigzag flying pattern. The crosswind flight pattern is getting smaller and smaller because he is getting close to the location of the female. As he approaches the female, the width of the pheromone plume is smaller. One analogy, close enough to the truth for the example here, is that the pheromone plume is cone shaped and gets larger as it moves downwind from the female. The male is close and located in the smaller portion of the

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cone. So, his crosswind flights are smaller and shorter in duration than when he was further downwind. With one last whiff of the plume, the male moth has locked on to the female’s location and is flying straight upwind. As he approaches the leaf, he initiates a different behavioral pattern to land on the leaf. Once he alights on the leaf, he starts walking around to look for the female. At this point, the moth starts using his eyes rather than using the olfactory signals from his antennae. Climbing upward, he is using search images (a mental picture of the female) to help locate her among the leaves of the plant. Once he spots her and approaches, the long-distance courtship comes to its natural conclusion.

15.2  The Science of Tracing the Call of Love The task outlined above seems like a relatively simple endeavor. Just smell odor and head toward the higher concentration. This concept is how we and many other animals find the sources of stimuli. For auditory cues, we turn toward the sound so that each ear is receiving the sound at the same time and walk forward to an ever-­ increasing intensity. The same is true for our visual system. Odors and aromas are fundamentally different in how they are dispersed throughout the environment, and this difference makes this seemingly simple task quite complex. Odors, whether in water or air, are dispersed by the movement of the medium. Unlike light and sound which have inherent energies that serve to move them through the environment, chemical signals need to rely on ambient wind or water currents. When this occurs, odors move downwind or down current as plumes which are really full of small filaments, somewhat randomly dispersed within the entire plume. Imagine sitting around a campfire on a slightly windy day and trying to stay out of plume of smoke. On most days, this is a tiresome task as the smoke plume shifts and moves when the wind blows. The same situation arises for the moth. As the wind shifts its direction slightly, the moth will find that the scent of the female can be instantly gone, despite being in the middle of the plume mere seconds previously. These descriptions are what happens to the entire plume and is termed meandering. Large-scale shifts in wind dynamics cause the moth in the above example to fly side to side in search of the ever-shifting plume. Even within the plume, nothing is constant. Smaller-scale dynamics in wind flow (called eddies) cause the odor signal to be pulled, stretched, and torn into tendrils of odor. These tendrils are identical to smoke that rises from a lit cigarette. Instead of smoke, odor patches are drawn out and are moved to and fro at the mercy of the eddies within the wind. The different filaments will have different concentrations of pheromone, and there will be no real pattern of odor within the plume. Because of the interplay between pheromone and wind, the male moth (and every other organism that moves through the world following their nose) will sense an odor plume as a very temporally dynamic signal. This is akin to a light with bad wiring that flickers on and off in a seemingly unpredictable pattern. Yet, male moths locate females

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apparently without an issue. Given that the end point of their journey is reproductive success, there is tremendous selective pressure for these moths to be successful in their quest to find females. Natural selection has shaped the male moth’s brain and the circuitry within it to be able to extract important information from the plume. This information, coupled with a unique set of behaviors, allows the moth to navigate the chaotic pheromone signal. The behavior exhibited by the moth during its flight is actually an elegantly simple set of instructions given the demanding task. The male simply switches between the two different flight modes: surge and casting. Odor serves to determine which flight mode is active. Given the right stimulation from the antennae, the moth will perform both of these behaviors and locate the female. Yet, what is the right stimulation? The switch isn’t just flipped whenever the moth smells a female. The moth needs to get the frequency of stimulation. When a moth moves through a pheromone plume, the independent filaments of odor are going to be perceived as a series of odor bursts. When flying through a filament, the antennae translate the odors to a series of electrical pulses called action potentials. The bursts of action potentials pass through the brain like drum rolls with pauses in between. If the drum rolls continue at the right frequency, then the switch in the moth’s brain stays pointing to surge, and the moth flies upwind. Yet, if the frequency slows down, even if the moth is still within the plume, the switch will move, and the moth will begin to cast back and forth. What is the right frequency? For the tobacco budworm moth, if the bursts arrive around three times a second, the moth will stay in surge mode and fly right upwind to the waiting female. Otherwise, the moth will begin casting (Fig. 15.1). Through natural selection, the brain and behavior of the moth have evolved a mechanism to fly long distances using a chaotic signal to locate its mate. I have always wondered if humans could perform the same task. For a thought experiment,

Fig. 15.1  The moth’s search for a mate. Moth’s track pheromone plumes by switching between a surge flying mode while inside of the odor plume (upper drawing) and casting back and forth while searching for the plume (bottom drawing)

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let’s place someone in the middle of a large room while blindfolded. Somewhere along a wall, we could place a tray of warm cookies with a silent fan behind them. Could we perform this surge and cast behavior and find the treat? I doubt it, but it would be a fun experiment to run. Sadly for us, we don’t have the wiring or behaviors to perform these long-distance tasks. For these, we fall back to using our eyes and ears and ignore any olfactory input. Yet, just like my bakery replete with morning smells, whether we chose to become consciously aware of these odor trails or not, they are all around us. The odor world is a series of intertwining tendrils of aromas. Nature, writ large, is intimately aware of the ephemeral nature of odor plumes, and many animals are still able to make sense of their world.

Chapter 16

This Is Not My House

One of the great pleasures of working at a university is the potential of having a sabbatical. Sabbaticals are designed such that faculty can work at other institutions to increase their knowledge in broader subject areas, perform research under unique conditions or special localities, or learn new methods and techniques. These usually only come around once every 7 years and aren’t always granted by the university. An excellent research proposal needs to be written and faculty need to show that the sabbatical will improve their ability to teach and do research at their home institution. I was lucky enough to be granted a sabbatical and fortunate enough to find funding that allowed me to work for 6 months at Lund University in Sweden. My hosts procured a wonderful little flat for me. Small, but cozy, the flat had an ideal location equidistant from my temporary office at the University and center city where I could do all of my shopping. In addition, the flat was between a small museum and a garden with fruit trees and rose bushes. Entering the flat for the first time, my initial judgement of the place was performed by my nose. Now, there was nothing off or bad about the smell of the flat, but it had a unique aroma to it. Probably a combination of odors from the local water, the fruit trees outside, and the detergents used to wash all of the linens and towels. An unfamiliar scent, but one that would become recognized as my new, albeit temporary, home. After spending a few hours settling in, I went on an olfactory scavenger hunt throughout the flat to try to locate the sources of all the new odors. The bed sheets, even the new ones that were provided to me, carried a suite of aromas that seemed to dominate the loft and closets. The towels had a different, still pleasant, scent that had permeated the small bathroom. Finally, the kitchen area had odors reminiscent of past meals located with the pots and pans and the different cabinets that must have been used as pantries. Although localized to different sections of the flat, the interaction of these scents produced the gestalt for my new flat and over the months, I began to recognize that odor as home. Certainly, the quicker conscious recognition came through the visual cues that told me I was home, but the more emotional connection of safety and relaxation would come through my olfactory system. For many animals, the unique

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combination of chemicals that signal home provide a sense of safety and security as well as lowers levels of stress and anxiety. For other animals, the aroma of home, particularly their juvenile home, beckons to them across long distances. These animals aren’t searching for security but for mates and suitable spawning grounds. One of the best examples of these homeward treks is the yearly migrations of salmon that are seen across the globe. The salmon start their lives in many of the coastal rivers across the globe, as the adults tend to lay their eggs in patches of rivers with dense gravel substrates. These eggs develop in the safety of the gravel for anywhere from 2 to 5 months and eventually hatch into larval salmon, called fry. These rivers are called their natal stream, which refers to the river in which they were born. Depending on the species of salmon under consideration, the fry stay in these rivers for up to 3  years and are constantly being bathed in a unique mixture of chemicals contained in the river. These chemicals, just like the unique bouquet in my Swedish flat, come from a number of different sources. The water in these rivers, in reference to the olfactory abilities of salmon, can be considered analogous to a fine cup of coffee. The water in the coffee carafe has percolated through the coffee grounds, and in doing so, the water incorporates the caffeine, color, and flavors of the coffee grounds. Coffee grounds in different parts of the world have different suites of chemicals, and certainly, the various roasting styles bring forth different flavors and odors. Water usually enters rivers as either snow melt, rain water, or by traveling underground and eventually emerging into the stream. Independent of how the water flows into the river, it usually picks up a unique combination of chemicals in the soils and lands surrounding the river. Just like different coffee beans will impart different flavors to the water, streams and rivers located in areas with different soils, geology, and ecosystems will pick up the chemicals as they make their way into the stream. Juvenile salmon become imprinted to the smell of their natal stream and carry this imprinting (or olfactory memory) with them on their long journey to sea. As these maturing fish make their way to the ocean, they grow and change color. The small streams that served as their homes during their younger years begin to merge with other streams which contain other populations of salmon. All the while, the chemical signatures of each stream gets diluted and blurred when two streams meet and their waters mix. Still, the young salmon continue their journey downstream. At each juncture, the waters from the streams blend together as the river grows increasingly larger. As these fish get close to oceanic waters, the salinity increases significantly, and the physiology of the animal begins to adapt to the intense salt water of the marine environment. Despite all of these changes in size and physiology, the olfactory memory of its natal stream remains intact. Living a full life for a salmon could mean a year and a half to upward of 8 years either near the coastal areas around the mouths of rivers or out in the open ocean great distances away from the coast. Eating their fill of shrimp, squid, and other fish, the salmon eat as much as possible in preparation for the arduous journey that ultimately awaits them. This journey is literally a life and death adventure for the salmon. The obstacles are as  plentiful as great oceanic distances with no clear

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d­ irectional cues. Bears and humans are both waiting in the stream to capture them for their food, and a constant battle against current and waterfalls is all part of the journey. Despite all of the barriers, the salmon is guided quite faithfully by its amazing nose. This time, each stream juncture is a choice: left or right. The consequences of making the correct choice are a triumphant return to its home and the potential to reproduce. The wrong choice and the salmon could be off wandering streams that might not be suitable homes for eggs and juveniles. Faced with this choice, the salmon recalls a distant memory of the olfactory signals of its youth. By comparing the current aromas of the two stream channels with the old memory, the salmon makes its choice and swims off toward home. I can’t imagine being blindfolded and asked to compare a mixture of odors with ones hopefully stored in my memory that are now over five decades old. Odor memories are definitely powerful events for humans, but we certainly lack the ability that this salmon has to remember its natal stream. If asked to locate our childhood home only using our noses, I fear that we would end up wandering around quite aimlessly. Perhaps an expedition to an Alaskan river to follow some salmon moving home might provide us some insight into this olfactory pilgrimage.

16.1  Following the Ribbon of Odor The Chilkat River in Southeast Alaska is an excellent place to observe the yearly salmon run. The Coho salmon, Oncorhynchus kisutch, make their runs throughout the fall (September through November), but the biggest waves of salmon head upriver in mid-September. The salmon make an exhausting journey home in returning to the streams they once inhabited as young. Once mature, the salmon make their way to the open ocean from their natal streams and spend 2–4 years there. On its way home, the adult salmon face many challenges such as exhaustion and capture by both the human and grizzly hunters along their route. What seems to be the most challenging aspect of their journey, though, is choosing the right tributary simply based on the unique mixture of chemicals. As the salmon navigates its way from the ocean to its native tributary, it will face numerous decisions as rivers merge and split. Each tributary that is approached supplies background chemicals that will mix with the current milieu in the main branch. While it is true that each stream has its unique mixture of chemicals, the streams greatly overlap in their chemical makeups. A simple analogy would be the makeup of beer in all its variety. The same main ingredients (barley, hops, water, and yeast) combined with subtle additives (fruit or spice) can produce a range of delicious flavors. In September, the river is running quite strong and the salmon population is very abundant. While all of these salmon are starting their arduous journey upstream, they all won’t head to the same home. This population of animals comes from the tremendously large watershed of the Chilkat River system. Each subpopulation will have their own set of challenges that includes powerful currents, waterfalls, bears, and fishing humans as well as smelling out their own little stream among the

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c­ ornucopia of chemicals in these waters. An average adult can reach 55 cm in length and should have just the right amount of stamina to make it home. As the total population of salmon start their journey, they mill around the mouth of the river as it empties into the ocean. The first signal that the salmon are approaching the beginning of their journey includes the salinity difference between the ocean and freshwater of the river. As they gather at the mouth of the river, their swimming around in the wide and slow-moving river serves to help them find that sweet odor that matches what they imprinted. Once an animal has found that odor, it initiates an up-current swim that is guided by those odors. Yet, even before this point, the salmon have made a remarkable journey. The Chilkat River officially starts as the mouth of the river meets the Chilkat inlet just northwest of Haines, Alaska. This population of salmon has had to navigate its way around numerous islands in the Chilkat inlet just to follow the scent of its home stream. Even in the mouth of the river, small shallow areas abound as a large number of tributaries pour into the main river. At each of these junctures, the odors of the tributaries combine as a large mixture of scents in the main river. Undoubtedly, the salmon are following a mixture of odors rather than any single unique odor that signals their home stream, just like the mixture of chemicals in the beer will give it the unique taste. The most interesting aspect of this journey for our observations is the critical decisions being made at the tributary. Literally, a life and death decision. The selection of the wrong tributary means retracing the salmon’s journey and wasting precious energy on wrong decisions. As the salmon move upstream, they’ll pause at each tributary, most likely sampling the different odors to ensure that they are following the correct water source to their natal stream. The sampling and decision-making takes some time and is often repeated. The salmon are attempting to detect minute levels of chemicals and comparing them to a long-ago memory hidden in their brain. If the odors are not recognized or don’t match the odors from its memory, the salmon will return to the main branch of the river and headed further upstream. This river contains a mixture of all the chemicals that are in the surrounding watershed. A watershed is a relatively large area where all of the water (either above or below ground) flows into this river. The chemicals in the soil, being released by all of the roots of the plants, weathering from the rocks, and other sources from the surrounding landscape, are within this stream. The salmon is capable of smelling the broad range of chemicals that all of those objects produce. Although our research has yet to find the exact chemical trigger recognition of the home stream, the salmon make very little mistakes on their journey home. Their olfactory system has been highly tuned by the sharp knife of evolutionary selection. Those salmon that made mistakes never made it to their streams to reproduce. As we monitor salmon swimming homeward, a subgroup has decided to exit the main branch of the river. As with the previous tributaries, the salmon spent some time in the tributary before making this decision. Unlike the previous times, the salmon must have found an excellent match between the current smell of the stream and that from their memories. Once this match has been determined within the brain of the salmon, the choice is made, and they head off up the smaller tributary. Heading

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off to mate, the salmon have to repeat this decision-making process dozens of times as thousands of rivers diverge to create each of the tributaries, and eventually, the small natal stream.

16.2  The Science of Recognizing Home Imprinting is a very powerful biological phenomenon. Konrad Lorenz won the 1973 Nobel Prize (along with behaviorists Nikolas Tinbergen and Karl von Frisch) for his work in understanding animal behavior and particularly animal behavior under natural settings. Imprinting is so powerful that Konrad Lorenz could get flocks of geese to imprint him as their caregiver. Lots of videos and images float around on the Internet that show this funny and insight ability in geese. Olfactory imprinting is really no different than imprinting on a caregiver at the behavioral level. A stimulus, in this instance the olfactory milieu of the natal streams, alters the underlying neuroarchitecture so that there is a strong connection between the stimulus and the response to the stimulus. In Lorenz’s case, the connection was the visual image of his face and body with the mental construct of caregiving. In the case of the salmon, it is the intertwining of the unique mixture of natal stream compounds with the image of mating and reproduction. Another feature of imprinting is the limited time period in which it can occur. This time, called the critical period, is species specific. Within Lorenz’s geese, the critical period is 1–2 days after hatching. In primates, the critical period is anywhere from half to a full year. In humans, imprinting can occur over years. For most animals, imprinting, especially for caregivers or parents, usually occurs rather shortly after birth. In this way, the critical period of imprinting for salmon is very different. Imprinting for natal streams in salmon usually occurs between two different life stages called parr and smolt. The timing of these stages depends on the salmon ­species, but for the Coho salmon, they spend their first 5 weeks in a stage called alevin where they are positioned deep in the gravel of their rivers. Emerging after weeks, they are now called parr and can live in this stage for 1 or 2 years. At this point, the salmon have still not imprinted on the aroma of their home stream. Certainly, changes in land use through human means (logging) or natural (fire) can alter the composition of compounds in the rivers (Fig. 16.1). As the parr grow and get ready to migrate from the rivers out into the ocean, they transform from a parr stage to the smolt stage. The salmon begin to take on the characteristic coloration of the adults at the smolt stage. This is the stage that makes the initial migration from the freshwater natal streams to their adult life in the open ocean. It is at this point that the salmon begin to imprint on their surrounding chemical environment. A sort of one last smell memory before they leave their juvenile home. At the neurological level, the parr to smolt transformation is also accompanied by changes in the brain of the salmon. Specific receptors, N-methyl-d-aspartate

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Fig. 16.1  The salmon’s choice. Salmon use the smell of their natal streams to return home to spawn. At each juncture in the river, different sets of odors mix creating a difficult choice for the salmon

receptor (NMDA), start to increase in abundance within the brain of the animal. These receptors are known to be associated with increased memory function, and this instance indicates that the animals are developing an olfactory memory. At this critical period, the salmon increases its capacity for memory in order to have a strong and indelible olfactory image of its home stream. This isn’t the only special adaptation the salmon has. Work has shown that for this animal, memories can be located both in the brain of the animal as well as the nose. How does a nose have a memory? The chemical senses, olfaction and taste, are different than other senses in that there is constant growth, change, and turnover of receptor cells. Olfactory cells have a normal lifespan in which they develop, function in smell, and then senesce. In humans, as well as other animals, the receptors in both our noses and on our tongues change consistently throughout our lifespan. The same is true for the olfactory tissue in the nose of the salmon. As cells develop, grow, and die, genes for olfactory receptors get turned on and off as they produce receptors for specific smells. For young salmon, it appears as if receptors for the chemicals present in the natal streams turn on more than receptors for compounds that don’t happen to be present. This means that the specificity of the nose of the salmon gets tuned toward those sets of compounds or chemicals in its natal streams and will get turned off to the chemicals that are absent. Thus, the noses are more sensitive to the suite of compounds that signal its natal stream. For those chemicals that are absent, the nose either produces less receptors or none at all that will respond to those chemicals. As such, the nose ignores the suites of chemicals present in non-­ natal streams. By increasing the capacity of its olfactory memory and tuning its nose to specific chemicals, it can be said that the salmon only has a nose for its home stream.

Chapter 17

Better Lies Through Chemistry

In the 2009 dark comedy The Invention of Lying, the main character, Mark Bellison, played by Ricky Gervais, lives in a world where everyone tells the truth. Everything from deception to little white lies is absent from the world, and the absolute truth dominates advertising, conversations, and relationships. In a world such as this, even fantasy tales, books, and make-believe movie scripts are missing. Honest conversations about sensitive subjects are an everyday occurrence. Although the audience members would probably view these conversations as quite awkward, the actors just simply accept such cases as how the world works. In a moment of intellectual brilliance, Mark Bellison invents a lie. Needing money to pay his back rent, the character tells the teller that he has more money in the account than he really does. When his stated amount is checked against what the computer reports, a conflict arises in the teller’s mind. Since lying doesn’t exist, she believes the computer is wrong and gives Mark the extra money. As the movie progresses, the scope of his lying increases and eventually, as one would predict in a cinematic universe, gets out of hand. Contrary to this movie world, our own world is constructed by layers and layers of lies. Every commercial or advertisement contains sets of false or misleading claims. Beauty products will make us irresistible to the opposite sex. Restaurants show images of perfectly constructed food that is exceptionally healthy for us. Footwear will allow us to move and play like our favorite athletes and the right car will fulfill our every wish. The goal behind each of these statements is to deceive the viewer or listener in order to separate them from their money. Although not a noble endeavor, it is one that is necessary to drive economies. On the less pernicious side, lies we tell each other are designed to keep our social interactions moving smoothly. When a friend asks for help after a long day of work, we’ll reply with a “no problem” or an “I don’t mind helping at all” when in reality we may just want to relax at home. Within our romantic relationships, if our mind drifts when our significant other provides a detailed story about the failings of their co-workers, we’ll reply with statements of emotional support even though we weren’t listening. If our closest friends confide their secrets to us, we’ll keep our © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_17

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silence even when asked about the secrets. Even something as innocuous as misleading answers about a surprise birthday party uses the fine art of lying. Unlike the previous paragraph, we would rationalize the use of these deceptions because the intentions are in the best interest of the deceived. Regardless of the intention of the sending, lies, defined broadly, are an essential part of our society. Because of the exquisite control we have over our auditory and visual signals, the lies within in our society are primarily constructed from these two sensory stimuli. A switch of a couple of words “I made the mistake” to “I didn’t make the mistake” takes very little energy. Poker players train for years to control any facial tells that might signal a desperate bluff. The famed psychologist Paul Ekman has made a career about studying the microexpressions that humans exhibit, and only the well-­ trained or truly psychopathic can hide all of their facial expressions. Probably the main reason that these sensory channels play a dominant role in the realm of lying is the cost to produce these signals is relatively small compared to other channels of communication like chemical signals. From a biochemical perspective, chemical signals are expensive. Most chemical signals used for communication, even pheromones, were initially by-products or secondary compounds in a regular metabolic process. These compounds are essentially left over from important physiological process. One great example is the host of compounds found within urinary products. Initially, these were waste products from the process of consuming and chemically altering food and water. Now, many different species use these signals in social or behavioral arenas like reproduction and dominance. In addition to the cost of the production of chemical signals, the production of the signal itself may alter the animal’s own physiology. Serotonin is a neurotransmitter involved in a large range of functions within the human body. One of these functions is mood and mood control. The correct amount of serotonin and its location within the brain determines, in part, the level of happiness we experience. If something is wrong with either the production or removal of serotonin, then mood alteration and even depression can result. Thus, a class of chemicals called SSRI for serotonin selective reuptake inhibitors have been developed that have provided relief for millions of sufferers of depression. Serotonin, the metabolic by-products, and breakdown products are also used as forms of chemical signals in different animals. If the production of the serotonin for external use is not tightly controlled by animals, the internal concentrations can cause a host of behavioral disorders. Because of these two points, cost and control, chemical signals are hardly the first evolutionary choice for lying. In addition to these problems, the production of both internal and external chemical signals is intimately intertwined into the physiology of the animal. Adult animals produce different aromas than juveniles. Animals in a reproductive state produce different body odors than those that are not. This connection between the external and internal chemical milieu was used by scientists as evidence that only honest chemical signals were thought to exist. Any change in the internal state of the animal would be reflected in its body odor. As sophisticated techniques of chemical analysis have increased, the thought that animals produce only honest chemical signals has seen its last days. There are a

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number of examples where one species will produce a dishonest signal to manipulate, trick, or trap another animal. Carnivorous plants often produce sweet smells that draw insects into their death. The titan arum plant produces an odor reminiscent of rotting flesh to attract flies for its own selfish reproduction. The ability of some animals to inhibit the reproductive potential of others within its vicinity through chemical signals is another example where the receiver doesn’t gain any benefit from smelling the aromas. Despite these examples, the attachment of the word “dishonest” to chemical signals is still something that scientists are reluctant to do. Instead of lying, research refers to a concept of “less than reliable” signal or, potentially, the term, “manipulative” in reference to chemical signals. Within this category are a host of chemical signals that will chemically castrate or inhibit surrounding animals. Within many insect societies with queens, the queen produces a chemical signal that inhibits the reproductive capability of fellow nestmates. In rodent societies, a newly anointed alpha male will release chemicals in their urine that will cause abortions in any pregnant mice. In other mammals, alpha females will release signals to keep other females from coming into estrus. These are manipulative or unreliable signals because of the disconnection between the reception of the signal and the benefit that the receiver obtains. Most of these types of signals occur within species as the sender often benefits at the expense of the receiver. One of the best examples of lies and deception with chemical signals is in a group of orb-weaving spiders called the bolas spiders. Bolas spiders are found in the Americas, Australia, and in Africa and can be found in both warm and cold climates. Orb-weaving spiders often build the classic spider web that is circular in shape and is used to trap flying insects with the sticky material used to construct the web. Most of these spiders can be considered sit-and-wait predators, as they’ll build their trap and sit on the edge of the web patiently waiting for a meal to find its way into the web. Once there, the insect is quickly subdued, maybe poisoned, and wrapped up in webbing for storage. The bolas spiders, just like the character Mark Bellison in The Invention of Lying, took a very different route to their hunting by developing the ability to lie through chemicals.

17.1  When We First Practice to Deceive Instead of weaving a beautiful web, the bolas spider takes an active role in the hunt. The American bolas spider, Mastophora hutchinsoni, can be found throughout the eastern part of the United States and feeds on two different species of male moths. Without a web or net to capture the flying insects, the bolas creates a lure that draws the moths in by using a fundamental drive of evolution: reproduction. In a very simplified view of evolution by natural selection, organisms compete for success which is measured only in terms of leaving the most offspring. The diversity of life is a testament to the many different ways that organisms can compete, but the bottom line of reproduction remains the same. Thus, the drive to find mates, at least in sexually reproducing species, is irresistible. As detailed in some chapters

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throughout this book, the ability to find mates through specialized sensory gear is probably the most important thing organisms can do. As such, an animal’s perception is tuned to those cues or signals that provide information on nearby mates. For many moths, this drive to reproduce is under strict control of pheromones. Contrary to popular belief on pheromones, these signals are not unique chemicals, but often come in blends. The blends allow different species of moths that overlap in their distribution to differentiate between calling females. One of the biggest mistakes organisms can make in the game of evolution is mating with the wrong species. This is an evolutionary dead end for their genes. So, moths have been finely tuned to smell their own unique blend (often three compounds) of pheromones and are turned off by the smell of closely related species. The males, upon smelling the right blend, begin a series of behaviors that are designed to lead them to a waiting mate. It is this drive that the bolas spider has exploited with its chemical lies. Bolas spiders are quite an unattractive species of spiders. If you are among the humans who think all spiders are unattractive, a viewing of the peacock spider might change your mind. Still, the bolas spiders have an abdomen that is covered with bumps and raised pores that make it appear sickly. This is its secret and will be explained below. Unlike their other orb-weaving cousins, the bolas spiders use their webbing to construct a tiny and sticky blob of web. Carefully constructed to be the right size and shape, the bolas spider attaches this blob to the end of a long thread. This is their bolas, and the name comes from the uncanny appearance and behavior of their hunting style to those made famous by the Argentinian gauchos. With its weapon ready, the bolas spider is almost ready to hunt. The last trick is to rub the sticky blob on the top of their abdomen. This covers the blob with a blend of chemicals that can mimic the pheromone of any local moth species. Since each moth has its own unique blend of chemicals, the bolas spider has to create multiple chemicals depending on the prey of the day. For the American bolas spider in the Kentucky region of the United States, its preferred prey consists of the smoky tetanolita moth and bristly cutworm moths. If the spider chooses the smoky moth, then its little chemical factory produces that pheromone blend, and if the cutworm moth is on the day’s menu, the factory produces a different suite of chemicals. Once the attractant is applied, the bolas spider constructs a single strand of silk between two anchor points. Hanging upside down from this guidewire, like Spiderman from the Marvel comics, the bolas spider begins its deadly hunt. While hanging upside down, the spider takes the thread end of the weapon between its two front legs and begins to swing the scented lure in ever-widening circles. Slowly at first, the spider increases its intensity, swinging the lure wider and wider. This swinging serves two purposes. The spider is spreading the aroma of the pheromone blend in an attempt to increase the downwind plume. Swinging helps to release the odor molecules from the bolas. Second, the swinging, just like the gauchos, is used to create momentum to hit its prey. Any poor moth, driven by the need to reproduce, that thinks a potential mate is waiting upwind is tricked by the spider’s lie. The selective pressure to respond to their sex pheromone is a drive too strong to resist. Once caught, the only thing that awaits the male moth is death at the hands of the spider.

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17.2  The Science of Making Chemical Cocktails To create a lie, or at least a chemical deception, the starting place should be the truth. For the bolas spider, the truth of the situation is the pheromone blends that will attract the males of the right species. The American bolas spider primarily feeds on two different species of moths as adults in the Midwest: the smoky tetanolita and the bristly cutworm moth. For most moth species, the sex pheromone is a blend of two to three compounds that are often related in structure and size. While the exact type of organic compound may differ across species, these two moths have blends that consist of organic molecules called acetates. Acetates are a group of molecules with a carbon chain or backbone and have a functional group that consists of carbon attached to two oxygen atoms and a methyl group (one carbon atom bonded to three hydrogens). The exact compounds have long organic names but are referred two by a series of letters and numbers that appear like a spy code. For the bristly cutworm, the pheromone consists of (Z)-9-tetradecenyl acetate (Z9-14:AC) and (Z,E)-9,12-­ tetradecenyl acetate (ZE-9,12-14:AC). The smoky moth’s pheromone blend has two compounds whose abbreviations are even more complicated (3Z,9Z-6S,7R-epoxy-­ 21:H and 3Z,6Z,9Z-21:H). The main point of these abbreviations is that the smoky moth uses a different kind of pheromone that is not based on an acetate molecule. So, the spider needs to not only mimic two different types of blends for both species, but the configuration of the molecules is also different. This would be the nightmare final exam for most organic chemistry students and yet, the bolas spider produces these chemicals on a daily basis (Fig. 17.1). On top of this complicated chemistry is that these moths are usually nocturnal fliers. Producing chemicals during the day would do nothing to draw in potential prey. So, the bolas spiders can upregulate the production of the fake pheromone blends during the nights. As a final source of trouble for the hunting spider, the

Fig. 17.1  The bolas’ chemical plant. While not a very attractive spider, the back of the bolas spider is its chemical factory where it produces the pheromone mimics to draw male moths to their death

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p­ erfumed bolas does shrink over time, losing both the attractive scent and adhesive properties. If this occurs, the spider usually consumes the bolas and recreates a new hunting weapon. Unfortunately, the underlying chemical production of these pheromones has not been elucidated yet. The spiders are exceptionally hard to capture, but when captured, they will produce the pheromones in the laboratory. The volatile chemicals have been collected and compared chemically with the real signal and the match is uncanny. From a perceptual view, the spider does not seem to be sensitive to the compounds of the moth, so the spider has produced a lie (deceptive chemical) without the ability to perceive the truth (true pheromone). This phenomenal ability is polar opposite to The Invention of Lying movie where the movie characters are unable to perceive a lie. In the spider’s case, the guiding hand on the development of these deceptive pheromones has been natural selection. In overly simplistic terms, those spiders that produce the closest mimic to the actual pheromones will be the most successful hunters. Over the long time frames of evolution, small incremental steps in the production of better and better mimics have been passed down to subsequent generations of spiders. The true test of the chemical lie is not the spider’s perception, but that of the moths. If the moth thinks a mate is nearby, then a successful hunt is possible. To be honest, this chemical example of deception stretches the concept of perceptual worlds for this book. These examples provide very little insight into the world of the spider and only some into the world of the prey. The tenuous link between this example and chemical perception is a clear indication of the difficult nature of lying with chemicals. What sparse examples are available are between hunters and prey and not within a single species.

Chapter 18

Can’t We All Just Get Along?

As a young kid growing up in the Midwest, I could be found either exploring out in the woods near my house or hunkered down in front of the TV for a nature documentary. My favorite show was The Undersea World of Jacque Cousteau. The show first aired in 1966 when I turned 2. I was probably too young to remember much back then, but the show ran until I turned 12 in 1976. I, along with many others, sat amazed at this world that was hidden from view. This show probably helped guide my education which ultimately led to my PhD in marine biology. The visual imagery, along with the excellent narration, not only explained the marine environment, but was years ahead of its time in focusing on biodiversity. The show covered a vast array of organisms from the unique and oddly shaped marine invertebrates to the much more charismatic megafauna of whales and dolphins. Shortly thereafter, the legendary Cosmos science documentary was aired in 1980 along with the companion publication. At age 16, this show tapped into the budding scientist in me and solidified my career choice. What these two shows had in common, or at least struck a chord with me, was the ability to make science exciting. Usually portrayed as a dull, impassive, and logic driven endeavor, science is difficult to make exciting to the general public and still stay true to the fundamental nature of science. Many of my field endeavors, if viewed from outside, are boring and unsatisfying. Animals aren’t found or don’t ever behave like you want them to. The conditions are rainy, wet, cold, or extremely hot, and quite frankly, I sit around either watching an instrument take measurements or filming an animal that just sits there. In fact, most fieldwork involves watching animals do very little in the way of exciting behavior. To overcome the boring aspect of nature, one of the favorite staples of many nature documentaries is to film and show the outright deadly and intense aggression between animals. Aggressive interactions between different species are often in the form of predator-prey interactions. The scenes involving these types of activities are gripping for the audience because life and death are literally on the line. The lion chasing down a zebra or a pack of killer whales singling out a seal will have us sitting on the edge of our seat in suspense. Many of these chases end up with the prey © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_18

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escaping, as predatory success rates are typically around 20–30%. Some species are far more superior hunters, as some studies suggest that dragonflies have a 95% success rate. Aggression between species isn’t the only game in the business. Within a single species, organisms often compete for resources like food and mates. Intraspecific aggression is called agonism and is seen across the animal and plant kingdoms. In many species of animals, males will fight with other males during mating season for territory, mates, or both. Nature documentaries tend to focus on the males from the large mammalian fauna that put on amazing displays of strength. Big horn rams will smash heads creating loud cracks that echo through the mountains. The large male elephant sea lions often fight each other until they are quite bloodied. Some of the most terrifying fights can be found between two male hippos vying for dominance and access to mates. Despite the dominance of these massive displays on the screen, the fights of much smaller animals can be just as deadly. In my own work with crayfish, I have seen one male dismember his opponent and then consume the missing appendages. The preponderance of the violent nature of these interactions in media creates a false sense of the degree of brutality that occurs in nature. Despite Tennyson’s view of nature as “red in tooth and claw,” there are plenty examples of cooperation. Cooperation across species lines comes in the form of symbiosis (where the relationship is a requirement of existence) or mutualism (where the organisms can effectively live apart from each other). This cooperation can even exist across Kingdoms where plants like the Acacia tree can form symbiotic relationships with ants. The ants protect the trees from insects arriving to graze away at the Acacia leaves. In return, the hollowed-out thorns on the tree serve as homes, and the tree supplies the ants with nectar and food. Within species cooperation is far more common. Family units, large troops, or related individuals can form cooperative groups that can survive far easier than if these animals were to live alone. Social insects have taken cooperation to another level by having complex organizational structures with specialized roles. Almost as diverse as human societies, the varied roles that bees can have within a colony range from queen, workers, and drones to foragers, cleaners, and nurses. Some bird species have extended families that will help care for, feed, and raise younger birds in the nests. These extended families usually contain older brothers and sisters that help forage during harsh times. Shared parenting duties are common in primate societies. This is termed alloparenting to indicate that someone other than the parents (the ones with the direct genetic link) is providing care. Often, related individuals (grandparents, brothers, and sisters) provide the care, but alloparents can be completely unrelated also. Providing food, safety, and care for young individuals can be quite costly. Time spent on raising an offspring (either through parenting or alloparenting) is time away from foraging and producing more offspring. Given the costs of parenting, it is not surprising that some animals have taken advantage of alloparenting for their own benefit. One animal that takes advantage of others is the common cuckoo. This bird will lay its egg in the nests of unsuspecting birds, like warblers, and leave the

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parenting all to this other bird. Unfortunately, the warbler cannot differentiate between its own eggs and that of the interloper and will take care of the cuckoo as its own offspring. This often leads to growth and survival of the cuckoo youngster at the expense of its own young. Thus, it is important to be able to recognize genetically related individuals or even one’s own offspring so that the time and energy spent in parenting is invested in the correct individuals. This concept can be broadened to include examples other than parenting. The investment of time and energy can be thought of as in-group and out-group behaviors. Social organisms treat individuals differently depending on their group status. If an animal is inside a group (such as a pod, nest, or hive), that individual will be provided cooperation. Conversely, if an animal is perceived to be outside of a group, agonism and aggression are often displayed toward the individual. So, whether an animal is part of the family or part of a larger genetically diverse group, determining the status of the individual is a key to maintaining group and social behavior. The ability to determine group status is a perfect job for olfaction and taste. What makes the chemical senses uniquely positioned to perform the task of identification is how the production of signals is so closely tied to the genetic makeup of the organisms. Certainly, the visual and auditory stimuli that organisms create are due to their genetics, but many organisms can readily control and change these stimuli. Decorator crabs add accouterments to the back of their shells to make crab-­ like fashion statements. Cephalopods (octopi and cuttlefish) are the masters of disguise in their ability to change the color and texture of their skin. The superb lyrebird can mimic almost any song that it hears. The chemistry of an organism’s body is different and not under conscious control like the visual appearance or vocalizations that organisms produce. The chemical signature for organisms is due to the interaction of a combination of the unique set of genes in an animal with the dietary building blocks that the organism consumes. Although changes in the diet can produce changes in body odors, the set of chemical signals that organisms produce can be used to identify their genetic makeup. So, if the in-group status is based on some sort of genetic relationship (as in families and social insects), the chemical signature of that organism should be reflective of that status. The champions at checking the right credentials and one of the most interesting groups of organisms on the planet are ants. Ant colonies vary by size and structure across the planet, but the one thing that ties them all together is an exceedingly large group of organisms that leave and enter the nest on a daily basis. Ant colonies can have single or multiple queens and millions of workers and even exist across physically different nest sites. Despite this variety, ants guard their colony borders with intense ferocity. Those that belong in the colony are quickly checked by their border guards and allowed to enter. The interloper can be detected very quickly and is often attacked and killed with precision. Unlike most airport security lines, there is no wait into or out of the colony. These TSA ants are efficient and flawless in their task. Formica ants are a genus of ants considered to be wood ants. As their name implies, these animals are often found in areas where there is an abundant supply of material for the construction of their mounds. These ants, like many other eusocial

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insects, have large colonies which must be protected from intruding ants from other colonies or even other species. Just as we would recognize our neighbors and friends by their face, these ants recognize their colony mates smelling their body odors.

18.1  The Secret Handshake Formica ants, Formica sp., are a cosmopolitan genus and appear on just about every continent on the planet. A stroll through any local woods is enough to locate a mound of ants. As their name indicates, they use decaying wood material as a substance to build their nests. The stump from a fallen tree or even the tree itself is an excellent place to start a search. The mounds often appear like small piles of wood mulch as the ants thatch their homes with the material. A good visual image to have is a mulch pile that looks out of place with the surrounding forest. It is almost like someone just dropped a pile of mulch in the middle of nowhere. Some mounds can be quite tall (taller than a human) and large, while others can be quite small (size of a fist). Once such a mound is located, a closer inspection can show what an amazing job the ants have done in shredding the woody material into a fine mulch. Like an iceberg, the above ground and visible part is just a small aspect of the entire nest. Below is a complex and roomy nest that can be quite large. Scientists and artists have made casts of the nests by pouring liquid metal or plaster into the nest. The resulting cast would show multiple chambers below ground as well as small pathways linking each of those chambers. At the entrance to these palatial grounds are fierce guards that only let certain ants enter the haven. Below the ground are two key resources that are guarded with their lives. The larvae, which are the future life of the colony, and the queen, who produces all the larvae, are safely kept unground in their own chambers. Moving in for a closer look, as an ant emerges from the nest and hurries out on its foraging run, it is quickly followed by numerous others who are making foraging or nest building material forays into the surrounding forest. These foraging or gathering ants are following well-marked trails that lead to caches of material in the forest. These trails are not visually marked, but consist of an invisible chemical highway that has been laid down by previous foraging ants. The highway is quite ephemeral. Each ant needs to reinforce the highway with new smells to maintain the trail. If the food cache at the end dries up, the ants abandon the trail, and it quickly fades into nothingness. The foraging ants can follow the highway by touching their antennae to the ground to pick up the scent trail. By doing this, the ant captures the odor molecules trapped on the soil’s surface. This is similar to how we feel around in the dark for a light switch and can discern the switch by feeling the change in the wall’s surface. As the foraging ants locate the foraging trail, they’ll stop and check the returning ants for the right smell. In addition, the ants returning with food to the nest will do their own investigation as well as periodically place their abdomens on the ground to renew the scent. It is a complex interrogation that takes place using chemical signals.

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Just as human highways can get congested, these chemical ones can be full of traveling ants. Just as the queen and larvae are precious to the nest, the trail is also an important resource. It leads to food and back to the nest. So, during the highly congested times, these ants have to ensure that their nest, and only their nest, use the trail. As two travelers run into each other, they begin a sort of questioning. In a scene eerily similar to crossing a border into another country, the right passport and visa has to be shown. In the ant world, these documents are replaced with even more chemical signals. The busy ants take a pause from their travels to intensely “question” each other. One ant begins by sampling the other traveler’s body for a secret chemical signature. The ant “frisks” the body of the other one with its antennae focusing a lot of its energy on the head of the other ant. While this is occurring, the second ant performs a similar body check in an attempt to determine if the right chemical signal is present. It may appear as if they are hitting each other with their antennae, but, really, they are taking quick and effective “sniffs” of the other ant’s body. The chemical answers to the questions will determine what follows next. Just like a secret handshake, the correct batch of chemicals on each other’s body will allow them to continue on their journeys, either to the food cache or to the nest. As a final act to the inspection, each ant will curl its abdomen forward to present that for inspection. If the wrong chemical handshake is detected, a ferocious battle will begin, and other traveling ants will join in to remove the interloper from their trail. When the battle begins, the ants will release alarm signals that will draw in their fellow nestmates. Because the trail belongs to a certain nest, only those nestmates will arrive to help in the battle. Usually, the interloper is killed rather quickly and either discarded by the side of the trail or taken back to the nest to serve as food for others. These chemical pat downs work exceptionally well as each nest has its own combination of unique chemicals. Because of the use of these chemical signals, the trail is saved rather quickly as numerous nestmates have been called in to deal with the intruder. As the aggressive interaction ends, all the other ants return back to their own chemical interrogations and then back off to the foraging runs.

18.2  The Science of a Coat of Arms One of the defining principles of life is the ability to transform energy from one form to another and to use that transformation to fuel cellular components. Plants absorb the energy contained within sunlight and transform that into chemical energy in the form of sugars. Animals, in turn, will transform one type of chemical energy (sugars from plants) into a different type of chemical energy (ATP) that is used to run our cellular machinery. In addition, organisms use these energy transformations to build cellular components like lipids, proteins, and nucleic acids. Thus, the cells within all organisms can be envisioned as little chemical factories that produce a host of different compounds used to maintain the composition of the cell. With all these chemicals being produced, it isn’t surprising that some of these chemicals can serve a dual purpose of signaling as well as cellular maintenance.

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For ants, one of the key chemical products are hydrocarbons like alkanes and ketones. Alkanes and ketones are hydrophobic, which translates into “water” and “fearing.” From a chemistry point of view, this means that these compounds don’t fare well in water, which is a scientific way of saying they don’t dissolve well. The ant’s exoskeleton happens to be covered in these hydrocarbons. This outer covering of alkanes and ketones serves as a waxy rain jacket for the ants. Instead of keeping water out, the rain jacket serves to keep the ants from drying out or desiccating, which is an essential tool for survival in many of the formidable habitats where ants are located. Having a rain jacket made of chemicals creates the possibility that other ants can detect or smell these external chemicals. If the chemicals of each jacket are unique to a nest, then it can also serve as a uniform that represents which species or even nest an ant belongs to. Some species of ants can have over 100 different types of chemicals attached to its exoskeleton. Each different hydrocarbon can be thought of as a new letter of an alphabet or a new symbol with a distinct meaning. With 100 different varieties of letters or symbols, the rain jacket of each species of ant could “spell out” the name of each species as well as the specific home nest for the ant. Just as the words “riding” and “ridding” have very different meanings simply by changing the “concentration” of the letter d, ant species can change the concentration and distribution of hydrocarbons on their exoskeleton to identify themselves. Unlike our uniforms that can be detected at a distance using visual cues, these compounds can only be smelled by contacting them directly using their antennae (Fig. 18.1). This explains the greetings that ant give each other. By tapping each other, and the ground, with their antennae, the ants are “reading” the hydrocarbons on the visitor’s body. By detecting the range and concentration of hydrocarbons on the body, the ants can determine whether the visitor belongs with the nest or is a potential aggressor. If the right combination of chemicals is present on their body, the ant is permitted passage into the nest. Conversely, if the wrong message is contained, the ants respond with an attack to repel the foreign ant. Of course, all this chemical reading is only possible if the ant’s sensory system and brain have the ability to detect and determine differences in the hydrocarbons on a visitor’s body.

Fig. 18.1  The sentinel’s search. Guard ants will chemically pat down approaching ants with their antennae to ensure that they carry the right chemical mixture that tells the guard they belong in the colony

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Located on the antennae of the ant are small porous bumps called basiconic sensillum. Within these sensillum are lots of nerve endings from olfactory nerves. These nerves contain the primary receptors that are sensitive to the hydrocarbon mixtures on an ant’s body. From here the olfactory nerves travel down the antennae to a series of processing centers in the brain of the ant. The brain of the ant has different areas with names such as the antennal lobe, the lateral horn, and mushroom bodies. These areas have smaller processing units called glomeruli that are really the areas of the brain where differentiation of signals from the antennae are filtered. These glomeruli are really numerous in ants and, in particular, female ants (who make up the majority of a colony). As a result of a highly organized “olfactory” region of the brain, these ants can differentiate a broad range of hydrocarbons and are exceptional at differentiating small differences in concentrations of hydrocarbons. Again, this is similar to being able to tell that the words riding and ridding are really different and contain different meanings. Thus, these ants have evolved the ability to read chemical messages on the outer covering of fellow ants and by doing so can determine their species and nest affiliation. The hydrocarbon rain jacket originally evolved to protect the ants from desiccation. If desiccation was the only function of these hydrocarbons, there would be no need to have such a diverse collection of chemicals. Indeed, there would be no need to have a change in hydrocarbons across the various species. Yet, the rain jacket has now evolved into a protective covering as well as a chemical naming convention. Just as surely as a team uniforms and their fans’ apparel signal a shared relationship, the hydrocarbon alphabet performs that same task for ant societies.

Chapter 19

Social Resume

As students in my lab and classes prepare for graduation, one of the key discussions that I often have with them is about their resume. In the academic world, the resume is called the curriculum vitae. Curriculum vitae is Latin and roughly translates into the course (curriculum) of my life (vitae). Different from resumes, the CV, as it is abbreviated, contains information on the degrees and courses one has taken as well as the skills and experiences that are relevant for prospective jobs. Typically, quite longer than resumes, the CVs of much older scientists can contain tens of pages or more. The CV serves as the academic calling card of students and professors. An examination of a complete CV should provide the reader all the details about a person’s professional life. Their grants and publications are presented as a measure of their scientific productivity. Students that have been mentored in the lab or a class are provided as credentials for being a scientific educator. Sections for talks, awards, and other external accomplishments are also included to show that the academic reputation is either local, national, or international. Other sections may include service to the university or outside organizations as well as coverage in popular press. The name CV is, thus, very appropriate for the document, as it contains every possible academic event in one’s life. This document is probably used most often in applications for jobs, promotion, or awards. In other words, it is used in any instance where someone has to judge the status of an individual. How good of a potential graduate student are they? A scan of their coursework, grades, and any research will provide quite a detailed picture. Should we hire them for a faculty position? Examination of their publication, and teaching history as well as any mentoring experience, allows a search committee to effectively rank candidates. Is this person worthy of receiving an award? The number and substance of their publications or teaching record is used by such committees to determine any laudable candidates. It seems strange that a single document serves this purpose, but judgements about the quality of an academic life is also solely based on the material contained in the CV.

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Without any personal experiences with an individual, a written document about the value of a professional life seems the next best way to make these judgements. While the concept of judging the value of individuals on a document might seem a little objectionable, social judgements are based on even less information and information that is far more biased by our backgrounds. It is a core aspect of how social animals, including humans, interact with each other. In the most optimistic vision of humanity, these types of judgements would only occur after many sessions of interacting with individuals including talking with them in detail about their life. Psychological work shows that this optimistic view is not realistic. Humans often make instantaneous judgements about other individuals and rarely stray from that initial evaluation. This can be illustrated with a simple example. Imagine walking into an elevator and seeing someone for the very first time. The conclusions drawn about the individual change dramatically if they are dressed in formal business attire or in clothes that have seen better days. What about their hygiene? Judgements will vary greatly depending upon the grooming applied to their hair and face. A neat and well-kept hairstyle leads to one set of evaluations, whereas an uncut and unruly set of locks leads to a very different conclusion. Clean shaven or neatly trimmed facial hair for men and makeup for women will also influence the status attached to the stranger. All of these examples use visual stimuli, but the more emotional decision is made through the nose. If they smell clean or even with a hint of perfume or cologne, the individual is placed in a far better light than if there is a foul body odor. In many sectors of the animal kingdom, the body odor of an individual is akin to their CV. Instead of exchanging greeting or business cards, animals will assess each other off the odors emanating from their body. Contained within those odors is a vast storage of information about the individual. Probably the most prominent piece of information is their sex and their reproductive state. One of the three primary goals of an organism (along with eating and to not be eaten), and most important aspect of their lives, is the propagation of their set of genes. The ability to determine the sex of an individual, as well as their readiness to mate, is an evolutionary requirement. Apart from sex, body odors can have some of the most intimate knowledge about organisms. My graduate advisor used to refer to animals as leaky bags of chemicals. The internal physiology and metabolism that is active around the clock produces a host of chemicals, some of which are purposefully or even accidently released into the environment. I can’t imagine that anyone purposefully releases foul body odors, but they are released independent of the intent. The connection of these chemicals to the body’s physiology is resolute, and because of this connection, any change in the health or hormonal status of the individual is invariably transmitted to the outside world. The social history of the animal is as apparent in these odors as if this history was presented in a CV. The health, reproduction, and even social history are all wrapped up in the metabolism of the animal. A good smell, such as dogs do when they greet each other, provides insight to who this individual really is. This information can be really important when determining with whom to love and to fight.

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As noted in the previous chapter, one of the most obvious behaviors exhibited in nature is conflict between animals. Most of this conflict is tied to the acquisition of resources such as food, shelter, and mates. Knowing the social history of an opponent or mate can be quite helpful when animals have to make decisions on whether to be a fighter or a lover. Whether a receptive mate is a virgin or has had multiple mates is critical information for determining whether your genes have a chance to be passed on. Whether a potential opponent has won a lot of previous fights or been on the losing end is just as important. In regard to fighting, knowing the social history of an animal can provide critical insight into the probability of winning. The previous social history of an animal determines the current neurochemical state of the brain. If an animal has won a number of previous encounters, a host of neurotransmitters, including dopamine and serotonin, has changed in their concentrations and effectiveness such that the chance of winning again is increased. Losing has the same effect but in the opposite direction. Thus, alpha males or females have different brain chemistry than those animals located at the bottom of the rung. Knowing the win streak of your opponent just might change a decision to engage in a battle or sexual act. The chemicals being naturally released by the body is influenced by the brain neurochemistry, particularly in organisms like invertebrates that have open circulatory systems. Reading an opponent’s body chemistry lays open all of their sexual and social history. This chemical relationship between social success and brain functioning is probably best understood in the crayfish. A model organism for these studies, crayfish are aggressive by nature and have an amazing chemosensory system. Depending on how the count is performed, the crayfish has between 10 and 13 paired appendages sensitive to chemicals in its environment. Essentially all of the functions a crayfish needs to perform to live are done through its ability to smell the world around it. Foraging, social behaviors, mating, avoiding predation, and fighting all hinge on the animal’s ability to perceive important chemical cues in the lakes and rivers it inhabits. In addition, the crayfish is a nocturnal animal, and located beneath the surface of the water, there is rarely any light to use for gathering information. Fairly ubiquitous around the globe, these animals can be found in and around just about any freshwater body. So, on this safari, we shall travel to the bottom of a pristine lake to find our animal.

19.1  Fighting by Molecular Means Crayfish are a cosmopolitan species and are a highly invasive animal. These two factors combine to make them an important species to study. Yet, the aquatic and nocturnal nature of crayfish make them a difficult animal to observe under their natural conditions. Nighttime diving can be both thrilling and scary. Sometimes the visibility in freshwater lakes is quite limited given the algal productivity or sedimentation that naturally occurs. Dive lights provide only the scantest cones of light in which to find your way in the water. Sometimes the visibility is limited to a single

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meter ahead of that previous cone. Outside of this cone, such as your peripheral vision, there is absolute darkness. A type of darkness that is rarely seen in the highly lighted terrestrial world. The thrilling aspect is the ability to see the nocturnal world of lakes which is a very different world than the daytime version. A different set of organisms are active at night, including the crayfish. As they emerge from their shelters and hiding spots, the crayfish move toward areas where aquatic plants are dense and to areas of the lake where detritus gathers. Detritus is terrestrial leaf and plant matter that has fallen into lakes and rivers. This plant matter is one of the staples of the crayfish diet, and animals can be seen fighting over access to these valuable food sources. Finding patches of detritus virtually guarantees that crayfish will be found also. Most of these patches are located at fairly shallow depths, but diving is still necessary to observe the social interactions under natural conditions. Nice, calm nights with a new moon are almost a requirement for these observations. The calm night means little wave action will disturb our observations and a new moon, with its lack of reflected sunlight, tends to draw out more crayfish. The darker the night, the less likely that visual predators, such as pike and bass, will be able to see and capture crayfish. Most lakes have very large populations of crayfish. On good nights, 500 crayfish can be found in a small area, and, relatively quickly, all gathered around the detrital patches. For the adult crayfish, detritus is a hefty portion of their diet, and the right combination of wind and wave action is needed to create the patches. Some of these patches can be as large as a meter in diameter. Each detrital patch can have up to 10–15 animals consuming the precious resource. Given the ephemeral nature of the food source, these good nights are prime feeding and fighting time. A nice little patch of oak and aspen leaves that have started to decay is home to one of the species that I study: the rusty crayfish, Faxonius rusticus. This species is called the rusty crayfish because of a prominent reddish spot on its side. It is a mean and aggressive species that has invaded a large number of habitats across the Midwest of North America. Crayfish are in a group of crustaceans called decapods. The word translates as “ten feet,” and the crayfish technically does have the ten different walking legs with feet attached to the bottom of the legs. Upon closer inspection of the crayfish, it really appears to have only eight walking legs because the first pair has evolved into fairly large and prominent claws. These are its weapons and defensive structures. With them, crayfish are able to defend themselves against attacks from predatory fish as well as rip the arms off of other crayfish. Deadly and powerful, the claws serve as warning signals to both predators and conspecifics alike. If a crayfish feels like it owns a detrital patch or wants to take a patch from another animal, the claws will be the instrument by which fights are determined. Given the density of crayfish and the rarity of detrital patches, these spots are fertile grounds for observing aggressive interactions in crayfish. As another rusty crayfish approaches an “owned” detrital patch, the owner stops eating and slowly turns its body to face the approaching threat. While these movements are obvious, what is more subtle is that the three olfactory appendages of the animal (antennae and two sets of antennules) are busily sampling the surrounding water for chemical cues. As the appendages move and sweep through the water,

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these noses of the crayfish are performing “sniffs” to capture important social signals in the form of odors. The approaching animal is also sampling the water as both crayfish are attempting to find chemical signatures of their opponent in the surrounding odor landscape. As these two crayfish approach each other in preparation for battle, most of the attention is drawn to the large claws. The animals have opened the claws and spread them wide in an attempt to appear bigger to their opponent. It is the initial signal to each other in hopes that size alone will scare off the aggressor. Unseen, among the claw movement, is the increased and intense sniffing being performed. The antennules are rapidly moving downward in the water, and each movement performs another sniff of their opponent. In the meanwhile, the large and long antennae are slowly waving back and forth trying to catch aromas further away from the animal’s body. At the beginning of these fights, these animals will not use their deadly claws as weapons. The fights have been shaped by evolutionary forces to slowly increase in intensity. So, the claws are used as visual displays first and only as deadly weapons if the fight escalates to its most intense levels. At lower levels of aggression, the crayfish will push each other back and forth in an attempt to resolve the fight without injuring each other. There is some speculation that this pushing is designed to measure the mass or size of the opponents as larger animals almost always win the interaction. The animals push and then back off from each other. They slowly circle in an attempt to gauge the seriousness of their opponent. These two actions, push and circle, are repeated in an attempt to resolve the fight. Then suddenly, nothing happens. During many of the fights, the animals will just stop, within touching distance of each other, and simply face the opponent. Sometimes these quiet stages last for minutes. Most casual observers of the fight would think that there is a pause happening here. Maybe the animals are “eyeing” each other up or trying to perform a stare down in hopes that the other will run away. What remains hidden from our visual observation is important chemical communication. These two animals are still fighting but they are fighting each other through chemical signals. During these quiet points, the two animals are creating water currents and at various points will release a chemical signal from the front of their body. Located beneath the eyestalks, the crayfish (and many other crustaceans) have two little white circles called the nephropores. These pores are connected to a bladder and gland system. In the bladder, the crayfish stores water and chemicals, and the exact mix of chemicals is dependent upon the social and physiological history of the crayfish. Both animals will exchange chemical information. Sort of like their resumes and from this information, the animals will be able to tell if they have fought each other before and the outcome of that previous interaction. Even if the crayfish have not fought this specific opponent, the animals can tell if their opponent is dominant or has some social status other than an alpha male. They’ll even be able to tell their opponent’s recent fight outcomes, all from these chemical signals. The information contained in these chemical signals plays a critical role in determining whether fights escalate to higher levels of intensity or whether one opponent will back off

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because they are overmatched. During these fights, the animals will periodically stop, exchange information, and then either walk away or continue fighting. We even have some good evidence that these animals are smelling their own chemical signals in order to compare the two social histories. This would be akin to laying out two resumes on a desk and comparing the experiences and skill sets of two candidates. Each mixture of chemicals in their urine serves as another line on their resume. By comparing the two chemical signals, the animals can determine whether their fighting skills are comparable or whether one is truly outmatched. If the resumes are close, the animals will continue to fight. If one of the chemical resumes is clearly more dominant, then the eventual loser will slowly back off and walk away.

19.2  The Science of a Chemical History Crayfish are quite the model system for these agonistic interactions and examining the role of chemical signals in social behavior. The crayfish has an open circulatory system. Instead of the veins and arteries that we have, the hemolymph, which is the invertebrate version of blood, is free to move around the various organs within the animal’s body. They do have a heart and a series of internal pipes that direct the blood to the various organs. Yet, the controlled delivery of blood to various organs is less precise. This means that chemicals have more freedom to move around in this type of system. Another advantage of the crayfish is the relatively simplified nervous system that is still controlled by two main neurotransmitters, dopamine and serotonin. Although these two neurotransmitters have a host of functions within our brain, they are also important in the emotional and social responses that we display. The same type of responses are seen in crayfish, particularly with serotonin. A lot of work has been done that demonstrates the connection between serotonin and social behavior in crayfish. Given the importance of this neurotransmitter in both mammalian and invertebrate systems, we know how the body produces and releases serotonin as well as the chemicals that are the building blocks and metabolites of serotonin. Finally, the role of the chemical senses in the daily functions of the crayfish cannot be understated. As shown above, the nocturnal animal has very little visual cues that are available when it is active. Thus, it is not much of a stretch to conclude that the many noses of the crayfish are its main source of information about the world. Everything that humans do with their eyes and ears is performed by the crayfish nose. We might even argue that these animals have a rudimentary language of chemicals that dictate all of its social and reproductive activities (Fig. 19.1). As stated previously, chemical signals are intimately tied to the physiology of the animal. Changes in that physiology, due to diet changes, illness, or even reproductive status, are often reflected in the types and amounts of chemical cues produced and exuded into the environment. In a number of ways, the physiology of the body is a good record of what has been consumed and the general health of the organism.

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Fig. 19.1  The chemical intimidation. During social interactions, crayfish release their stored urine toward their opponent and attempt to convince them to retreat from the fight

Doctors perform a series of metabolic tests on patients because it provides them a physiological resume of what the body has recently been through. For crayfish, this physiological record is heavily influenced by their social interactions. As a result of the fights crayfish engage in, which happens to be all of the time, their physiology changes. If they win fights, the production of serotonin increases. As a result of this increase, crayfish become more aggressive and are less likely to retreat from a fight. This is a positive feedback loop. The opposite occurs if the crayfish loses the fight. A negative feedback loop arises. Thus, the serotonin levels in the body are an accurate record of the animal’s recent fight history. The changes in serotonin are mirrored by the metabolites of serotonin that end up in the urine of the animal (Fig. 19.1). This is the same urine that is released during the fights. This chemical connection produces a positive feedback loop. The fight outcome changes serotonin functioning in the body, which changes chemical composition of the urine. This, in turn, is released as a chemical resume that is being read by the other crayfish during fights. Each animal produces this resume during a contest, and they compare the various chemicals and their concentrations. This information is decoded and provides each of the animals the ability to compare their relative fight histories. If the chemical resumes are similar enough, the animals will continue their fights, and they will often escalate to the intense use of their claws. If the chemical compositions are different enough, the fight often ends shortly after the urine release.

Chapter 20

The Emotion of Chemicals

As I have written elsewhere, the world of chemical signals is essentially hidden from us because we are visual and auditory animals. We become aware of the chemical landscape around us only during mealtimes or if something is odd (like a natural gas leak or dirty diaper). Yet, the odorous world is far more ubiquitous than either light or sound. Odors exist in the brightest of light and in the darkest of night. At the bottom of the ocean and deep underground, the chemical landscape exists and contains secrets about the organisms and features of the habitat found there. Although we are far more capable of being in tune with this world, we consciously ignore the signs and signals that are there. The chemical sense is a primal sense in a couple of different ways. It is the first sense that evolved and is even used by single-celled organisms to communicate to each other. When queried about social behavior, humans, other primates, and mammals quickly come to mind. Images of family units, grooming and other care, as well as deadly fights for harems are often thought of. Yet, even single-celled organisms can be social. Usually living the solitary life, the amoeba, Dictyostelium discoideum, calls out for help when food supplies are running scarce. When the call is answered, millions of single cells come together and form a superorganism that is used for sexual reproduction. The ancient and primitive organism uses cyclic AMP as its chemical SOS. This same molecule plays a central role in chemical communication in animals and plants. So, cyclic AMP is an ancient chemical sense that is still functional today. The chemical senses are primal in another way too. In mammals, visual and auditory information is passed through the cortical area of brains. The visual and auditory cortex receives the information from eyes and ears and processes this information. This means that mammals “think” about this information before anything else happens in the brain. Conversely, chemical information is first sent to the limbic system of mammals, which is considered the emotional brain. As a result of this different circuitry, chemical signals and the information contained within them are felt emotionally before they are thought about. This can be considered intellectually primitive in that the conscious part of the brain is not needed for the initial response. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_20

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As a result, chemical signals evoke powerful odor memories and deep-seated emotional responses, which are far more powerful than those evoked originally by visual and auditory stimuli. These primitive signals are the primary sources of information for the animals covered in this section as well as most of the kingdom of life. Organisms easily navigate the complex odor landscape to find their homes and sources of food. They sense these signals with their bodies covered with “noses.” They can construct a sort of 360° panoramic chemical view of the world, while we are locked into two small sensors on the front our face. Many insects have the ability to smell with their feet, so every step provides insight into their unique chemical landscape. Imagine walking barefoot through a field and instead of feeling the plants, soil, and gravel underfoot that you are tasting the very ground you tread. Reaching out with your fingers to feel plants would return the chemical makeup of each individual blade of grass. Each plant, animal, and even the inanimate objects produce chemical signals like little chemical factories. Upon meeting our fellow travelers, their life would be clear to us without a single word being spoken. A sniff would tell us their name and even what they ate for breakfast that morning. The puffs of chemicals produced by the mini-factories covering our skin use the combination of our genetics, health, and diet to expose us to the world. The ability of dogs to detect cancer cells within a body is only a fraction of information that is available to the right nose or tongue. This is the world that is hidden from us but so obvious to most other forms of life.

Part V

Gustation

I have drunken deep of joy, And I will taste no other wine tonight. —Percy Bysshe Shelley

Chapter 21

Putting Your Best Foot Forward

Most humans don’t live on the razor’s edge of life and death. We do not fear predators in the night nor worry about having a shelter to fend off the elements. Known locations of food and water are relatively close, and the need to actively search and hunt for the next source of nutrition isn’t required. There are populations of people around the globe where famine, war, and droughts certainly create some doubt in the veracity of that first statement. There tends to be an abundance of food on the planet, and maybe it is the distribution of this food that is the problem in these areas. Despite these areas of human suffering, we are still the only species on the planet that purposefully eats for pleasure. We can walk into the local coffee shop and have a dozen choices of the strength of our coffee, sweet additives, and artificial flavors. In the grocery store, the simple decision about a breakfast cereal is hampered by the plethora of choices. Most of these choices are not based on health concerns but the flavors used to enhance the eating experience. Due to the advances in the chemistry of flavors, companies are outsourcing the development of their next chip flavors to the general public. The use of contests to arrive at their next flavor has resulted in chips with milk chocolate, garlic Caesar, wasabi ginger, and chicken and waffles that line grocery store shelves. The ability to artificially flavor any type of food to taste exactly how we would want is evidence enough that our need for energy and nutrients has turned into a pleasure-seeking endeavor. The gestalt of an eating experience is a combination of smells as well as taste. The aroma from our food stimulates our olfactory sense before we consume it and while the food is in our mouth. The volatile stimuli travel through the back of our mouth and enter our olfactory system through the back door. Our perception of the odors is combined with the more simplified taste system and provides us the sum total of the “taste” of a meal. Our five tastes, sweet, sour, salt, bitter, and umami, are the limit of the information we gather from our food. Historically, these tastes served specific survival function. For example, sweets tended to signal energy that our bodies need to perform its metabolic function. Our bitter taste is connected to the detection of bad or poisonous food. Given advances within modern society, these two taste subsystems are used more often in the consumption of deserts © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_21

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(sweet) and beers (bitter). Our understanding of the neurobiology of our taste system has allowed chefs and cooks worldwide to create fantastic dishes of complex flavors and aromas. As with our concepts of vision and hearing, the common understanding of what taste is and how it functions is based on a human centric view. Within this view, there are five distinct tastes, and these tastes arise from a sensory organ called the taste buds. Taste buds are only located within the mouth and are neural structures that don’t produce axons. The information from a taste bud is quickly handed off to other neurons and carried to our brain. Finally, taste is strictly used to detect stimuli at close range, i.e., within the mouth and in direct contact with the tongue. This is a description for the mammalian taste system, but mammals are less than 1% of all life on this planet. This description only works for a very small population of organisms. A broader view of taste is possible but difficult. The formal name for taste, gustation, occurs across a wide diversity of organisms and, as one could imagine, varies greatly in structure and in function. So, a definition of taste is very different if that definition is centered on the types of stimuli (food or energy intake), the distance between the origin of the stimulus and the organ, the organ producing the sensation (which isn’t always a taste bud), or the behavioral function of the final act of sensation. As future chapters will present, taste can occur on the outside of the body on little hairs with pores at their ends. Some animals have taste organs all over their body, and these organs contain bipolar neurons (dendrites and an axon) that look indistinguishable from human olfactory cells. While most organisms use gustation for distinguishing healthy from unhealthy consumables, others use it for mating, anti-predator defenses, and social behavior. The animal world is full of diverse mechanisms to taste their world. One of the first model systems for gustation was the lowly house fly (Musca domestica). A common creature across the globe, this animal has evolved alongside humans for a long time. These annoying pests are so intertwined with our lives that they are considered a commensal organism to humans. This means that they live in close association with us (almost like symbiosis), but instead of providing us some benefit, they spread diseases and bacteria. We provide them nice warm shelters to protect them from the environment and copious quantities of food in our trash, on our dishes, or bits and morsels dropped inadvertently on the floor. In addition, our and our pet’s feces are quite useful for laying eggs for their reproduction. They are not particularly good housemates, but all that they have to do is avoid our swings with newspapers or swatters to live another day. Our role in their lives is really to provide them with ample liquids to consume, and we perform this task really well. This is probably why the flies have a much greater affinity for us than we do for them.

21.1  The Walk of Life Our spoils, and even some food items that we are still consuming, serve as the food sources for house flies. Despite their lack of control over their menu, flies are a connoisseur in regard to the consumption of food. Their choices of what constitutes

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good food are a matter of survival. For us, the wrong choice at a restaurant or at home means that we’ll have to eat something that is not enjoyable. Like eating a mixture of spinach and Brussel sprouts, the meal may not taste good, but we’ll still get our nutritional needs. It is unlikely that this odd pairing will lead to illness or death. For the house fly, this choice is literally a matter of life and death. The consumption of the wrong type of spoiled food could lead to the ingestion of poison or other degradation products that are harmful to the animal. The fly has a need to test the meal before consumption. Because of the location of our taste system, we have to start the process of consumption before we can assess the quality of the meal. Of course, we always have the option of spitting the food out of our mouth, but doing this in public is quite the social faux pas. Although allowing your child to do this at home while testing novel food can lead to some hilarious moments. Flies, and a host of other animals, don’t have the ability to spit the food out, so testing before ingesting is a critical aspect of the entire eating process for these animals. While we are just trying to enjoy a pleasant time at cookouts or summer time picnics, those pesky flies are doing their best to make the right culinary choice as they fly around our foods. The aromas arising from the grilled meats, fresh fruit, and homemade salads serve to draw the housefly toward our spreads. The large diversity of choices present a smorgasbord of odors, but not all of these meals are equally pleasing or useful for the fly. The fly will detect an odor emanating from a food source and hone in on that location. For the fly, the dominant choice for a delicious meal contains sweets. The presence of sweet-tasting compounds indicates some form of sugars. These sugars are natural sources of energy and provide the fly with all of the power it needs to make it through the day. Even the caramelized sugars from grilled meats can serve as a nutritious meal for the fly, so the hunt for sugars begins with olfaction. Using plume tracking techniques similar to the male moths in a previous chapter, the fly will find the source of the sweet odors and land near that piece of food. At this point, the fly switches its sensory attention from its olfactory system to its exquisite taste. Walking toward the source of the odors, the fly will traverse the area in search of the meal. The animal will take a few steps and then stop. This behavioral pattern is repeated again and again. In between the steps, it is possible to imagine that the animal is considering something, like it is in deep thought. If the fly is walking across your freshly cooked lunch, the reaction is typically to shoo the animal away. It has invaded the territory of our meal, and we want to protect the integrity and healthy status of our food. If one is brave though, the whole sequence of behavior can be seen, and this sequence provides intimate insight into the mind and sensory world of the fly. During its walk, the fly is tasting the food. Its feet contain a variety of different receptors that are sensitive to the different chemicals present in the meats, fruit, and salads. Each step provides the fly with detailed information on the nutritional makeup of the food underfoot. So, the steps and pauses are akin to our exploration of a candy shop or bakery before making our choice to purchase something. We would walk up and down eyeing the different choices available to us while inhaling the aromas. Our choice for the candy or pastry is primarily based on the olfactory gestalt that each item presents to us. The fly’s steps are giving the animal some

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measure of the sugar levels as well as other potential negative compounds (poisons from decaying food) that are in the food at our picnic. Step by step, the fly gently samples the feast on the table. If the wrong taste is detected, it will lift itself off of the table and search for the next morsel. What is a wrong taste to a fly? Flies crave sweetness. The old adage that you can attract more flies with honey as opposed to vinegar isn’t just about being nice. There is a kernel of truth to the saying. Other flavors, salt, sour, and bitter, are not favored by the animal. The detection of these will cause the fly to move on and not partake of that particular morsel. If the correct taste is sampled, then the fly will eat its fill. On one of those outdoor picnic days, be brave enough to allow the fly to sample the wares and have a little of its own lunch. If this is done, an interesting set of behaviors can be seen. As mentioned above, the fly will walk through the meal and periodically sample the flavors with its feet. If the right amount of sweets is detected, a potential meal is available to the fly. Flies can only consume liquid food or even the juices that are on foods such as fruit or meat. If the fly tastes something good, but the piece of food is solid, like a slice of apple, the animal will move on. For your lemonade or juicy watermelon, the fly will land and slowly extend its proboscis. The proboscis is a tube-like structure that has its own chemoreceptors on it. Extending the proboscis into any liquid allows the fly to drink its fill. Without this extension, the animal doesn’t eat. Similar to the attempt to feed creamed spinach to a toddler. The key to the entire selection and the extension of the proboscis is the feet though. Stimulate the feet with some sugar and out comes the proboscis. Mix a little bitter in with the sweet and the fly is as stubborn as that toddler.

21.2  The Science of Tasting with Your Feet Imagine entering your favorite chocolate shop. A glance around the shop would deliver images of delicious sweets in all shapes and flavors, but most likely, your decision on which morsel to purchase and consume would be based on the initial scents stimulating your olfactory system. The information gathered from this sense provides you with valuable information on the types of aromas and tastes located in each treat. If your olfactory system is impaired by anosmia or literally stuffed up with a cold or flu, the overall experience in the chocolate shop is significantly different. The fly that is buzzing around your food is simply performing the same premeal sampling behavior exhibited upon your entry into a chocolate shop. The fly really doesn’t use its nose, even though it does have an olfactory system. The fly is highly specialized to taste with its feet (Fig. 21.1). Receptor cells associated with the sense of taste are structurally soft and very sensitive to physical deformation. Thus, the idea of walking along on your tongue, as the fly does, is quite the alien concept. The tongue, like our skin, is a soft and supple organ and not really made for the long-term hard labor of walking. The advantage of skin is the ability to grow without going through a molting process and the flexibility that skin provides for moving appendages. Yet, skin is not a very

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Fig. 21.1  Tasty feet. The house fly has taste receptors embedded in its feet and tastes future meals by simply walking around

strong covering in terms of protecting the inside against punctures and abrasions. Small scrapes of the skin can lead to exposure of the internal body which can lead to infection and further injury. Certainly, the skin on our feet is thickened to take the abuse of walking around barefoot. Instead of a skin, flies, like all arthropods, have an external and hard exoskeleton. This covering is an excellent set of armor against the world’s ill will. The fly’s feet, as well as its body, have an exoskeleton that allows it to walk around without the aid of any protecting covering like shoes. This solves one issue of having to walk on your tongue but generates a serious problem for the functioning of the fly’s sense of taste. The downside to having your gustatory receptor cells sealed inside of armor is their inability to have access to the precious food compounds it needs to sample. To solve this issue, the feet of flies are covered with tiny hairs. Called sensillum (which means sensory hair), the feet of flies contain thousands of these hairs spread all along the bottom of each foot. Each of these hairs has a small hole, called a pore, at the tip of the hair. This pore allows molecules within the microliquids covering our food to move inside of the sensillum of the taste hair. With every step across the sensory landscape, the tip of the hair contacts fluids, which then get sucked into the hair through the pore. Each step acts as a taste sample. A good image is the small sips that wine tasters use to sample their wares. The steps of the flies are small sips of its potential meals. Inside the sensillum, the gustatory neurons are grouped together. Although the number varies, most invertebrates have three different gustatory neurons within each hair. The body of the neurons sits below the exoskeleton, and each neuron sends dendrites out into the shaft of the hair. The dendrites are thin tendrils that branch off in even smaller extensions. The dendrites terminate at the pore of the sensillum or right where the taste molecules enter the hair. Here, at the terminal end of the sensillum, is where the important steps of the fly’s taste sensation occur. At the pore, taste molecules find their way into the space near the ends of the dendrites. Located on the end of each dendrite are receptor molecules. Theses receptor molecules are embedded in the membrane of the dendrites and are connected to a series of other cellular proteins that will trigger the response of the neuron. The taste

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molecules, through molecular diffusion, move to the membrane of the dendrite and make contact with the receptor molecules. On the receptor molecule is a binding area that has a certain molecular shape. This means that the binding area has both a 3D physical shape and a series of atoms and ions that can help or stop binding of molecules. Often described as a lock and key mechanism, the receptor molecules are the locks, and the taste molecules are the keys. Only the right key can open the right lock. If the match occurs, the receptor molecule changes its shape and begins a series of cellular cascades that ultimate notify the fly that it has tasted something. All of these molecular interactions occur rather quickly because of the exceedingly small spatial scales at play in the space between sensillum pore and gustatory dendrite. Despite what we might think of the lifestyle of the fly, the animal is actually quite discriminating when it comes to food choice. The fly’s favorite flavor is identical to humans, and that is something sweet. Sweet (mainly sugars) equals energy in the natural world, so it isn’t that surprising that the fly favors this taste over others. Not all taste is equivalent though, as some sugars are favored more than others. The fly appears to have the same preferences as humans do in regard to sweet flavors. The sweetest of the sweet is the sugar, fructose. Fructose, considered the fruit sugar, is perceived as the sweetest by humans and can be found in fruits, honey, and agave. Next in line, in regard to sweetness, is sucrose and, then, in the last place is glucose. If the fly tastes sugar, it extends its mouth parts, the proboscis, and begins to drink its meal. The fly isn’t just tuned to sugars though. As mentioned above, the taste system has evolved to provide information on the healthiness of food. From an evolutionary point of view, healthiness means the presence of energy and the lack of poisonous compounds. So, a good taste system needs to be able to detect both types of compounds, and the fly’s system is exceptional in this regard. Bitter compounds often designate the presence of poison or other unhealthy compounds within potential food items. If the fly’s feet detect the presence of bitter compounds, the proboscis doesn’t extend, and it avoids those foods altogether. The detection of bitter compounds occurs in a similar fashion to how sugars activate the receptor molecules and can occur within the same sensillum as the sweet receptors. The evolutionary function of the taste system is to prevent animals from consuming poor-quality food. Thus, the critical aspect of the taste system is that this ­detection, and the decision to accept or reject the food, needs to occur before the consumption of food. The mammalian system, where the food is actually placed within the mouth for detection, seems quite a poor design. If poor-quality food is sensed, the mammalian system would require the organism to spit the food out. Although the benefit of this system is the plethora of videos where babies react to new foods by spitting them out. The flies seem to have it right. Simply walking along and sensing the quality of the meal would be a wonderful way to approach dinner time. Although, I am not sure I would like walking into a restaurant and seeing the patrons taking strolls up and down the smorgasbord. Maybe it would be better to have the fly’s taste system on our finger tips, and we could dip our fingers in food before consuming them. Either way, maybe we should think twice before shooing those pesky flies off of our food. Instead, watch them and see if they think the meal is worthy of eating.

Chapter 22

The Sweet Taste of Life

Spending the fall in Lund, Sweden, on my sabbatical was quite an interesting endeavor. The fall that I was there was quite rainy and damp. Seeing that I spend most of my research life in and around water, this wasn’t particularly troublesome for me. What turned out to be a minor inconvenience for me was an absolute boon to the lush vegetation around my flat and the university. Just mere steps out of my door was a small garden with seven apple trees and several berry bushes. The fruit was so plentiful that the ground was full of fallen apples. Even with the occasional visitor plucking quite a bit more than a few off of the trees. If I took a 2-min walk down the road, I found myself in the botanical gardens which had a much greater diversity of fruit and berry plants. On my 15-min walk to my office, I would pass other trees including a chestnut tree which had dropped all of the nuts onto the sidewalk. The smells on my runs or walks around Lund were a lovely mixture of ripening fruit, crushed apples on the sidewalks, and bright red berries on all the bushes. I probably could have just closed my eyes and followed all of the scents back to my flat in a similar fashion to the homing salmon. Certainly, the aromas of such a vast array of edible parts of plants were a feast to my nose. A symphony of sweet, tart, and sour odors hung in the air on my various sojourns around the town. The downside of these smells is that I always longed for a nice juicy apple or bowl of berries whenever I came back home. As much as I stopped and enveloped myself in odors at key hotspots along my walks, the sensation was never quite as satisfying as actually consuming the same fruit at home. On my walks, I was only using my olfactory sense, but at home, I could invoke both my sense of smell and sense of taste. It is true that a large percentage of the sensations we receive during meals are due to odors from our food activating our sense of smell. The importance of the sense of smell can be seen in how those individuals that have lost their sense of smell react to food. Anosmia, or the loss of the sense of smell, can lead to a large number of problems including a decreased sense of enjoyment at meals. Without the ability to perceive the rich diversity of odors from a hearty meal, eating becomes functional rather than enjoyable. Plug your nose and an apple tastes just like a potato. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_22

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Yet, our taste buds play an important role in augmenting the dining experience. The five tastes, bitter, sweet, sour, umami, and salt, provide our brain with important information about the food we are consuming. For example, bitterness is often associated with harmful chemicals in foods such as poisons. We tend to avoid foods with these flavors. The sweet sensation is linked with the caloric content of the food which supplies our bodies with the energy needed to carry out all of our daily needs. Even though the enjoyment of our dining experiences is dominated by aromas, our taste provides a clear functional role in determining some aspects about the quality, in terms of health, of the food we consume. When we think about the importance of our senses, we tend to overlook these aspects of our sense of taste. Often, we will rank vision and hearing as the most critical senses to living our lives, but taste hardly ever appears on this list. This may be due to the limited nature of our sense of taste. Hidden inside of our mouth, our taste is really only activated when we purposefully place objects there to be sensed. In contrast, we hear, see, and smell things by pure chance. On my walks around Lund, I heard the noise of the passing cars or cyclists without even focusing on them. The sweet aromas of ripening apples and berries titillated my nose without having to walk up and purposefully inhale the smells. Our tongues are not exposed to the outside world. We don’t walk around casually licking objects akin to our casual glances to see things. We might have a better appreciation for our taste if our tongues weren’t so protected inside of our mouths. What if things were different? What would the world be like if we tasted with our feet? Many animals do indeed taste their environment with various parts of their body which gives them quite a unique perspective of the world. Most flies, like the common house fly, will taste their surroundings with specialized endings on their feet, catfish with their whole bodies, and other animals with their fingers. All of these appendages extend outside of their body exploring the sensory world. Scorpions, which are related to spiders and ticks, have a unique set of structures on their abdomen called peg sensilla. These structures function as mechanical and chemosensory detectors. In order to use these taste organs, the scorpion will walk around the environment and touch its abdomen to the ground in search of food, prey that it has stung, or even good nesting areas. As with other organisms and their sense of taste, the scorpion uses it to locate and discriminate between food items. Certainly, having taste receptors on your feet and stomach is an interesting adaptation, but probably the world’s champion taster has to be the catfish. Catfish are a widely distributed group of fish that appear on every continent except Antarctica. Named for the whiskers (called barbels) on the front of their faces, catfish have amazingly diverse body shapes and colors. Some catfish have exceedingly small and almost nonexistent barbels, while others can have long and elaborate barbels. Most of these animals are found in rivers, but several species inhabit lakes, swamps, and other slow-moving bodies of water. Almost all catfish are bottom feeders and have a flattened body design with a downward pointing mouth that helps them pick up morsels buried deep within sediments. For the purposes of this chapter, the most interesting feature of the catfish are their taste buds.

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The entire body of the catfish is covered in taste buds. Unlike our tongues, the fly’s feet, or even the scorpion’s belly, the catfish do not have a localized taste system. Rather, their entire body functions as a giant tongue. Most animals that move in a single direction have the highest concentration of sensory apparatus near the front. The same is true for the taste system of the catfish. The gills, barbels, and mouth have the highest density of taste buds. This is the part of the body that will most likely encounter potential food items first, so the forward-focused sensory array makes sense. Having a body covered in taste buds is an amazing adaptation, but it really becomes useless unless the animal can tell exactly which part of the body is being stimulated by aquatic odors. When we drink or eat something or even when we smell odors, the experience is very dissimilar to how we hear or see stimuli in our environment. Within each eye, we have a spatial array of receptors covering the back of the eyeball. With two separate eyes and this spatial array, we have the ability to determine with a good degree of accuracy the direction of the light impinging upon our retinas. If an object is to our left, only a certain area (the right side) of our retinas is stimulated, and our brain can easily calculate the location of the object. Our hearing can locate the direction of sound, but that is based on the difference in arrival times of sound to our left and right ears. Regardless of the sense, these two primary senses allow us to navigate spatial cues in our environment. Odors and tastes are very different. When we drink a mug of morning coffee with sugar and cream, our entire tongue is stimulated by the bitterness of the coffee and the sweetness of the additives. We don’t have a spatial array of receptors along our tongue that can differentiate the location of bitter versus sweet tastes. In a similar fashion, we do not have an ability to differentiate smells between the left and right nostrils. Unlike sound, the separate nostrils produce a singular experience, and we have to use other mechanisms to locate the source of aromas. So, why would a catfish need taste buds all over its body? Catfish actually have a somatotopic map of the taste buds on their brain. What this means is that the taste buds on the tail go to a section of the brain that tells the fish that the tail is being stimulated. The same occurs for the mid-body, barbels, and even lips of the catfish. Some fish even have a somatotopic map of the taste buds in their mouth. In these species, the fish often feeds by taking a mouthful of gravel and food on the bottom of a lake or river. They can differentiate the food particles from the dirt in their mouth and press their tongue (actually a bony structure) against the roof of their mouth where there is food. They spit out the rest and keep the food. Unlike our tongue, the taste system of catfish (and other fish) allows them to view the world as a landscape of odors. Viewing odors in space and time is the undersea sensory world of these animals. To discover this world, another trip to the aquatic realm is necessary. We shall chase down the brown bullhead catfish in the murky and stagnant waters of the swamps of the southeast of America. The fish can grow as large as half a meter in length. The brown bullhead has four small barbels under its mouth, two larger barbels on either side of the mouth, and two more on top of the mouth for a total of eight barbels. So, it is well equipped to find food buried deep within the mud, sand,

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and silt of its native habitats. In addition, the body is covered with taste buds in order to help the animal locate potential food items. Catfish are not picky eaters and will readily consume small fish swimming up in the water column. Even for this type of prey, the external taste system comes in handy. The catfish can use information gathered from its entire body to determine where a potential prey is located and attack. We’ll travel to the backwater swamps of Louisiana in the southern part of the United States. Here the catfish rest on the bottom and slowly search for morsels of food buried within the muddy sediment. These can be worms, decayed pieces of dead fish, or even the abundant crustaceans like crayfish and amphipods that inhabit the sediments.

22.1  Searching the Dark for Food The cypress swamps of the American south carry a large diversity of fish. These swamps are a beautiful mixture of terrestrial and aquatic habitats with the main feature being the majestic and tall cypress trees. The massive trunks of these trees create a wide diversity of habitats and serve a refuge for both terrestrial (in their tree tops) and aquatic (among their roots) species. Despite the appearance of a calm water’s surface, the swamp water slowly flows south from Lake Okeechobee to the southern coast of Florida. The water in the swamp is dark and murky due to the shading of the trees and the abundant organic matter in the water. One of the most abundant catfish in the swamp is the brown bullhead, Ameiurus nebulosus. As their moniker indicates, these animals are brownish in color which can fade into a green. While not the biggest of the catfish, these animals can get as large as half a meter in length. Typically bottom dwellers, these predators use specialized receptors to search the muck and sediment on the bottom of the swamp for their own buried treasure: food. Slowly gliding along the bottom of the swamp, these animals can smell food buried underneath layers and layers of soil. The catfish, as a group of fish, have their name because of the prominent “whiskers” that protrude from the bottom of their jaws. Depending on the species, the whiskers, technically called barbels, can number anywhere from two to as high as eight. As they hunt for food, they’ll drag their barbels along the muck in hopes of detecting smells emanating from potential prey items. While the barbels and head have the highest density of receptors, the entire body of the animal is covered in chemical sensors. While these chemical sensors are on the external surface of the animal, the sensors are considered taste and not olfaction. This is primarily due to the construction of the receptors which is identical to the taste buds found within our own tongue. These receptors are connected to nerve endings that are similar to the ones found in the human face and hands. The fine endings in these two areas allow us to locate items on our face and use our hands with great precision. From an evolutionary perspective, these two areas of our bodies are very important for us. With the ability to use tools and fine instruments, we needed a nervous system that allowed fine

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detection and feedback. The same is true for the catfish that is hunting for its meal. Its world is dark and murky with very little information beyond the smell of prey items buried in the sediment. The distribution of taste buds gives the catfish a very fine-scale chemical map of its world. If the animal is stimulated by the taste buds near its tail, it will reverse course because this indicates that there are prey items behind it. As the animal swings around and begins to swim back toward the area where it smelled something with its tail, it swims forward. The forward movement brings the barbels and facial taste buds toward the stimuli. Although the barbels have the highest concentration of taste buds on the body, the entire face is covered with them too. It would be akin to our ability to sense heat with our faces. Imagine taking a hair dryer, on low, and slowly moving it across your face. Even with your eyes closed, you could instantly tell where the dryer was located in space down to the centimeter. This would be a heat map of the world around your face. Although we do this, our map is rather large and crude, and certainly we lack the ability to locate objects with the same precision as the catfish. This catfish has the ability to create this map but uses chemicals instead of heat. As the catfish locks onto its prey, it slowly sways its head back and forth allowing the barbels to drag through the sediments. It is attempting to locate the source of the delicious taste. The catfish is likely sensing all sorts of living animals as well as decaying organic matter in this swamp. Anything from crustaceans, small fish, insects, and even leaves will leave little traces of organic chemicals. The catfish can sense them all and is working hard to focus on the its intended prey. Given its spatial sensitivity and highly tuned chemical senses, the catfish has created a spatial map of the different food patches and prey items around its head. Just as if we were looking down on a map of a city with all of the restaurants marked, this animal knows where all of the food is located and is making its way to its goal. Making several passes over the chemical hotspots, the catfish is fine-tuning its chemical map. As one barbel is stimulated more than the other, the animal turns toward that side. The hunter is closing in on the exact location of the prey. When the catfish is confident in the location of the buried treasure, the animal acts quickly. In a speed that seems impossible given the slow search, the catfish opens its mouth and dives into the muck. With one quick scoop, the animal has captured its prey as well as some of surrounding sediment and is ready to consume its meal. The map was read and the buried treasure was successfully unearthed. By using its advanced sense of taste, the catfish has found another meal in the lightless environment of these swamps.

22.2  The Science of Tasting with Your Body The commonly held distinction of smell and taste is biased based off our own (and other mammalian systems) version of taste and smell. It is important to note that mammals likely represent less than 1% of all of animal life on the planet. So,

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defining sensory systems as important as smell and taste by such a small group of animals certainly misses the larger context of how these senses are being used. One of the ways that scientists divide the sense of smell and taste is based on the anatomy of the receptor cell. The sense of taste is performed using an organ called a taste bud. The taste bud is a cup-shaped structure located in the epithelial tissue of the organism. This tissue can be inside a body cavity (such as a tongue) or the surface of body (such as the skin). Any chemicals floating around come in contact with the top (or apical) end of the taste bud because that end is exposed to the stimulus environment. Here the chemicals react with receptors and begin the process by which the sensation of taste is produced. The taste bud has a larger number of cells in various stages of development and decay. Another distinction between olfaction and taste can be found in the structure of the receptor cell. Olfactory receptor cells have a bipolar anatomy. Bipolar cells have three different parts. Dendrites are located at the outer end of the cell and contain the receptors that will bind to chemicals (aromas in the case of olfaction). The middle part of the cell is the cell body, and this section is where the receptor signals from the dendrites are turned into action potentials. Action potentials are the signals of nervous systems and contain the information that brains use to make decisions. Finally, the last part of the bipolar receptor cell is the axon which carries the action potential to different parts of the nervous system. In contrast, taste buds and the receptor cells within them have no axons. All of the excitation from the activation of taste receptors is kept locally within the taste bud. The information is transmitted to the brain from the taste buds by neurons coming from the central nervous system. This means that, unlike olfaction where the information travels to the brain from the receptors, the brain of the animal plays an important role in determining how and where the sensory information is distributed. The specific connections from the brain to localized taste buds determine where the information goes. Thus, taste information can be parsed out to specific locations within the catfish brain. This feature, receptors without axons, is an important aspect of how the catfish perceives its world (Fig. 22.1). Another important feature of the catfish taste system is the somatotopic map which really is a chemotopic map. A chemotopic map is identical to a somatotopic map but refers to chemicals (chemo) instead of touch (somato). The map part of the word refers to the spatially explicit connections of the neurons. Imagine taking the top layer of a brain and laying it out on a desk so that you have a flat two-­dimensional representation of the brain. Now, imagine lying on top of this flat brain a drawing of a catfish and all of its appendages. This drawing would represent the map of the catfish that is projected onto the brain of the animal. To add one more trick of the mind, imagine that this map and brain are connected to the catfish like some weird construct of the game Operation™. This mental construct can be used to illustrate how the taste system of the catfish works. Take a cotton swab with a particularly tasty morsel, say a bit of crayfish, and touch the tail of our catfish. As soon as this is done, that part of the tail on our drawing lights up. Move the swab to a different location, under the right eye of the cat-

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Fig. 22.1  The body as tongue. The body of the catfish is covered with taste receptors (red dots) which allow them to reconstruct a three-dimensional world of taste

fish, and that exact area on the drawing also lights up. Touch a barbel and the same location on our drawing lights up. The chemotopic map means that the catfish has access to the precise location of a taste chemical in its environment. In addition to this mapping, the catfish has a much higher concentration of taste buds on its barbels and near its head. This increased density means that this section of the map has a much higher spatial resolution than the back of the body. This higher density, and as a consequence finer spatial acuity, enables the catfish to precisely locate food items in dark and murky waters. Dragging the barbels within the sediments increases this accuracy. Once located by its taste map, the catfish moves in and makes the strike where the highest concentration of taste chemicals was located. The combination of taste bud distribution and their unique connections within the brain of the catfish allow them to taste their world in great detail, in a similar way that we feel our physical world with the detail nerve endings in our hands.

Chapter 23

More Than a Feeling

One of the most common items seen across a university campus is the ubiquitous backpack. As fashionable as it is functional, the variety of bags and carrying styles is dizzying. The classic backpack has the two padded straps across the front and a large open storage area. More modern versions of this traditional pack have a webbed cup on the side to hold a water bottle and various small holes in which the wearer can feed cords for headphones. More advanced styles have numerous modular side pockets designed to hold all the electronics that the current crop of students need to carry. Phones, laptops, portable games, charging cables, and even battery banks are just the basics that many students have. In the non-electronic category of items, students transport books, food, water, and even clothing depending on the weather. I feel as some of these students are packing for an assault on Everest as they empty their bags in my classrooms. Besides the classic two strap backpack, students use large purses, cloth bags, the old-school briefcase, and even small rolling suitcases to carry all the necessary items for a successful day on campus. Personally, I have opted for a messenger style bag for my commute. I can easily swing the bag over my head and start my walk or bike ride into work. Although not as loaded as my students’ bags, I do have my computer, charging cables, a leather-bound notebook, pens, earbuds, my wallet, and other various objects. I use the bag on my commutes, during my car or plane trips, and even on days I am out in the field doing research. The bag has become an extension of my body on most days. I have found that one of the best benefits of the messenger style bag is my ability to access the contents without removing the bag. The bag hangs on my right hip, and I can easily flip open the outer flap to retrieve items even while on my bike. Sometimes, I need to grab my phone, or at other times, it is the water bottle that resides in the main section of the bag. I have trained myself to find just about anything in my bag without having to actually look into the bag. The real trick in this ability is being able to “see” with my hand. Using the sensitive sense of touch in my fingers (as we all have), I create images in my mind as my fingers dance around the

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various objects in my bag. Without much work at all, the differences between pens and objects of very different dimensions can be determined. The ability to determine the presence of different objects by the sense of touch is quite a beneficial skill to have for fieldwork too. As mentioned previously, the nocturnal and aquatic nature of my fieldwork requires the occasional need for scuba diving at night. Under conditions with the absence of light and very poor visibility, I often need to reach into the pockets of my BCD to grab a wrench, bag, or even some fine twine. Quite recently, I was doing some mussel surveys in a mucky lake. This task required laying down a meter quadrat, which is a square frame made from thin PVC pipe weighed down with sand, on the bottom of a lake. This action alone caused the fine sediment to shoot up into the water column. While blinded by this silt, I had to reach into my right pocket and grab a single mesh bag out of the three that were in the pocket. After grabbing the bag, I had to find the opening and then run my hand along the bottom of the lake, inside the quadrat, and grab every mussel that I could feel with my fingers. Occasionally, I would feel a rock, but the subtle differences between the smooth surface of the rock and mussel allowed me to distinguish the two. Finally, after sweeping systematically through the entire quadrat, I would zip the bag shut and place it inside the left pocket of the BCD. Of course, this process needed to be repeated at 200 other sites. In the previous chapter, the idea of a somatotopic map was introduced both for our hands and face as well as the catfish taste system. The ability to find that lost pen within a bag or a mussel at the bottom of a mucky lake is done because there is a point-to-point correspondence between the sense of touch in my fingertips to a specific brain region. Thus, when my right pinkie finger touches the tip of a pen in my bag, I know exactly what part of my pinkie finger is stimulated. As I wrap my other fingers around the pen, the subtle different shapes of the pen are transmitted through my fingertips into my brain. I can distinguish the small metal ball on the end of the clip from where the clip connects into the plastic top of the pen. Sliding my fingers around the pen, I can feel the button that would extend the ball point out from the base of the pen. As the physical sensation is sent to my brain, I can form an image in my head of the shape and size of the object and conclude that this is the pen that I was attempting to find. While an exquisite skill to have for finding pens and mussels, imagine having to perform this task to do something far more vital to your survival, like finding food. Of course, I am not suggesting that you shut off the kitchen lights and feel through your cupboards for daily meal. I am not sure I would want to eat a meal constructed in this manner. It would be quite difficult to determine the difference between a can of soup, beans, or cranberry sauce and a box of cereal versus crackers. There are animals where the tips of their fingers (really appendages) are used to find their daily cuisine. One such animal is the common octopus, Octopus vulgaris. As the name implies, the common octopus is a cosmopolitan species and is found in the warmer climes across the world’s oceans. The octopus is part of a group of marine organisms called cephalopods which means “foot head.” The octopus is both notorious and famous for its intelligence and problem-solving. Within aquarium settings, captive octopi can be challenged to solve complex puzzles such as

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u­ nscrewing tightly sealed jars placed inside a closed box to obtain food or to travel through mazes in order to feed. Among more astute observers, the octopus’s eye is equally as famous. As covered earlier in this book, most invertebrates have compound eyes, but octopi have single lens eyes almost identical to humans. The construction of the retina is such that they do not have a blind spot like humans, so it is possible to claim that their eye design is even better than most vertebrates. As a final point about their amazing abilities, octopi have two exquisite adaptations that allow them to be the masters of camouflage. They have meticulous control over the musculature of their flexible body that they can mimic a diverse range of objects in their environment. They can make their bodies appear as rough as coral heads, as smooth as rocks, or as flimsy as plant leaves. In addition to this ability, the octopi’s skin contains chromatophores that allow them to change the color of their skin in very complex ways and in moment’s notice. Yet, none of these amazing traits helps them find their food which is why the animal appears in this chapter. Octopi have a varied diet that can consist of mussels, scallops, fish, crabs, turtles, shrimp, and even other octopi. Because of the large and diverse nature of this diet, the octopi have a set of hunting techniques that are equally diverse and complex. The octopi’s normal habitat is often near or around rocky or coralline structures, which affords them crevices in which to hide. These same crevices are excellent locations for some of the prey on their diet. As such, the octopus faces a challenge that is similar to the ridiculous kitchen scenario presented earlier. Without the aid of their powerful eyes, the octopus needs to determine if something tasty is at the bottom of a deep crevice in a coral head. This problem is further exacerbated by being nocturnal. The darkness of night, coupled with the depth of the water, and deep crevices makes their marvelous eyes fairly useless in the search for food. Akin to reaching into a messenger bag for pens or silt for mussels, the octopus needs to reach within these crevices and determine whether the object they touch is a rock or a shell of a potential prey item. They perform this task with their sense of taste.

23.1  A Sucker for Good Food The octopus is a voracious predator in its ocean habitats. The combination of flexible arms, strong suckers, poison, and forceful beak for a mouth make this creature quite a formidable predator. In particular, the rubbery arms of the octopus have the ability to reach deep within the holes and crevices of reefs to extract mollusks (mussels and clams) as well as crabs and crustaceans. Watching an octopus traverse the rocky terrain is quite a thing of beauty. Each of the arms is controlled independently, and the animal flows along the surfaces in an almost liquid fashion. The tips of each arm will dart in and out of pockets along the surface of reefs searching for a hold to pull the animal along and in search of potential meals. Even if the terrain is a pile of rocks or rubble, the small spaces between the rocks can hold delicious prey who think the smaller spaces can effectively hide them from predators. Deep within these spaces, the octopus can find its favorite food, crustaceans.

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Crustaceans as a group have hardened exoskeletons and can easily be mistaken for inanimate objects like rocks. As the octopus flows along these surfaces, the arms will reach into holes attempting to determine whether an object is food or rock. Unlike feeling through our purses or bags for a specifically shaped pen, the octopus can’t simply rely on the sense of touch to determine if the right object has been found. The fundamental differences between the rock and the hard exoskeleton of a crab are the chemicals found on the shell of the crab. The octopus uses its sense of taste to detect these chemicals, and as for its sense of taste, the octopus is quite a discriminating hunter. Sweeping across the coral reef, the octopus typically keeps the tips of the arms curled inward and back toward its body. While the exact reason underlying this behavior is unknown, it may serve to protect the small and sensitive ends of the arms of the octopus during movement. On the hunt for an appetizing crab, the octopus knows to be careful. Its prey has powerful claws that will be used to defend itself against the octopus. Often, these claws, when not fighting off predators, are used to crack open the shells of snails, clams, and scallops that the crab consumes. So, the crustacean definitely has the strength to make quick work of any soft octopus arm reaching into its home. The octopus, with the curled arm, sends a thicker section of the arm into a crevice and then slowly unfurls the arm. As the unfolding arm extends deep into the crevice, the suckers on the underside of the arm will come into contact with the walls of the hole as well as any prey potentially hiding there. The suckers’ function as holdfasts and allow the octopus to extract its food from these holes, but the initial function of the suckers is to taste whatever the arm is touching. Feedback from the gustatory receptors allows the animal to make decisions about whether the prey, unseen and buried within the hole, is up to its usual standard of quality. As discriminating as any New York Times food critic, the octopus frequently passes up prey items, even if it is hungry. The prey has to have the right combination of flavors, and this right combination can change based on the mood of the hunter. Sampling the gestalt of the prey with the gustatory receptors in its suckers, the octopus acts like a wine connoisseur smelling and sipping a bottle of Chianti before a meal. If the right mixture of aromas and tastes are not present, the octopus moves on to the next hole in hopes of finding a better meal. As the animal moves across the surface, hole after hole and crevice after crevice is explored while prey items are tasted. When the right food is found, the arm encircles the prey and drags it out of its hiding spot. Quickly, the octopus brings the prey close to its beak to break apart the outer shell and, in doing so, injects poison into its future meal. The combination of poison and the powerful crushing with the beak is enough to do in just about any prey. That critical choice, right or wrong food, is done by the chemical information provided by the suckers. In addition to functioning as devices to grab, hold, and, eventually, manipulate objects, the suckers are the octopus’s search organ. Before the animal decides to grab, pull, bite, and consume, the octopus determines whether the meal is on today’s menu by sampling the various chemicals emanating from its prey and attached its shell. With eight arms and several hundred suckers per arm, the octopus has thousands of tiny tongues to help with its hunting.

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23.2  The Science of Tasting with Tentacles The sucker on the arm of an octopus is an amazing example of evolution’s design power. Certainly, it is far more evolved than any comparable human designed sucker (like a toilet plunger or kid’s toy), which mainly consists of a rubber or silicone bowl. The octopus sucker also has an internal space that is the “bowl” of the sucker. This area has the complicated name, acetabular lumen, and is surrounded by a set of muscles that are connected to the sphincter (opening) of the acetabular lumen. The muscles serve to close and open the sphincter to generate the suction force. If viewed from the side in a cutaway diagram, this lumen is almost circular with a tiny opening at the bottom. This hole is connected with another opening called the infundibular lumen. This second lumen is what is typically thought of as the sucker. This is the opening that is visible when watching an octopus at an aquarium. As the acetabular muscle contracts, it reshapes the acetabular lumen. As this occurs, a suction is created and the side walls of the infundibular lumen stick to the surface being touched. The octopus has delicate and precise control over these muscles and can create a tremendous force in mere seconds. Just as quickly, the animal can release the suction and move the tentacle (with suckers) to some other location (Fig. 23.1). During these moments of contact, the octopus has the ability to taste whatever substance the suckers have latched onto. The taste is performed by sensory cells imbedded into the skin on the inside of the infundibular lumen. The taste cells, within the sucker, are similar in structure to those cells within the taste buds of our tongues. The cells have a thickened and elongated body that tapers toward the end of the cell that contacts the environment. At this end of the cell, small cilia and microvilli extend outward to connect the cell with the chemical world. As mentioned in the section on hearing, cilia and microvilli are commonly located on the business ends of sensory cells. The two structures are really different. The cilia are technically hairs that extend out of the end of the cell, and the microvilli are actually folds of skin. The functional difference between these two structures found within hearing organs and those cilia and microvilli within chemosensory organs is the

Fig. 23.1  Tasting with an arm. The octopus tentacle has suckers that are ringed by taste receptor cells (red dots). The outer lumen (infundibular lumen) is the part of the sucker that sticks to surfaces and allows the octopus to taste potential meals

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presence of small pores at the tips of the cilia and microvilli. These pores serve to allow chemicals to enter into the cells interior and interact with receptors to produce a taste sensation. At the base, other end, of the taste cell are axons that carry the taste messages to the brain of the octopus. Along with the axon, there are fibers termed collaterals that most likely allow the taste cells surrounding a single sucker to talk with each other. Typically, the interaction of taste cells either enhances the sensation of a taste molecule or serves to inhibit or cancel out sensations that the animal doesn’t need to sense. There are a great number of taste cells around a single sucker where these interactions can occur. A single sucker has around 10,000 taste cells. These cells are arranged in a circular pattern around the lower opening: the infundibular lumen. In some ways, a good analogy is that a single sucker is like a single taste bud in our tongue. So, each individual sucker is quite sensitive to the taste of its environment with all of these taste cells sending signals to the animal’s brain. To complete the amazing calculation started earlier with the number of suckers, the number of taste cells can be added into the equation. If there are around 10,000 taste cells around a single sucker and, conservatively, 200 suckers per arm, the octopus has around 2 million taste cells on a single arm. For an octopus with 8 arms, the final total is over 16 million taste cells placed on elongated and flexible tongues (or arms). With all these taste cells, one wonders what compounds or tastes in their environment activate the taste cells. Here, it seems, the octopus isn’t so different than the rest of the world. In the work that has been to date, the octopus tastes many of the same types of compounds that vertebrates do: bitter, sweet, sour, and salty. Octopi are far more sensitive to these compounds than humans. Their sensitivity is around 100–1000 times greater to these compounds in seawater when compared to humans consuming similar compounds in water. In addition to this high degree of sensitivity to the taste compounds, the octopus can discriminate fine-scale spatial differences in concentration. The animals can tell the difference between two solutions that differ by 30% in their concentration across a single sucker. So, these animals can certainly locate small prey items in the bottom of a hole. There is one other aspect of the octopi’s taste system that is quite novel. The suckers are even sensitive to the compounds coming off the octopi’s own skin but not to compounds coming off from other octopi. So, the animal can specifically taste itself as opposed to just a general octopi taste. This is a critical feature when sending two or more of its arms down into deep crevices hunting for food. The flexible arms are quite the advantage in getting into small spaces, but there is always the potential of accidently grabbing on to your own arm and thinking it is a prey item. Think how hard it is for toddlers or puppies to control their four limbs that remain within their field of vision, so controlling eight unseen arms has to be a difficult task. As the octopus senses its own arm, the suckers on that arm will not lock on to the arm. So, this unique feature is a self-protecting device so that the animal literally doesn’t tie itself in knots. The tasty world of the octopus is illuminated by a series of sensitive tendrils of arms that seek out food. The animal has the ability to send 2 million (per arm) taste cells in 8 different directions and deep-down holes in search of its next meal.

Chapter 24

At Death’s Door

One of the more interesting jobs within the annals of history, at least from a sensory perspective, has to be the taste tester. This is the person who is hired, coerced, or bought into a job whose sole purpose is to sample the food planned for another person. Often this other person is someone who is important, such as a monarch or dictator. The taster samples the various food that has been prepared, and if they survive, the food is deemed safe to eat. Any poisons, poorly cooked meals, or bad food will be detected by the health of the taster before it reaches the king or queen. As a side note, if the taster is sampling beverages, their official title is cupbearer. Taste testers are still being used today as even modern presidents of both the United States and Russia use their skills. The job title of taste tester isn’t really appropriate because the testers aren’t sampling the food for the right mixture of flavors. Their job really boils down to whether they get ill and potentially die or remain unharmed after a fine meal. These individuals usually travel with their employer and will literally eat like kings (or presidents). Not a bad job, although there is that potential downside of poisons hidden in the food. Depending on the number of assassination attempts aimed at the employer, the job security might not be so great also. Thankfully, most of us do not have enough power, money, or enemies that we would need to worry about poison in our food. The requirement for our own personal taste tester or even a cupbearer is probably quite low, but there are chances that we would get food poisoning. Sometimes we’ll even choose to poison ourselves. Foods such as raw cashews, nutmeg, and bitter almonds all contain compounds that produce very uncomfortable aftereffects and, if consumed in high enough quantities, can kill. Some of our favorite foods, like rhubarb, tomatoes, and cassava, have dangerous concentrations of poison in their leaves and stems. The most notorious and dangerous dishes to consume for the intentional poisonous rush are mushrooms and puffer fish. While instances of illness from self-poisoning are rare, food poisoning from poorly prepared meals is quite common. Remembering those times that a slightly off meal is consumed is not very difficult. The day and night of nausea, weakened body, and other artifacts of food poison © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_24

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cement themselves firmly within our brain. The behavioral end point of a bad meal of shellfish or poorly cooked meat is often the avoidance of the meal. We’ll even avoid particular restaurants that serve that specific food for extremely long periods of times, and, for some people, the smell or mention of that food can trigger a quick bout of nausea. The avoidance of the food that made us sick (and the bout of nausea) is called taste aversion. The aversion is a learned behavior that strongly associates the painful physiological experience with the entire sensory gestalt of the meal. The taste aversion is extremely powerful, lasts a long time (if not a lifetime), and even gets generalized to similar foods and smells. The learning that occurs through taste aversion is quite interesting and has a fundamental role in all types of learning. Before taste aversion was discovered (by Dr. John Garcia in the 1950s), most psychologists had the assumption that any type of learning took a large number of repeated “training” sessions to take hold. This longer type of learning was termed classical conditioning. Through this type of learning, psychologists could certainly train animals to do amazing things but only after continuously running sessions where a behavior was paired with stimulus, like Pavlov’s dogs. Animals can learn on their own in nature, but, again, psychologists thought that a large number of attempts were required to have learning occur. Garcia showed quite conclusively that rats could be conditioned to avoid sweetened water (using irradiation to produce the negative effect) after single trials or even with long delays between the water consumption and irradiation. The field of psychology was at first quite skeptical to Garcia’s findings, and it took many years and a herculean effort on his part to get his findings published. Still, the psychological community was swayed rather slowly. Now, many years later, single trial learning has been demonstrated for other types of behaviors and stimuli. The hallmark example of this style of learning is still food aversion. One has to wonder why food aversion is so powerful as animals rarely are the subject of coups or assassination plots. The overthrow of the king or queen of dominance hierarchies in nature is often by brute force and rarely through behind-the-scenes sinister plots. Yet, the natural world is full of organisms attempting to poison their enemies by any means. This relationship, poisoner to target, often occurs between gentle herbivores and their assassins, plants. Most of the noxious chemicals or poisons that human society has produced are readily found within the plant world. Plants are the champion chemists and have turned to the development of noxious and deadly compounds to protect themselves against the ever-present threat of a grazing by herbivores. Unable to move quickly or to fight back physically, plants develop intricate chemical pathways to produce some truly nasty chemicals. As a result of this poisoning, an arms race has developed where grazers need the ability to detect and respond behaviorally to the poisons and plants need to continuously develop more toxic chemicals. This arms race has resulted in animals evolving exquisite taste mechanisms to detect poison and excellent learning, like food aversion, to avoid the consumption of the more noxious plants. One animal known for the detection of poison is the rat. The ability to detect and withstand different amounts of noxious chemical has to be one of the features that

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has allowed the animal to invade human society so successfully. Often eating the leftover meals found within the trash from our dinner plates, rats have the ability to detect bitter compounds which would indicate that food has gone bad. These animals are so adept at this ability that the business of rat poisons is always adapting and changing poisons as the rat’s learn rather quickly to avoid any of the currently used compounds. Apart from our houses and city streets, this ability still helps the animals in their natural setting also. A natural example of this poison detecting ability lies with the desert wood rat, which lives in the western part of the United States. As their name indicates, these animals are found in desert regions or in chaparral (which is a habitat dominated by shrubs). The habitat is quite sparse in regard to vegetation, so every plant is a precious resource to be consumed. The plants, on the other hand, are harmed by the consumption, so they fight back by producing toxic compounds.

24.1  A Gut Feeling The white-throated wood rat, Neotoma albigula, is a small rodent that lives in the inhospitable climates from Texas to California in the southwestern portion of the United States. These areas have plants such as juniper, sagebrush, yucca, scrub oak, and poison oak. The chaparral contains a diversity of plants species, but they are sparsely scattered across the habitat. Most of these plants produce sufficient levels of toxin that to consume them in large quantities would make most animals suffer from digestive track problems. In addition, some of the compounds that these plants produce can cause long-term deterioration of the nervous system. The threat to the wood rat can certainly escalate beyond just poor nutritional health. As a final complexity to the wood rats consumptive riddle, the amounts of toxins and noxious compounds also vary based on season and the degree of previous grazing that has occurred. As a small consolation, wood rats do produce compounds in their livers that serve to detoxify the plant matter, but their liver cannot handle large doses of plant toxins. The problem that the white-throated wood rat has to solve is to determine which plants are low enough in these harmful chemicals to consume without suffering negative consequences. This is where the sense of taste is used, but probably not in the way most people would think. More on that later in this chapter. The white-­ throated wood rat is termed a generalist because it will consume a wide variety of plants. In contrast, kolas are the classic example of a specialist in that they’ll only consume eucalyptus leaves. Evolutionarily, being a specialist allows the creation of unique physiological adaptations for the diet of the animal. There is no need to have liver enzymes for a variety of toxins or plants because only eucalyptus leaves are consumed. A generalist, by its very definition, needs to have a physiological system that can handle a wide variety of toxins as well as a large range of concentrations of those toxins within the plants.

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One of the ways that a generalist can physiologically handle the diversity of plants and their toxins is to monitor the intake of different toxins. Each toxin might have a different concentration that the animal has to be wary of. Thus, not only does the animal need to monitor its own internal health, but it needs to connect that health, or the discomfort, to the plant matter consumed right before that change in health. In a way, the wood rat has to maintain a mental table of the plants it has consumed, the level of toxins it has tasted during that consumption, and the subsequent physiological discomfort that arises as a result of that consumption. A difficult task for the animal as it traverses its environment in search of scarce food. Certainly, the taste buds on the tongue can serve part of that function. As noted in previous sections, the taste defined as bitter is associated with toxins and poisons. As the wood rat consumes its chosen plant, the teeth of the animal serve to grind the plant matter to a pulp. The combination of grinding the plant matter down and mixing it with saliva releases the toxins. These toxins come into contact with the bitter taste cells, which will eventually send signals to the animal’s brain that something noxious is in its mouth. At this point, the animal likely makes a mental note of these toxin levels but continues to consume the meal. This is where the interesting aspects of Garcia’s work on food aversion come into play. The impact of the toxins on the health of the animal is often delayed in regard to the detection of the poison. While the wood rat consumes the meal and tastes the poisons, the effect of the poisons on the animal’s health doesn’t occur for several hours or even days. If you have ever had the displeasure of suffering food poison from a bad meal, you’ll recognize that the impact of that poor meal often hits later in the day or even in the middle of the night. Garcia showed that animals can make the connection between a stimulus and effect that are delayed by hours. This is one of the unique features of food poisoning. For the wood rat, learning which of the toxic plants has caused its delayed discomfort is one way that it handles the variety of poisons and toxins in its environment. Consuming small samples of plants and waiting for any negative effects, the wood rat can learn to avoid particular plants that are high in noxious chemicals. Being selective in its choice and consumption of plants allows the wood rat to avoid any serious long-term side effects of large-scale poisoning. The ability to learn, based on its sense of taste, leads to behavioral modifications such that the animal eats smaller meals of a larger variety of plants and pauses between its meals to allow any detrimental effects to come and go. The white-throated wood rat alters its consumption based on the feedback from its taste buds in order to maintain its health, but its perception of its meals doesn’t only come from the sensory feedback in its mouth. If animals relied solely on the tongue, the entire toxic effect of the meal may be underestimated. The full measure of poisons in the food is not felt until the plant matter is broken down into its constituent components in the stomach. The acidic environment, with its diverse bacteria flora, is an excellent place for beginning the process of extracting nutrients, but this same process releases all of the toxins. Because of this delayed release of the toxins (at least delayed from when the initial poisons are tasted), food aversion might be a less potent version of learning.

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To detect and respond behaviorally, animals have evolved the ability to taste their food beyond their tongues. The stomach and intestines also have taste buds, and these taste buds play an important role in the way that animals perceive their meals. So, while we may savor the aromas and flavors arising from our foods with our nose and tongue, the stomach and intestines have a final say into the overall health gestalt of the meal. Perhaps, it is this gut feeling, or more precisely gut taste, that is subtly guiding our culinary choices.

24.2  The Science of Internal Taste As discussed in earlier chapters, the oral taste sensation is guided primarily through nerve impulses received by taste buds. The bud is a pore on the surface of the tongue that contains several taste cells. Each bud contains around a dozen or so cells that are either taste cells, cells that will eventually form taste cells, or some supporting cells. The cells have hairs at the apical end of the cell that are sensitive to one of the five different types of tastes: sweet, salty, sour, bitter, and umami. Each taste bud has an array of cells sensitive to one of the five different tastes. The concept that different parts of the tongue are sensitive to specific tastes is an old, but quite persistent, myth. These taste buds are located solely on the tongue and are termed lingual receptors. Many scientists would prefer that the concept of taste be reserved for lingual reception, and whether this type of distinction is appropriate is reminiscent of the similar distinction on the sense of smell outlined in previous chapters. Taste, like all other senses, can be defined by the cellular mechanism of detection, the specific receptor cell, the physical construction of the sensory organ, or the behavioral function of the sense. The choice of any singular definition is biased and arbitrary and in most cases is biased by a vertebrate or human-centric view of the world. Setting aside this interesting, but academic, discussion on definitions, the term taste will be applied quite liberally in the following explanation of how animals sense with their guts. The pathway that food follows after ingestion (mouth to esophagus to stomach and then to intestine) creates the possibility of a number of different taste points. Each part of this pathway involves some manipulation and degradation of the food which will further release potential taste compounds. Located in the later parts of this pathway, solitary taste cells can be found within the stomach and intestine of animals. The term solitary is important because, unlike lingual receptors found in buds, the taste cells that line the stomach and intestine are found as single cells. The cells located in these regions of animals’ bodies are often only sensitive to two of the five tastes: sweet and bitter. The taste cells in the stomach and intestines have similar receptor mechanism as the cells in the mouth. The same types of receptor proteins and internal mechanism of activation of the cells are present. They are not considered taste because these stomach cells don’t occur within a bud surrounded by a group of other taste cells. Perhaps these two taste types (sweet and bitter)

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Fig. 24.1  The inside taste. Not all taste buds are external to the body. Many animals have taste buds (green cells) located in the stomach and intestines that help mediate the learning involved in food aversion

remain in these sections of the body because these two tastes represent an ancient and fundamental reason for eating: to gather energy (sweet) and to avoid poisons (bitter). Thus, the stomach and intestines of an animal’s body have the potential for participating in the overall perception of taste. The question remains that even if the cells detect the appropriate compounds, does this information alter the behavior of the animal. If not, this wouldn’t be taste (Fig. 24.1). Maybe a more refined question is do these cells participate in the ability of an animal to learn to avoid poisons. A novel way to test this question is to bypass the lingual sensation of taste and test whether animals can still learn to avoid foods. In an interesting set of experiments, rats were given foods with varying levels of bitter compounds, but instead of allowing the rats to eat these foods, the foods were pumped directly into the stomachs. Thus, the taste cells in the esophagus as well as the stomach were allowed to detect the bitter compounds, and the animal felt the effect of these same bitter compounds. In a subsequent test, the same animals were allowed to sample (orally) different foods, and the rats displayed aversive behaviors to the bitter compounds. These animals altered their food seeking and consumptive behavior based solely on the sensation of taste produced in their intestines. The oral sensation of taste wasn’t required for learning to avoid certain noxious foods. So, the rats learned their food aversion through the stimulation of the taste cells in their stomachs and intestines. This type of food aversion behavior is at least enhanced by the receptor cells in the stomachs and intestines if not entirely driven by this additional sensation. These cells, and the sensation that they produce, are

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more closely aligned in time with the negative physiological effects of toxins in meals. As such, the temporal connection strengthens the association between an ingested food and the sickness that follows. In habitats with plants that are actively attempting to poison them, the wood rats make effective use of these additional sensations to alter their consumptive behavior. Tasting with their stomachs, they are capable of detecting the subtle changes in the levels of toxins within their food. Based on this information, wood rats will increase their water intake to lessen the concentrations of toxins within their system. They also space out their meals to prevent toxins from building up and producing larger and more harmful effects. This system of an internal taste can also help the wood rats bypass the plants trickery. Humans attempt to disguise the taste of helpful bitter compounds (medicines) by hiding or masking the bitter taste with sugary flavors. Cherry-flavored cough medicine is just one classic way that we attempt to fool our bodies into thinking that something bitter is actually good. The advances into our understanding of sense of taste have led to the creation of a host of additives to medicines. Chocolates, fruits, and even birthday cake flavors are used to induce children to take medicine by masking the unpleasantness of the bitter compounds. Plants, while not quite as adept at chemistry, have similar tricks to mask the bitter toxins in their plant tissue. While these compounds may inhibit the ability of the wood rat to initially taste the toxins, the stomach taste receptors are not as easily fooled. Thus, those gut feelings that the wood rats have are powerful and accurate sensations of the potential danger in their food.

Chapter 25

A Different Chemical View

A simple walk around the block with any dog illustrates the importance of the odorous world to these animals. Whether the walk is going to be a short and brisk one or long and leisurely, the dog doesn’t care. Its entire focus is the novel odors and potential trails of chemicals that line its walk. Bits of grass, trees, sign posts, and shrubs are all must stop and smell spots for canines. Contained in these odors are a wealth of information on animals (both canine and otherwise) that have previously passed this spot. Those earlier animals have either left inadvertent signals (body odors) or intentional markings (urinary signals) that advertise the genus, sex, and health of these animals. The sniff of the dog creates a suction that draws any loose aromas into the nasal passage of the animal. When excited, dogs have incredible inhalation rates (8–10 times a second), and each singular whiff serves to inform the dog of the chemical history of this spot. It’s almost as if the animal is reading short stories written by the animals that have passed this point. Certainly, the species of these previous visitors are penned in the chemical arrays left behind. Beyond that, the sex and reproductive status of any dog is as carved out by the odor molecules as clearly as any lover’s initials in a tree. If the previous animal was a potential prey item (squirrel, bird, or chipmunk), then the reaction is quite different, and the dog will begin a more detailed search. These behaviors, at least for our canine friends, are triggered by odor molecules stimulating their olfactory system. In the more recent chapters, there have been stories about the other major chemosensory system, gustation. Usually, humans divide the chemical world into olfaction, which is used for distant chemical signals, and gustation, which is confined to chemical signals that contact the tongue right before the ingestion of food. As demonstrated in the previous stories, this dichotomy is certainly artificial and is biased by a view centered on mammals and other terrestrial vertebrates. Octopi, catfish, and even flies use their exquisite sense of taste in other ways, and in doing so, have a vastly different perception of the chemical world. The preceding chapter demonstrated that this distinction even falls apart for the mammalian sensory world. Woodrats perform gustatory learning that is © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_25

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heavily influenced by taste cells deep inside their digestive track. Thus, the concept of olfaction and gustation is not as clear and definitive as the common use of two different words would imply. To muddy the waters even further, there is a third important chemical sense found among the vertebrates of this world. Within the scientific world of sensory ecology, the chemical senses (both smell and taste) lag behind the level of understanding that is present for vision and audition. One explanation for this discrepancy is that humans acquire information about our world primarily through the visual and auditory landscapes, so research efforts follow the importance of the sense to our behavior. Another explanation is that the stimulus for the chemical senses is far more complex to control and deliver in experiments than light and sound. The abundance of diverse chemical compounds that can serve as signals don’t fall neatly along a linear spectrum like light or sound. On top of that complexity, the movement of chemical signals is difficult to measure and quantify because they are transported by turbulent wind or water. The study of turbulent flow is quite a complex and difficult field. Whatever reason, the fact remains that our understanding of the chemical senses is very poor compared to that of vision and audition. This third and last chemical sense, the vomeronasal system, is an even deeper mystery that olfaction and taste. Found only within vertebrates, the debates about the function and use of the vomeronasal systems have been very heated, particularly because of the dearth of scientific knowledge. The vomeronasal system is a chemical sense that is mediated by the vomeronasal organ (VNO). In both location and function, this organ is a hybrid of olfaction and gustation. The organ is also called the Jacobson’s organ in honor of Ludwig Jacobson, a Danish surgeon who was the first person to describe the organ in detail. Sadly, the organ was originally discovered by the Danish botanist and anatomist, Frederik Ruysch, but his works was lost until rediscovered after Jacobson’s work. The vomeronasal organ is a small set of sensory cells that lie within a cuplike structure at the base of the nasal septum. Access to the organ, for chemical signals, is through an opening in the back part of the roof of the mouth. The organ is comprised of a pair of cups residing on either side of the roof of the mouth. Thus, it resides in the mouth like the tongue but responds to chemical signals in a paired fashion like our olfactory system. Initial work on the behavioral function of the VNO tied it directly and solely to pheromone communication. This was thought to be the organ that triggered any vertebrate animal’s responses to sex pheromones. Most of the behavioral responses that animals have to the stimulation of this organ are highly repeatable, related to sexual behavior, and quite dramatic. In many vertebrates, stimulation of the VNO with pheromones causes a behavior known as the flehmen response. Commonly seen in horses, but apparent across a large number of animals, the flehmen response occurs when the animal curls its upper lip backwards, bares its teeth, and inhales chemical signals with its nostrils closed. The response enhances the ability of pheromones to reach the VNO and is thought to be important for intraspecies sexual communication. The response to pheromones is so pronounced that many researchers focused their behavioral work on the functioning of the VNO as a pheromone

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organ. Beyond the mammalian system (in reptiles), the VNO serves a much different function and is involved in predatory behavior. Squamate reptiles are a group of organisms that include lizards and snakes. Most of these reptiles are carnivorous and are quite voracious predators. Their prey can be active adult animals, such as birds and spiders, or passively found within the environment, like eggs. In addition, this group of reptiles can be subdivided into two different types of hunters: active hunters, which seek out and track prey, versus sit-­ and-­wait hunters, which hide and ambush the prey that stumble upon their location. Regardless of their predatory mode, one of the most prominent behaviors displayed by squamate reptiles is the flicking of their forked tongue. Given the historical perception of these animals by humans as evil, we have co-opted the forked tongue as an idiom for duplicitous conversation and action. As such, the forked tongue has become a symbol of negative behavior, and maybe from their prey’s point of view, this might be true. The forked tongue, and its constant flicking, is a fundamental aspect to how these animals perceive their world and become exceptional predators.

25.1  Smelling with a Fork The eastern kingsnake, Lampropeltis getula, is commonly found among the grasslands and open chaparrals in Northern Mexico. Although the eastern kingsnake is found exclusively in these habitats, the entire group of kingsnakes have a broad range of environments in which they can be found. Specializing on the hunting and consumption of other snakes, kingsnakes are also known to eat eggs, amphibians, lizards, and even small mammals. The eastern kingsnake is not venomous and kills its prey by constriction. A very active hunter, the kingsnake, uses its exceptional tracking abilities to track and locate far ranging prey. The kingsnake is territorial in that it has a set range within a habitat in which it frequently hunts. Within this range, the snake is quite active in moving throughout the habitat searching for prey. The kingsnake relies heavily on chemosensory cues to hunt, and its forked tongue is the primary tool used to track prey. Moving through its habitat, the kingsnake is keenly aware of any odor cues in the surrounding environment that signal the presence of potential prey items. As it wanders, the kingsnake moves in a meandering general search pattern in the hopes of detecting a scent trail. The initial cues of existence of prey are the aromas of body odors left behind just like the cues picked up by the dog during its walk. Prey do not actively release these chemical cues but produce these odors as by-products of their natural metabolic processes. Chemical cues are released by breathing, through the various pores and glands near the surface of the skin, and by other natural metabolic processes. A necessary, but unfortunate, situation for the prey, but highly advantageous for the snake. The chemicals are lofting downwind from the prey, and the kingsnake draws them into its nostrils by inhaling. This is the predator’s first hint that a meal is close by, and the snake quickly switches into an active hunting mode.

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The kingsnake’s prey, itself a snake, slithers along the ground as it moves through the environment. As each part of the prey snake contacts the ground as it moves, it leaves behind a small but noticeable, chemical trace of its presence. This trace, like the body odors described above, is unavoidable and will prove to be its eventual downfall. The hunter, stimulated by the olfactory cues, now activates its tracking sense, the vomeronasal organ. The olfactory system has an internal mechanism that creates air currents to bring odor molecules to its receptors. Within mammals, this is called sniffing, and each sniff brings a separate sample to the olfactory receptors. Snakes have similar mechanisms for their nostrils, but the vomeronasal system lacks this ability. The VNO’s location, deep within the mouth of the snake, inhibits the active movement of air, and without this movement, the organ is devoid of chemical stimuli. A chemosensory organ that doesn’t have access to chemicals is a poor design, but the snake (as well as other squamate reptiles) has an interesting solution: their forked tongue. The kingsnake, having caught scent of its prey, shifts its sensory focus from its nostrils to its tongue. The animal’s forked and flexible tongue darts out of its mouth and lightly touches upon the ground in front of it. As the moist tongue contacts the soil, it picks up tiny molecules left behind by its prey. Retracting the tongue as quickly as it protruded, the snake curls the tongue and gently places the split ends against its vomeronasal organ. Once here, the chemicals stimulate the organ and create information on the prey species that is currently under hunt. This entire process is quite rapid and lasts only a few seconds. The hunter has gathered some initial information on its prey but needs to begin the tracking phase. As an active hunter, the kingsnake needs to be able to follow the chemical trail that is left behind by the prey. The kingsnake flicks its tongue out again but this time samples a different location than the first one. The tongue touches some foliage off to one side and gathers any chemical cues that are there. Quickly, the tongue is retracted, and this chemical sample is presented to the vomeronasal organ for analysis. The hunter repeats this process again but samples a third, and unique, location. The tongue delivers the chemicals, and the hunter is beginning to construct a crude spatial map of the prey’s trail. Repeatedly sampling left, right, and center, the kingsnake can determine the direction in which its prey slithered off. Not satisfied with sampling the soil and foliage, the kingsnake flicks its tongue into the air to pick up any volatile chemicals that might be lingering about. Left, right, up, and down, the kingsnake flicks its tongue out at an amazing rate of 20 times a minute. The hunter uses this information to piece together the chemical landscape in front of itself. Comparing the concentration and types of chemicals sampled, the kingsnake heads off in the direction of its prey. As the kingsnake stalks its prey, the tongue repeatedly samples air, soil, rocks, and plants to take quick snapshots of the chemical trial left behind. The chemical landscape is recreated every second to determine where the highest concentration of prey chemicals is located in space. These chemical snapshots are the kingsnake’s world. If the prey headed off to its right, the environment would appear more chemically concentration to that ­direction.

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By updating this chemical photograph at an amazing rate of 20 times a second, the kingsnake has an excellent stilted movie to follow and track its prey. If there are subtle changes in the prey’s path or perhaps the appearance of a potential predator, the kingsnake instantly knows and changes its hunting behavior accordingly. All of this chemical mapping is accomplished solely through the vomeronasal system and bypasses the gustatory and olfactory abilities of the animal.

25.2  The Science of Tracking with Tongues Tracking prey in a three-dimensional world using chemical signals is a difficult task. Most animals use auditory or visual cues because these stimuli have an excellent spatial relationship to the source. Both sound and light travel outward in all three dimensions from the source. Chemical signals are bound to the flow (either air or water) that moves them throughout the environment. Thus, almost by default, chemical tracking is restricted to downwind or downcurrent of the prey. The kingsnake has a set of unique adaptations that allows it to use chemicals to track its prey. The most obvious of these adaptations is the forked tongue. The tongue of most squamate reptiles is quite different than the powerful and squat muscle that resides within the mouths of mammals. The mammalian tongue has been shaped by natural selection to help with the mastication of food. Thus, it is a thick and strong muscular structure. The kingsnakes (as well as other squamate reptiles) have tongues adapted for a completely different purpose, which is sampling the chemical world. The kingsnake’s tongue is thin and flexible which allows the animal to twist, shape, and move the tongue to a much higher degree than mammalian tongues. The increased movement allows the kingsnake to collect chemical samples from a large spatial area in front of it (Fig. 25.1). The next unique feature is the forked nature of the tongue. Certainly not adapted for telling lies, the forked structure actually allows the kingsnake to take two

Fig. 25.1  The forked tongue and VNO. Many reptiles have a vomeronasal organ that is stimulated by chemicals placed on the receptor surface by the tongue. Snakes quickly flick the tongue to chemically sample their world and then place the tips of the tongue on the VNO

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s­ eparate and distinct chemical samples of the world. The left and right tines of the fork contact two different points of the animal’s environment. As the tongue delivers the samples to the VNO, the tongue keeps the samples separated and thus, delivers a left and right chemical sample of the world. After delivering the samples to the VNO, the kingsnake can compare the concentration of the chemicals in the two spatial samples. If the left tine presented a higher concentration to the VNO, the prey went off to the left (at least, to the left side of where the tongue sampled) and vice versa. Without the split in the tongue, the kingsnake couldn’t compare spatial differences of the chemical world, and its tracking of prey would suffer. The split tongue and two samples don’t ensure that the chemicals will be processed as different samples. When vertebrates drink liquid or taste food, the mouth acts as a mosh pit for the chemicals as they get sloshed around and ground down by the teeth. Everything is mixed together, and there is no spatial information. This is not so for reptilian vomeronasal systems. The word “system” is appropriate here because within the kingsnake (and other reptiles), the vomeronasal organ is actually a paired organ, and each organ has a distinct opening to the mouth cavity. Along with this anatomical design, the connection between the vomeronasal system and the main olfactory system is absent in squamate reptiles. In other vertebrates, the two chemosensory systems (VNO and olfaction) are connected and influence each other. Because of these anatomical and neurological adaptations, the vomeronasal system in squamates functions as a fully distinct and operational chemical detection system. The vomeronasal organ is best described as a small inverted cup (called a lumen) or an indentation in the roof of the mouth of the animal. The bottom of the lumen is lined with receptor cells sensitive to a host of chemical signals. Upon stimulation, the receptor cells send their information onward to a brain structure called the accessory olfactory bulb and finally to various parts of the brain that interpret this information. The receptor cells in the lumen respond to hydrophilic chemicals, which are chemicals that can be dissolved in water. Any molecules the snake is hoping to detect have to initially be dissolved in the fluids on the tongue and passed into the lumen, which is also filled with fluid. In its anatomical position, halfway between the tongue and nose, in the types of chemicals captured (hydrophilic), as well as how the signals are processed by the brain (through the olfactory bulb), the vomeronasal system truly is a hybrid between the taste and smell sensory systems. The most interesting design of the reptilian vomeronasal system is the coupling of the forked tongue and lack of interconnection between the paired vomeronasal organs. The openings to the lumen are quite small, and in most reptiles, the tips of the tongue either place the molecules close to the opening or deep inside the lumen itself. The left and right tine of the tongue remain separate through the entire process from flick to delivery. So, for animals like the kingsnake, the forked tongue and the separate organs allow the animal to compare the concentration and composition differences of very small, but spatially distinct, areas of its environment. Both airborne and substrate-borne chemical signals are sampled during the tracking process through the vomeronasal system. The snake uses these signals to create a chemical image of its surroundings at two different scales. There is a fine

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spatial  scale where the snake can detect differences across the tips of its forked tongue. At the larger scale, the tongue darts out in all types of directions at an incredible speed. The speed and disparate sampling areas allow the snake to quickly sample a chemical landscape before it changes due to wind movement. Using these more disparate samples, the snake can form a larger image of the chemical landscape. Central to this landscape is the chemical trail left behind, unknowingly, by the unfortunate prey item. The vomeronasal system helps the snake piece these two scales together to extract directional cues and locate its prey. This quick trip into the world of snakes and tongues has introduced a little known, but significant, third chemical sense. Beyond the world of taste and olfaction, numerous animals sense their chemical worlds with the vomeronasal organ. Since the organ is only found in vertebrates, the question naturally arises about a human vomeronasal organ and its role in our own behavior. The intriguing aspect of this type of question almost always leads to questions about whether humans have a functional vomeronasal system and its sensitivity to pheromones. Humans do have a vomeronasal organ, but the functionality of that organ is quite in doubt. Despite years of searching and attempting to find any sensory capability of the human vomeronasal organ or to link this capability to awareness or behavior patterns, nothing has arisen. It appears that this organ is just another case where animals are sensing a world that is quite different than our own.

Chapter 26

The Gustatory World

The chemical senses are routinely underappreciated by humans. Our social world is geared toward stimulating our eyes and ears and ignores our noses and tongues. Survey after survey reveals that humans rank the chemical senses as the least important sense, and a majority of people feel that life would be fine without these senses. More detailed research displays that the sense of taste is relegated even lower than olfaction on this ranking. This ranking is further exacerbated by the knowledge that the flavor from our foods is mainly aromas being detected by our olfactory system. No longer really used for survival function, except for taste testers and cup bearers, taste really only serves for pleasure purposes during our meals. For humans, at least, our taste buds are a minor addition to our perceptual toolbox. Within the animal kingdom, the sense of taste is from more profoundly used. To fully understand the world of taste beyond our tongues, we need to open our mind to different concepts of taste. No longer should we confine our concepts to an oral sensation. Trapped within our mouth, our sense of taste is accessed only in an active sense in that we must actively put something on our tongues to produce the sensation. The very act of getting ready to consume foods influences how we perceive our tastes. A very common example of this happens when we think we are consuming one type of drink, and it turns out to be another. Frequently, when my wife and I dine out, she’ll order a dark cola to drink, and I’ll get an iced tea. If the cups are opaque enough, it is easy to mix the two drinks up. If I reach for the wrong class, I’ll take a sip expecting iced tea only to be greeted with cola. Normally, the cola wouldn’t taste unpleasant, but the expectations before the act of consumption change my perception. In contrast to humans, for many animals, the sensation of taste is located outside of the oral cavity, and as such, it becomes a far more active sense. Because of the evolutionary design of different taste systems, the world of taste is far more diverse in nature than just about every other sense. Eyes are fairly constrained in their construction across the animal kingdom, and auditory structures show similar conservation. Even noses consistently have flow (either inhalation or flicking of the olfactory appendage) across a wide, diverse set of animals. Taste, though, is an entirely different type of sense both in structure and function across © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_26

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the animal kingdom. From the tentacle tips of octopi to the whole-body sensations of catfish, the natural world is full of flavors waiting to be sampled and analyzed. From the internal taste sensors of the stomach and the mysterious vomeronasal system, this chemical sense is used to track prey, keep animals from being poisoned, and find the next perfect mate. Finally, the natural world is full of molecules firmly attached to all manner of items. Trees, plants, rocks, sidewalks, and the walls all contain a chemical history of the organisms that have passed by that point. We blithely walk past, ignorant of the wealth of information in the chemicals left behind. These molecules weave intricate stories if only we could read them. The fly has the ability to read this history, as does the kingsnake while hunting its prey. The catfish is visually blind to prey buried in the murky depth of swamps but can easily perceive a very precise world with its barbels. In our own world, the floors and sidewalks contain invisible chemical footprints as surely as the footprints left behind in freshly fallen snow. The stories in this section represent just a taste (pun intended) of what animals can perform with their own complex system of gustation. Beyond just the salt, sweet, bitter, sour, and umami, these animals can detect complex mixtures of chemicals and extract critical information for their survival. Their sense of taste can reveal reproductive states of other animals, the difference between self and prey and create spatial images of the chemical world. This knowledge, along with the more pedestrian information about the nutritional aspects of a meal, allows the animal key insights into its survival. Certainly, far more knowledge than what humans extract from our own meager taste system.

Part VI

Tactile

Life is too sweet and too short to express our affection with just our thumbs. Touch is meant for more than a keyboard. —Kristin Armstrong

Chapter 27

Picking Up Good Vibrations

One of my favorite places to be in nature is near water. The sound of running water is soothing and, if I am alone, can produce a Zen-like meditative state. Staring at the ripples on the water’s surface and the constantly changing distorted reflections of the surrounding terrain is all that is needed for a meditative pause. Often though, the sounds and sights of rivers and streams aren’t enough for me. For some reason, I am drawn to touch the water’s surface. I don’t feel the need to plunge my hand into the water but just to run my fingers along the surface of the river. This interface between air and water is intriguing to me. The need to touch the surface of the water must be a deep-seated emotion, as I have watched countless people run through fingers across streams, rivers, and even fountains. Whenever I am around young children near puddles of water, I watch them do the same sorts of behavior. They’ll slap the water to feel the surface, produce splashes, and create sounds. Pulling their hands away, they’ll stare at the droplets forming on their fingers and follow the tracks of water as it runs down their hand. I don’t understand our shared fascination with touching water. There doesn’t appear to be the same type of attraction for soil or the ground. Maybe because we are always in contact with this terrestrial surface, we become so accustom to it we choose to ignore it. Playing with river water is certainly not the only place where I use my sense of touch. If I am hiking in the woods, I’ll often stop to feel the roughness of the barks on different trees or the surface of any large plants that happen to be sticking out of the ground. The soft, velvety surface of a flower petal or the tiny strands of fibers on grass blades are some of the many targets of my fingertips. As I wrote earlier, we often subscribe to the notion that seeing is believing, but I am far too aware of how our vision is susceptible to illusions. So maybe a corollary adage should be “Seeing is believing, but touching makes it real.” Urban environments have just as many tactile distractions for me. A well-worn wooden railing is a delight for the eyes and tactile sense. The cool and sleek surface of a metal door handle or siding of a building is an intriguing investigation for my fingers. Interestingly, a large number of objects that are at hand heights in the urban environment tend to be on the smooth side. The glass of doors or windows, table and © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_27

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desk tops, mice for computers, keyboards, and even pens are all designed to eliminate roughness. Even the leather binding of my journal is manufactured to give the impression of flat and polished surface. In a number of different ways, these many sleek surfaces are actually the absence of information. The bumps, jagged edges, holes, and hills of rough surfaces can provide our fingers a lot of information about the nature of an object. With our eyes closed, we could easily reach into a bag and determine what type of objects is contained inside simply by the size, shape, texture, and temperature gathered from our hands. Particularly adept individuals could easy tell the difference between coins based on size and the texture on the outer rim of the coin. Without the differences in texture and shape, we would fumble in the bag and grab items at random. In all of these instances, we are using our sense of touch to gather information about the world around us, but we rarely use it to communicate to others. We can set aside unique instances like the hugs given to a person in need or the subtle touch to a lover’s face as there are certainly complex messages being sent. A short aside is necessary here. I am going to lump together what could be separated as two different senses. First, there is the sense of touch that I have alluded to in the preceding section. For humans, our touch is not limited to our fingertips, but the mechanical sensation that occurs at our fingertips and other areas of our body is different. The feeling of clothes against our skin or the wind blowing across our arms can be considered a form of touch, or more technically correct, the tactile sense. These other sensations are mediated through hair cells that are very similar to the hair cells in our inner ear. These cells transmit mechanical sensation through stretch receptors in the cells membrane. The second sense that I am lumping with the first is the ability to detect vibrations. These vibrations are transmitted through very dense media like the ground or hard objects like trees, rocks, or the floors in the human world. A perfect example of vibrational detection is the Tyrannosaurus rex water cup scene in the original Jurassic Park movie. Each powerful step of the dinosaur was transmitted through the ground, up into the car, and finally on to the water cup on the dashboard. Each step created vibrations seen as ripples on the water’s surface and felt as vibrations in the ground and car. Humans are not very adept at this sense, but occasionally, we will have use of this information. Excellent mechanics can tell engine problems by the weird vibrations produced while the car is running. Vibrations sent through the floor of our house by a clothes washer would provide information on an unbalanced load. Yet, these senses, for humans, are only one-way senses. A one-way sense is used to gather information and not really used for communication. Humans can detect vibrations and use that signal to gather information from our environment, but we lack the ability to create vibrational cues as a form of communication. Even the ability to gather information from vibrational signals is very limited. In part, this limitation arises because we tend to isolate ourselves from the vibrational world by wearing shoes over our feet. This padded covering further inhibits any ability to feel for oscillations in the ground beneath our feet. In only rare instances, our hands are placed on objects in order to detect the small-scale pulses or tremors being created.

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The ability to detect vibrations is the first of many senses that are truly alien to us. The detection of magnetic, electrical, vibrational, heat, and other cues are abilities that other organisms possess but humans lack. These signals compose a rich world of information and communication that is invisible to our umwelt. Our evolutionary pathway has turned away from these environmental energies because they lacked any necessary information needed to survive in our ancestral history. But, it would be a mistake to think that these other sensory modalities are minor and relatively unimportant. Take, for instance, the water strider. Water striders have a variety of names such as water skippers, pond skaters, and the theologically driven, Jesus bugs. These bugs are a handful of creatures that truly live at the interface of two distinct domains: air and water. Skating across the surface of lakes, rivers, and even the ocean, these creatures have harnessed one of the fundamental physical properties of liquids: surface tension. The unique adaptations of fine hairs at the end of their legs help spread their weight over the surface of the water. On the surface of the tiny hairs are hydrophobic molecules. Hydrophobic translates into “water fear” but means that these compounds exclude or repel water. The molecules keep the hairs “dry” and allow the hairs, and legs, to maintain their position on top of the water. The high surface tension of the water coupled with the hydrophobic molecules lets water striders skate along the surface of the water at very high speeds. This system of movement produces a visual image of walking on really thick gelatin. Each and every single step sends ripples along the surface of the gelatin and signals the walker’s presence. Additionally, any other walkers would also be sending ripples by moving around the surface. In this scenario, it would be even possible to tap a foot in some sort of rhythmic pattern to purposefully send ripples outward. The intensity of the tap and the frequency could be used for communication purposes, and any returning ripples could be used to determine who is around me. This imaginary scene is exactly the system of communication that water striders have evolved. Called high-frequency ripple communication, water striders can tap their legs on the surface of the water generating small waves that travel outward to any other striders in the vicinity. These signals can be as high as 100 Hz in frequency, and like many communication systems, males have a set of signals aimed at each other for territorial disputes and another set aimed at potential mates. These animals use the unique wave patterns to perform the very important function of differentiating between males and females. This was proven in an interesting set of experiments where the researchers artificially manipulated a water strider’s ability to drum on the surface of the water. A seemingly impossible experiment, the innovative team connected some small magnets and wires to the front legs of a strider. The other ends of the wires were fed through some instruments and into a computer. The computer would then control the intensity and frequency of the signals created by the wired strider. By changing the vibrational cues, the researchers could make other males think that the caller was either another male or a female. If the other striders thought the manipulated strider was a male, they would engage in some territorial calling. Conversely, if the other striders were fooled into thinking the calling animal was a

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female, the other striders would attempt to woo the calling female. This experiment certainly proved enlightening, but it only revealed the tip of the complexity and depth of the water striders vibratory language. Water striders use these complex array of vibrational signals to create territories, establish dominance hierarchies, and fight over food. In the reproductive area, the signals are used to identify the sex of the sender, for courtship, copulatory, and even postcopulatory behaviors. These amazing creatures have a whole language created by exploiting the surface tension of their watery habitat. Since these organisms can be found in pockets of water across most of the continents, a simple journey to any body of water will likely find the striders skirting across the surface. In warmer environments, water striders will perform their reproductive activities year round, but in more wintery environments, the reproductive periods are only during the warmer summer months. The best places to find water striders are calm bays or beaches in lakes and around bends in rivers. Sitting at the edge of the water, the striders are an easy visual target to watch for their social interactions.

27.1  There Came a Tapping Approaching the shore of the lake, large populations of striders can be seen hanging out at the edge and skating along the water’s surface. The warm afternoon sun provides a nice environment under which the striders will create territories and initiate courtship behavior. One particular species of strider, Aquarius remigis, is one of the more common species, and their bodies can reach lengths of 1.5 cm. The long legs can add another half of centimeter in length. The strider has six legs in contact with the water, and the last two pairs of legs are elongated to generate the force necessary to skate and move across the surface of the water. The smaller fore legs are the ones that create the vibrational cues that will be sent to other water striders. As the water striders begin the process of attempting attract a mate, they will draw upon a complex array of communications. By tapping on the surface of the water with their front legs, they can create surface waves that propagate outward from their location. Almost identical to dropping a small pebble into a quiet puddle, the waves are simple undulations in the water’s surface that move outward in a radial motion. The water striders use the surface tension of the water to create three distinct types of signals. The three signals are a medium frequency (around 22 waves per second and used as call signals to attract females), a lower frequency (12 waves per second to begin their courtship once the females approach), and a high frequency signals (60 waves and higher to fend off males who are entering their territory). The strider begins the communication process by tapping the surface of the water. One can almost visualize the strider using the water’s surface as his personal keyboard and tapping away creating his message. To continue this analogy, as we compose our message, we often pause to gather our thoughts about the next words or sentences. The water strider will also periodically stop in-between messages.

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Unlike our thinking process during typing though, the water strider is “listening” for return signals during his pauses. The incoming messages will be from either other males attempting to take over his territory or from females that might be approaching him as potential mates. The ability to differentiate between the frequency of movement of animals, small background waves created by wind, and the different calls of fellow striders gives this vibrational communication its rich diversity of uses. Upon receiving silence in return to his call, the water strider starts to skate around. The lack of return calls indicates that there aren’t any other striders in this area. So, our focal animal is in search of other striders in hopes of luring in a mate. As he approaches other animals, the strider will stop and generate a couple of calls hoping for the start of a conversation. After another round of calls, our focal animal detects a response. The return call isn’t from a female but from a rival male. Now the two will begin an intense session of wave generation. Facing off, the two males begin their high-frequency calls in hopes of intimidating their rival enough to force him to skate off. Similar to two rival drummers having a contest at a battle between two bands, these males are trying to determine who is dominant by sending the longest and most intense surface waves to each other. These males are signaling their territory by sending high-frequency signals toward each other. The winner will stay, and the loser will likely back off several body lengths. These battles are important for establishing territory which could lead to a likely mating. As the battle rages onward, the striders are striking the water’s surface with great intensity now. At least, great intensity for them. From our vantage point, we would just see ripples upon ripples moving between the competing males. As the battle continues, both the frequency and intensity of the wave generation increase. At some point, one of the animals will recognize that they cannot match their opponent’s vigor and cannot continue signaling at this level of intensity. From our vantage point, the non-focal water strider appears to be slowing down, which is a clear sign that he is giving up. The intensity of the continual wave generation from the focal males is beginning to wear the second animal out. As the focal male continues, the other male ceases his communicates and concedes the territory. Having lost, the tired water strider moves away from the victor to find a new territory in hopes of attracting a female. New territorial boundaries have now been redrawn on this watery map, and the winning male can switch back into mate calling mode with renewed vigor. The switch from territory calls to mating calls is both a drop in the frequency and intensity of the waves. The water strider is calling for any females in this new part of his territory. If his message is heard, the females respond but not by calling back. They’ll move closer to the calling male, and their movement will create a set of surface waves. The female’s slow movement toward the calling male creates just enough of a disturbance that the males can detect their presence. The female approaches in spurts, which creates surface waves that are more irregular than those created during male-male fights. She’ll move forward and then stop. Just like the calling male, these pauses in movements allow her to feel for the mating call of the focal male. If the call has the right characteristics, she’ll find the male attractive and

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move in more closely. As the female approaches, the male continues to lower the frequency and intensity of his calls. These changes are noticed by the female, and she continues her slow approach to the male. If the female chooses this male to copulate with, then the signaling will end with the two water striders making contact with each other.

27.2  The Science of a Touching Reply Vibrational reception is both similar and distinct from what is commonly called hearing. Both senses serve to translate environmental vibrations into neural impulses. For hearing, this is done through a medium such as air or water, and the main transformation is done through a membrane (ear drum) or air-filled sac (swim bladder) that vibrates as pressure or sound waves contact the structure. Within insects and crustaceans, the vibrational sense is detected through structures called the chordotonal organs. These structures contain a bipolar nerve cell and some supporting structures that allow the neuron to become active when external body parts are set in motion. These organs are also used by insects and crustaceans to sense wind movement or even the relative movement of body parts which is called proprioception. This is the same sense that allows humans to know which fingers, elbows, legs, or toe joints are bent without looking at them. For a water strider, its leg has a number of different joints including a rather long foot that rests on top of the water’s surface. For simplicity’s sake, the leg can be imagined as the capital letter Z with the body attached to a joint at the top of the Z. In this scenario, there are three joints. One that attaches the body to the top of the Z and one at either end of the diagonal line that forms the middle of the Z. In real life, the water strider’s legs are stretched out in all directions, such that the angles between the joints are greater than 90°. In the capital letter Z, the angles are far less than 90°, so for the analogy to work, the Z needs to be stretched in the horizontal dimension. This difference in design and position of the legs is critical (Fig. 27.1).

Fig. 27.1  Feeling the waves. Water striders place their long legs on the water’s surface to detect the presence of waves. The movement of the leg and the angles between the joints allow the water strider to sense its world

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As vibrational cues approach the receiving water strider, the feet of the animal move up and down in rhythm with the crest and trough of the little waves. This upward motion serves to increase the angle between the feet and the bottom leg joint. As the angle increases, stretch receptors located within the nerve endings of the chordotonal organs are activated. The degree of activation is directly proportional to the change in the height of the surface wave. So, more intense surface waves produce stronger neural responses. The frequency of the surface wave is recorded by the speed at which the leg bounces on the water. Imagine sitting at a restaurant and glancing across the room. More likely than not, a number of people will bounce their feet and legs as nervous twitches. People can move their legs with little effort such that the motion is barely detectable or with a lot of vigor causing the table itself to move. The height of the leg bounce is the intensity of the signal, and the speed of the repeated bounces is the frequency. A really nervous person may move their legs rather quickly, whereas a different person would just calmly and slowly bounce in time with some unheard song playing in their head. The water strider’s legs move in a similar fashion as the water’s surface vibrates. The detection and coding of the surface waves only work for water striders if the leg and foot stay on the water’s surface. If we were to attempt to place our hands on a lake’s surface to feel the waves, our hands get swamped by the motion of the water, and the motion of the wave is lost. The unique design on the water strider’s foot is the key to staying afloat. The feet of the water strider are covered with a large number of very fine hairs, over a thousand hairs per square millimeter. Both the top (dorsal) and bottom (ventral) parts of the foot have hairs, but only the hairs on the bottom of the foot are in contact with the water’s surface. The vast number of hairs creates a sizeable surface area which serves to spread out the weight of the water strider. In addition, all of the fine hairs trap air bubbles that help create buoyancy to keep the strider afloat. The greater surface area and trapped air bubbles help the water strider to stay on the surface of the water, but it is the biochemistry of the surface of those hairs that is critical to the detection of surface waves. The hairs and feet of the water strider are covered with hydrophobic chemicals. It is their version of the water repellent chemicals that we add to our raingear. In addition, water molecules are polar (meaning that there is an unequal distribution of charges on the molecule) which causes the molecules to be attracted to each other. So, while the legs repel the water, the water molecules are attracted to each other which creates surface tension. Since the legs repel the water molecules, they stay dry and on top of the water’s surface because of the surface tension. This elegant physical-chemical solution to skimming across the water’s surface creates the possibility of feeling the surface waves as they travel across the lake. While we may not enjoy the sensation of the ground literally moving beneath our feet, the motion of water underneath the feet of the water strider is the window to its world.

Chapter 28

Coordinating the Team

Every 4 years, the sporting world gets intensely focused as nations come together to prove which team is better on the football pitch. The World Cup is a dizzying tournament of games where national pride and individual legacies are at stake. Preparation and qualification for the World Cup is a long and arduous process, so in totality, the event is really much longer than the month the tournament runs. Despite the long period of qualifying, an entire nation’s hopes and dreams, particularly in countries with rich traditions of football, are tied to the events and outcomes of those tournament games. The games themselves are an interesting clash in styles and strategies. Some clubs adopt a more defensive posture and look to counter strike. Others play a more physical game which includes a lot of body-to-body contact. Some clubs prefer highly technical passing and strict sets of plays, while others search for a free-­ flowing style with exquisite ball handling and courageous passes. Each strategy is a reflection of the football culture and, many times, the social culture of the nation. The vast differences in approach and play are reflected in each team’s attempt to fine tune a strategy that works for their current batch of players. In some cases, the preparation and teamwork produce the beautiful game that many countries aspire to. Regardless of style or strategy, the one element in common across all successful teams involved in the World Cup is teamwork. Passes cannot be completed from player to player without knowing where and when teammates will be moving on the pitch. Defenses would be porous, and scoring would be considerably higher without teammates working together as a flawless unit. Although there are shouts or calls that help coordinate the movement of teammates, much of the flow appears to happen spontaneously as passes will be performed even before a player initiates a run. The best coordinated attacks happen with very little overt communication. Players will notice subtle nods of the head or a slight shift in the body position of their teammate before they begin a cut through the defense. Much of this coordination comes from playing and practicing together. The familiarity of movement and ball play between players helps form these unspoken relationships that give rise to the entire team acting as a single entity. All ten field © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_28

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players will move as though there is a single mind controlling their actions. As coordinated as the best teams are, there is still a differentiation of tasks or roles. If everyone played striker or defender, the seamless coordination would still lead to defeat. These two features, differentiation of tasks and coordination of effort, not only lead to success in the World Cup, but they are essential elements for the evolution of social behavior in animals. Usually, when the words “social behavior in animals” are read or heard, the immediate thoughts turn to charismatic megafauna. Examples span from large herds of ungulates on the plains of Africa to the depths of the oceans with pods of whales. At the “pinnacle” of these megafauna is the complex and humanesque behavior exhibited by our closest relatives in the primate community. Within these groups, shared parental care and foraging duties are a common feature of the groups where differentiation of tasks is seen. In addition, coordinated efforts such as the efficient hunting activities in wolves and killer whales demonstrate the ability to use auditory and visual signals to bring down prey much larger than the hunters. By expanding the survey of social behavior outside these large organisms, even more wonders can be found. The architectural design and construction skills of the social insects are rivals to none. Groups of termites build mounds designed with large and complex living quarters on three different continents (Africa, South America, and Australia). Mounds can be several meters tall and tens of meters wide. With ventilation shafts, living quarters, nurseries, and even some gardens, the interior design can surpass some of the best human buildings. These masterpieces of engineering and construction can last decades and are built by the combined effort of millions of workers about the size of a centimeter. These natural architectural wonders are built, just like a world-class football team, through differentiation of effort and coordination of activities. Within human building projects, the coordination usually comes from a central location or person. The architect has blueprints that serve as visual guides about the overall structure of the building. The lead contractor coordinates the general activities of many other subcontractors, and foremen oversee the daily activities at the construction site. An actual hierarchical map of the entire project with all of the communication channels and oversight responsibilities would look as complicated as the inside of a termite mound. In an ideal world, lines of communication are followed, and messages are transferred up, down, and laterally throughout the hierarchy with perfect clarity. Even in this hypothetical and ideal world, the responsiveness of this complex system is slow and fraught with errors. If this level of complexity existed within a football team during play, the ball would probably never even be kicked. The master builders in the social insects accomplish the construction of their nests without the complex internal construction framework that humans have and without the detailed blueprints to guide their building decisions. During their building process, they make decisions on the fly about where work needs to be focused. Without the need to discuss choices with contractors and foreman, the workers decide where to add material, where to demo walls of tunnels, and how many

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t­unnels and openings are needed. The speed and efficiency of this network of communication surpass even the best of football teams with their shouts, slight hand signs, and head nods. One of the main channels that social insects use for communication during the building process is chemical signals. Within the social insects, chemical communication has evolved to quite a sophisticated form of language. Chemicals are used to guide reproductive efforts, create temporary foraging highways, and control the movement of workers in the nests or hives. Whole books have been written about the use of chemicals in insect societies. The other, less obvious, channel of communication used by insects as they build are vibrational signals. Vibrational cues are formed by either drumming on the surface of some substrate (leaves, soil, the walls of a nest) or by rubbing two body parts together and transmitting that signal through those same substrates. These signals are a form of acoustical communication in that mechanical waves are sensed by the insect. Yet, because of the design of the sensory organ, vibrational communication is considered a separate sensory modality. The mechanics of signal production and reception are fundamentally different for signals that are traveling through solid surfaces compared to sound waves traveling through air or water. For examples of vibratory communication, attention can be turned away from the skyward building termites to the subterranean nests of leaf-cutter ants. The name leaf-cutter ant refers to a large group of ants that span two different genera, Atta and Acromyrmex. Most of these ants are found in warm to tropical habitats. These ants can often be seen walking through the forest floor carrying sections of green leaves or blades of grass back to their nests. Not only are these ants excellent builders but are superior gardeners as well. The green foliage is used as the substrate for their vast underground fungi farms. The ants cultivate these farms as their sole food source, and, as such, the importance of well-built and designed chambers for their farms is a key element of their construction. Without a healthy fungus garden, the entire colony will die. The two key elements of a world class football team, differentiation and coordination, are quite apparent in the leaf-cutter society. The colony of ants can be broken down by job roles that mainly fall along the size of the individual ants. The job tasks and the roles that the ants play are called castes, and many different social insects have caste systems. Within the leaf-cutter ants, the different castes are the queen, who is the sole individual that reproduces; the soldiers, large individuals that patrol the opening to the colony nest; foragers, the ones that procure the bits and pieces of leaves; guards, often seen riding along the tops of the leaves and protecting the food from potential interlopers; gardeners and nurses, who tend to the fungus garden and care for the eggs and larvae; trash collectors, leaf-cutter ants produce a lot of trash and have specific chambers dedicated to the storage of that material; and finally, the excavators, who dig out tunnels, build the different chambers, and make repairs to the nest. Along with this differentiation in work effort, the leaf cutter’s colony isn’t simply a big chamber or a series of identical tunnels and openings. The excavators coordinate their efforts to build a royal chamber for the queen, brood chambers for the

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eggs and larvae, garden rooms that allow the maintenance of the all-important fungal gardens, garbage dumps, and even more diversified chambers. An unearthed (and abandoned) leaf cutter colony in Brazil was so large that it extended almost 10 m deep into the soil and required 10 tons of concrete to fill the entire nest. The excavation of the nest required the removal of an additional 40 tons of soil. All of this complexity and coordination are performed without the central oversight of a blue print, architect, or contractor. The leaf-cutter ants produce these large and elaborate subterranean colonies and coordinate the digger’s activities through the previously mentioned vibrational signals. Deep in the colony, particularly in the Amazon region of Brazil, are tunnels upon tunnels that take lots of coordinated effort to construct and maintain. The colonies can possess millions of individuals, some of which work tirelessly to repair the nest and excavate new breeding chambers, tunnels, or even chambers to house the fungal gardens. If humans tried to coordinate a large group of people like this, a tremendous amount of emails, signs, and numerous other forms of communication would be needed. The ants are much better organized than any human construction project because they create tremendous feats of coordination with just a few signals.

28.1  Someone Gently Rapping We shall have to travel to the Amazon to find a leaf-cutter nest. Thankfully, a trail of foragers, all carrying leaves, is an easy thing to spot and track back to their nest. As the foragers enter the nest opening, we’ll follow them down into the darkness. In the dark, tight tunnels of the leaf-cutter ant colony, no visual signals are possible. A couple of meters below the surface without skylights, sunlight cannot make its way through the winding and narrow tunnels leading to the spot where these ants are digging. This situation highlights human’s dependence on light and visual cues to navigate the world. Being placed at the bottom of a dark winding area, like a mine, would be very disorienting to us even with light, but this is the world of the leaf-­ cutter ants. As the ants expand and grown their colony, the need for new chambers, such as another garden, initiates a new construction process. To perform this task, the excavating ant will need to call in help and then systematically show the newcomers where to dig. These dank and dark conditions are the perfect place to use vibratory communication. Leaf-cutter ants perform a series of repeated behaviors in their digging and excavating process. These behaviors serve to form pellets of soil that are then transported out of the nest. As we watch the ants perform these tasks, we can see that sequence of behavior. First, the ant approaches a side wall and touches it with its antennae. This behavior may allow the animal to get a sense of size and thickness of the wall. Once that is determined, it opens its mandibles, cuts into the soil, and then drags the soil toward its feet. Once there, the feet work to compact the soil into a pellet. This process is repeated over and over until the pellet is large enough to

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t­ransport out. Working alone, the new garden addition would be a massive project. Yet, with a million or more feet and mandibles ready to help, the project will get finished rather quickly. A quick review of the anatomy of the ant is necessary before any further explanations about digging and communicating can be understood. An ant’s body is actually made up of three different segments. At the front is the ant’s head. This section contains the eyes, antennae, and other sensory apparatus as well as the mandibles (mouth parts). This section is connected to a smaller section called the thorax. The thorax contains the legs of the ant. The final section is the abdomen (gastor) which is a little enlarged and contains scent glands. The connection between the thorax and abdomen contains a small segment that is flexible which allows the ant to lower its abdomen to the ground to lay down scent trails. In other ants (fire ants for example), the abdomen can contain poison glands that can inflict painful stings. As the leaf cutter goes through its motions to dig, the large abdomen bobs up and down in a continual rhythm. The connection between the abdomen and the small segment that leads to the thorax contains several hardened structures. These structures rub together as the abdomen moves up and down and creates stridulatory sounds (similar to cricket sounds). These sounds are transmitted through the hard parts of the ant’s body and down into the soil. Once there, the sounds are transformed into vibrations carried outward through the tunnel walls. As the initial ant continues to remove dirt from the wall, it periodically stops to produce more vibrations. As this is done, the surrounding walls carry these signals to other ants. This is a call for help to other diggers. Within moments, other digger ants come in swarms to answer that cry for help. As the calling ant begins to finish up and carry its load of soil out of the tunnel, more ants begin to dig at the location our first ant started to remove soil. So, the vibrations not only called in other workers, the exact location of the vibrations is where the highest level of activity from the new ants is concentrated. As such, the ants use a little ground vibration to coordinate the activity of the entire colony. The digging process actually serves two functions. First, and obviously, the motion creates tunnels and rooms such as fungus gardens. Second, the vibrations, carried out through the soil, signal to other ants that a new room or tunnel is being created, and help is needed. Although the first ant has moved off to take its bolus of soil outside the nest, a large number of ants have converged on the location to continue the process.

28.2  The Science of the Excavating Call One of the hallmarks of the societies of social insects is coordination. Having millions of organisms in your society doesn’t work well unless different jobs are parsed out and workers are coordinated. Having all your ants foraging leaves the colony unguarded and the young languishing. So, social insects have developed simple rules and signals that allow fairly complex organizational structures to arise. Whether the structure that is a 5 m tall termite mound or the different chambers of

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a leaf-cutter ant nest, coordination is needed to add material in the right spot while removing it in another. This level of coordination comes from the use of vibratory signals. Many different insect species have stridulatory organs that they use to create both sound and vibrations. Probably the most familiar insect to produce such sounds to humans is the house cricket. Beyond the insects, fish, spiders, and even some snakes produce sounds using stridulation. The sound of stridulation is produced by dragging a hard scraper (technically called a plectrum) across a file, which is a raised surface technically referred to as a stridulitrum. This action is similar to dragging a fingernail (scraper) across a plastic straight comb (file) or even running a stick across a hard, wooden fence. The file, when struck with the scraper, vibrates and creates sound waves. If the file is in contact with the ground, vibrational signals are also produced. The signal can be modulated to a significant degree too. The intensity by which the file and scraper are struck together can change the volume of the sound or the intensity of the vibrations. The speed at which the scraper is dragged across the file changes the frequency of the signals being produced. In addition, the construction of the file plays an important part in the frequency of the sounds being produced. Closer-spaced ridges will produce a higher-frequency signal, and further spaced ridges will do the opposite. Thus, the signal can be modulated to a great degree which creates the possibility of series of complex signals each with their own distinctive meaning. The leaf-cutter ant cannot detect any sounds. So, communicating by using sound waves, similar to crickets, is out of the question. Vibratory signals are carried through different media (air, water, and soil) by waves of motion. In air and water, signals are carried by compression and refraction where the molecules of air get closer together (compression), and in between periods of compression, the molecules space out (refraction). The speed at which these waves move through the material is dependent upon the density of the material. As a result of this relationship, sound travels faster in water than it does in air. In previous chapters on hearing, the detection of sound waves has been discussed and is often performed through the vibration of a membrane. Recognizing that even sound detection involves the movement of some solid medium could lead to the conclusion that even hearing is a form of vibration detection. Returning to our leaf-cutter ants, they don’t have ears that can translate sound waves to vibrational waves. These ants detect the vibration of the soil through hairs on their legs. The organ that produces the vibrations is located between the large bulbous end of the ant (the gaster) and the small joint that connects the gaster to the thorax (the petiole). By changing the way the large gaster moves up and down, the leaf-cutter ants can produce signals of different frequency and intensity. The gaster naturally moves as part of the digging process of the leaf-cutter ants. As such, they are constantly generating signals to each other on where and what work is being done on the tunnels. The workers then respond to help excavate specific tunnels (Fig. 28.1).

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Fig. 28.1  The vibration of the ant. Leaf-cutter ants signal to each other by rapidly vibrating their hind end (the gaster). This motion sense vibrational signals through the soil which other ants detect as a call for help

Further coordination is provided by the modulation of the signal intensity and duration. Leaf- cutter ants increase the intensity and duration of the stridulations during periods of intense digging, such as when constructing a new chamber or tunnel. Conversely, the ants decrease the production of vibratory signals when they have broken through to an existing tunnel or chamber. The surrounding diggers can respond to these changes in an adaptive fashion. The increases in intensity cause workers to congregate and dig, whereas the drop in intensity slows down, and eventually stops, the recruitment of additional diggers. The entire complexity of the construction of these massive colonies is coordinated on site by vibrations. Without a foreman, directions from plans, or even any architects, simple vibrations allow this social ant to construct whole neighborhoods for millions of ants.

Chapter 29

The Rhythm of the Bass

In the first book of the best-selling Harry Potter series, on the first day of school, all the students, as well as faculty and staff, rise and sing the school’s song. To match the quirky and magical setting of the book’s universe, the school’s song has a definitive set of lyrics, but each student is allowed to add their own unique tune to the words. In the story, some students chose upbeat and happy songs, while two characters, the Weasley twins, decided on a long and slow funeral march. The eccentric headmaster of the school, Albus Dumbledore, conducts the twins all the way to the final note as they are the last ones to finish. After the twins complete their version, Dumbledore proclaims, “Ah, music. A magic beyond all we do here!” It appears as if J.K. Rowling, the famous author of this series, was on to something, as music seems to cast a spell upon us. If a happy tune comes across our playlist, our emotions soar just a little bit. Conversely, a more reflective song may switch our mood and we’ll become more somber. Listening to music while exercising can boost our effort and at bedtime lull us to sleep. Recognizing the influence that music can have on our mental state, I have developed my own set of playlists that help me during my periods of writing and another completely different set of songs that I use during data analysis. The beat and tempo of the music seem to find its way into our brains and infects us with its rhythm. The beat primarily, composed of the bass or drums, has a particularly heavy influence. When the right dance song is heard, people will tap their feet or bob their head to the pattern of the song. I have seen this phenomenon walking to work, standing in lines at stores, and while traveling on planes or trains. Whether alone and walking along the street or in very crowded areas, I have seen the telltale signs of someone lost within a song. The head bobs, the toe tapping, and the swaying are all obvious signs that the music has taken hold of someone. Something about the repetitive and consistent nature of the beats induces us to move right along with the song. Within the metal and punk rock music scene, the head bobbing has been taken to an extreme level. Instead of gentle bobbing back and forth or up and down, the head motion is a lot more violent and appropriately called head banging. Performed both by fans and musicians alike, the head banging is sometimes accompanied with very © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_29

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long hair that brings an artistic flair to the motion. Although the origin of head banging is clouded in the mists of time, Led Zeppelin, Black Sabbath, Motörhead, and Deep Purple have all been linked with the first instances of head banging. Clearly, this behavior is tied to the heavy rhythms of this music genre. Today, musicians across a wide spectrum of musical styles can be seen head bobbing or banging in rhythm with their music. One of the origin myths around head banging emerges from a rock group that seems to have its fair share of myths and legends—Led Zeppelin. With the advent of heavy metal in the late 1960s and early 1970s, the high amplification of guitars and basses, along with a heavy drum beat, produced a genre of music that had a deep and massive sound. A side consequence of this type of music was a driving sound that was not only heard but felt by the entire body. The drumbeat and bass, if amplified enough, would create vibrational cues that traveled through the floor of the stage and out into the audience. Led Zeppelin certainly fit the bill of one of the emerging heavy metal bands during this time period. According to legend, on their first United States tour at a show in Boston, Massachusetts, a number of concert goers were seen banging their heads against the stage in rhythm to music. Within similar time periods, patrons of Deep Purple, Black Sabbath, and other groups were routinely seen head banging to their favorite tunes. Certainly, the attendees in the front rows would have felt the reverberations of the instruments through the stage and floors, but it is doubtful that the musicians would detect any of the vibrations created by their fans. So, this version of head banging would not have served any useful purpose at least from a sensory perception point of view, but head banging does exist in several different forms in nature. The most famous head banger that evolution has provided for us is most likely the woodpecker. Woodpeckers are a group of passerine birds whose most prominent trait is the use of vibrational cues to forage and their characteristic drumming against the sides of trees as a form of communication. During my childhood, a large number of woodpeckers could be found in the woods close behind our house. Periodically, one of them would fly to the house and begin drumming on one of the small sections of our house that would be covered in metal. The sound production was both amazing and annoying. The bird apparently enjoyed the amplification of its information as it would continue its drumming for extended periods of time. This type of drumming is actually auditory communication and as such belongs back in Part III of this book. One of nature’s best head bangers is a rare and interesting mammal. As a subterranean group of organisms, mole rats are probably one of the least observed mammals in the world. The term mole rat is used for three families of burrowing rodents. The most famous member of this group is probably the naked mole rat, due to its unique genetic makeup and social structure. These mole rats have eusociality and behave more like bees, wasps, and ants than other mammals. The one thing these interesting animals lack though is the head banging ability of their cousins, the blind mole rats. The blind mole rats, in the genus Nannospalax, are found in Southeastern Europe, Southwestern Asia, and Northeastern Africa. Their entire existence is spent in

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s­ ubterranean environments which lacks light as a source of sensory signals. As their name suggests, they are truly blind as their diminished eyes are completely covered by a layer of skin, so their other senses become the primary mode of communication. Heavy metal bands and their fans could learn a thing or two from these mole rats about head banging. Their primary mode of social communication involves driving their head against the walls of their tunnels to produce vibrations. Males will use these thumps to communicate territorial boundaries as well as aggression and resource allocation. An entire language of head thumps has evolved without the need for drums or basses of the rock bands. Solitary and extremely aggressive, the blind mole rats use this head banging mode of communication when two mole rats meet underground. Most of these interactions are an accidental consequence of tunneling activity but can turn quite deadly for the participants if the interaction is not resolved through these physical signals. In the dark and quiet tunnels, signals are transmitted along the floor and ceiling of the passageway. Imagine the type of behavior humans would exhibit during a blackout or those midnight journeys to the bathroom or fridge. In these instances, most of us would reach out with our hands to feel the wall and move around corners, but this type of sensory feedback is not vibrational in nature. These mole rats add a new layer to the concept of feeling your way with your hand. Not only do they communicate by banging their head against the wall, they also use the bones in their facial region to conduct these vibrations into their central nervous system. In the subterranean world, vibes aren’t just something unknown you pick up on when you meet someone, these vibrations are the entire sensory world for the mole rats.

29.1  Did Thee Feel the Earth Move? The tunnel system of the mole rat is not unlike the massive caverns that the leaf-­ cutter ants from the previous chapter. The tunnels serve as their nests and a safe shelter. As with most subterranean animals, these tunnels are used to travel around underground avoiding terrestrial predators. The mole rat has strong teeth that are used to chip away and dig through the soil. When a large enough lose pile of dirt is fashioned, the pile is moved topside. In addition to the passageways, the mole rats create all the necessary rooms for comfort. There is a specific chamber for birthing and care of the young called a nesting chamber. This chamber is typically the largest underground chamber. Several widened trails have side chambers that are used for the animal’s bathroom, and waste is deposited in those chambers. All of the connecting tunnels vary in width based on how much mole rat traffic crosses those different sections. The tunnel network can be hundreds of meters long and several meters deep. As in the leaf-cutter ants, this system of tunnels and traffic would rival any subway complex in the world. In human subway systems, control of the flow of cars and traffic is critical to the function of the subway system. The same is true for the blind mole rats. So, there is an intense pressure to have an effective communication system both within a population and across different populations within the

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same area. The communication system is designed to carry information about the movement of individuals and the location of potential mates and to reduce aggression by ensuring better spacing among individuals in the population. As individuals decide to expand or extend tunnels, they’ll begin the digging process. Teeth gnaw against the soil, and the legs pull the piles beneath themselves. The digging animal is literally blind to any potential hazards (such as another colony’s territory). Transgressions into another’s territory could create conflicts, so the digging animal needs to ascertain where they are in relation to any surrounding and competing populations. Here is where the communication between populations becomes essential. The digging mole rat switches between two distinct behaviors. The digging behavior is used to create new chambers or extend tunnels, but between bouts of digging, this animal will stop and listen for other diggers that may be in the area. The listening is performed by laying its lower jaw against the side of the tunnel. When this is done, the mole rat is sensitive to the vibrational cues of other diggers as well as the more powerful territorial signals. Just as you or I would feel large vibrations in our feet when a large truck or train passes our house, the blind mole rat can detect the vibrations using its jaw. If everything is clear, the mole rat will continue to excavate until there is enough soil to transport to the surface. After clearing the loose soil, the mole rat returns to its digging. As the excavations get more involved and the side chamber is taking shape, there is an increased chance of running into other colony’s territories. As the mole rat returns from the surface, the animal continues to work on the side walls with periodic stops to listen. As it detects the subtle vibrations of another mole rat digging away, its behavior changes. The two digging mole rats have to determine which population of animals owns the underground territory. In a sense, a distance battle begins, and the winner will get to continue digging. It is a weird battle though as the combatants will not see or even come into contact with each other. The two diggers will begin a series of vibratory signals in order to determine who is the dominant animal and as such, will be allowed to continue to dig in this area. To help generate territorial signals, the mole rats have a flattened top part of their head. Underneath this part, the skull bone is slightly thicker than would be expected on normal mammalian skulls. That part is the signaling tool for the mole rat, and this species is an exceptional head banger. To signal territorial boundaries, the animal forcefully rams its head into the side of the tunnel. Better than any heavy metal fan, this animal is a world champion head banger. The flat area is hardened and creates a nice broad surface which the animal uses to strike the walls. Powerful enough to send signals quite long distances, these signals are used to ward off intruders that are advancing to foreign territories. Most likely, we tend to think of head banging as a slow motion action with a large movement up and down motion associated with it. Yet, these mole rats are trying to really pound the tunnel walls hard, and by doing so, they are creating vibrations that can be used as signals. Unlike our concert goer, the naked mole rats can create relatively fast vibrations using their head. Some of the signals can reach as high as two thumps per second, and, right after producing the signals, they place

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their jaw against the ground to listen for responses. This pattern of communication can seem both dizzying and painful at the same time. They thump their heads and then lower their jaws to detect replies. This is repeated back and forth until one animal decides to exit this area.

29.2  The Science of Bypassing the Eardrum Vibrations are mechanical movements within solid objects. Ripples in water, foot falls within a home, and the drumming of fingers on a wooden desk are examples of common vibrations that are part of our world. Our hearing is not really designed to detect the types of vibrations that the blind mole rats do. Still, if we place our jaw on a solid surface, we can also detect the vibrations in our world. It is rumored that Beethoven overcame his deafness and continued to compose music by using bone conduction. The stories involve the attachment of a metal rod to a piano. As Beethoven played, he would clench the metal rod in his teeth. The vibrations created by the hammers striking the wires of the piano would be transmitted through the rod enabling him to hear the music. Thus, if the right equipment is used, we could even hear the sounds of vibrations. Mole rats detect the head banging signals produced by other animals through a process called bone conduction hearing. The central concept of hearing and bone conduction involves the movement of the tiny ear bones found with mammalian inner ears (covered in Chap. 9). One of the key anatomical designs of the inner ear is the ability to amplify vibrations. The differing sizes of the inner ear bones along with their configuration allow vibrations to be increased in intensity as the wave of motion progresses through the three bones. Often, the movement of these bones is a result of sound waves moving the eardrum, which subsequently creates vibrations in the inner ear bones. A secondary pathway to the detection of vibrations involves the transfer of vibrational energy from bones surrounding the inner ear. The skull, including the jaw, is actually a series of bones connected through sutures and joints. Within the mole rat’s skull, the lower jaw and the bones of the inner ear have a unique configuration. A cup-shaped bone is connected to what is known as the anvil, similar to human inner ears, by a short and thick ligament. This ligament connection creates a physical structure that helps transmit low-frequency sounds from the jaw to the inner ear. While transmitting vibrational signals, these unique shapes are not very efficient at transmitting airborne sounds. In some ways, these mole rats are blind and deaf. By placing the jaw against the tunnel, the mole rat creates a pathway from tunnel wall to the inner ear that effectively transmits any environmental vibrations to the inner ear to be detected. This configuration does make the inner ear more sensitive to low-frequency sounds which are just the type of sounds produced when a mole rat thumps its head against the sides of a tunnel. The flattened, thick skull makes the perfect device for head banging (Fig. 29.1). The mole rats have skulls that gradually slope from the top of the head down to the snout. The skulls of more familiar mammals, like cats and dogs, have a large

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Fig. 29.1  Head banger’s skull. While most mammals have a sloped skull that drops from their forehead to their nose, the mole rat has a flattened skull. The unique shape of the skull is used to both generate powerful vibratory signals and detect incoming vibrations

slope at or near the eyes which then tapers off toward the nose. This type of shape has a curved surface that, if hit against a hard structure like a tunnel wall, would have a smaller striking surface, which means weaker signal. The gradual and continual slope of the mole rat skull creates a large surface area that strikes the walls of the tunnel. The larger surface area creates more powerful signals that would ward off competitors. Rather than a single powerful thump, the mole rats actually modulate their head strikes in order to create different vibrational signals. Although all of the signals are relatively low frequency, less than 10–20 Hz, the differences in frequency appear to carry different information for the receiving mole rat. In addition to these primary signals, the thumping creates secondary vibrations in the tunnel’s surface that can be as fast as 600 Hz. Humans can typically hear in a range of 20 Hz up to 20 kHz, so even these reverberations are in our detection range. These thumping signals appear to function as a deterrent or warning to neighboring mole rats. Despite the blind digging, the extensive tunnel networks of mole rats colony rarely intersect, although the tunnels can get close to each other. When this happens, the mole rats engage in several rounds of head banging and jaw listening to determine the extent of each other’s territory and dominance. Just as head banging at concerts keeps everyone in rhythm, the mole rats use of the same technique to keep their communities peacefully co-existing (or in rhythm) in their subterranean world.

Chapter 30

The Rhythm of the Dance

In a previous chapter, I wrote about the need for unspoken communication in team sports. This is particularly true for sports that are often free-flowing such as basketball, soccer, and ultimate Frisbee. The fast pace and relative uncertainty of where the ball or disc will be moving creates a need for a system of signals that move just as quickly. Players often speak of chemistry when they work together cohesively as opposed to a group of individuals. The chemistry has nothing to do with the sport but everything to do with the ability to predict a teammate’s future action from understated movement of a teammate’s arms and legs or even a head nod. When these teams have good chemistry or are in sync, the fluidity of game approaches that of a world class ballet. When this is missing, the ballet will have the cohesiveness of a grade school production. Apart from the coordination of the individual members, there is a smaller, but as complicated, level of harmony taking place. Watching single athletes perform their craft is as elegant a display of motion and coordination as watching the entire team. The timing and movement of the hand and hip, foot and arm, and chest and knee is exquisite in athletes that have achieved mastery of their sport. Having taught young kids judo for years, I recognize the level of training and discipline that is necessary to move so many body parts in synchrony. Just getting youngsters to move their hands and feet together in a dojo is a lot more difficult than it sounds. Although body parts are certainly not the same as freethinking individuals, the coordination necessary to perform some of the most difficult athletic maneuvers shouldn’t be underestimated. While not athletes, dancers are certainly quite athletic, and their body control extends to the very ends of their bodies. The need to coordinate arms, legs, hips, and torso is a given with dancers, but even average dancers control and emote with the motions they create with the tips of their fingers and the toes of their feet. Whether subtle and slow or violent and fast, the audience interprets the movements of the dancer’s body just as surely as words being spoken. The best dancers, paired with the appropriate music, can evoke such deep feelings in their audience that the watchers can be moved to tears. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_30

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Nature also has its own set of dancers attempting to send their thoughts and feelings to their audience members. The graceful movement of a male swan courting a female is an often seen sight but is a pedestrian attempt at dancing compared to the efforts that other animals go through. The tiny peacock spider will display the brilliant colors on its abdomen (for which its name derives) and shake its legs to some internal mating song. At the other end of the size spectrum, the male of the humpback whales not only will engage its intended partner in a waltz but will sing the tune while dancing. Even these impressive displays are nothing compared to the Clark’s grebe. These freshwater diving birds, with long necks, perform a stunning display with their heads and wings when courting. If these movements are sufficient to impress a mate, the pair rise from the water and dance along the surface. In perfect synchrony, the mates glide across the water with wings back and heads held high in a proud display of bonding. Of course, all of this dancing, and most dancing found in nature, is associated with love and courtship. Males often take the lead and enact their performances in an attempt to convey their attractiveness to the females of the species. In biological terms, attractiveness ultimately means reproductive success. So, the males are sending messages designed to convey the strength of their genes, the commitment to parenting, and the ability to provide food, shelter, and protection to any future offspring. Given the importance of reproduction in the game of evolution, it is not surprising that some of these courtship displays have evolved to be quite complex and compelling for us to watch. The movement of the animal and the motions of brightly colored appendages are designed to send a message of fitness. The brightest displays, the highest jumps, or the most energetic twirls are attempts by the males to tell the females that they are the most suitable mates among all of their suitors. With all of these romantic courtship displays, it would be possible to think that there are no instances of animal dancing outside of reproduction. One of the best studied examples of dancing has nothing to do with mating but everything to do with foraging. That dance is the famous waggle dance of the honey bee. First described by the acclaimed Nobel Prize-winning ethologist, Karl von Frisch, the waggle dance of the bees has been a deep well of scientific exploration for decades. Most of this work centers on the meaning of the dance and the mechanism by which bees supply information to their hive mates. The dance consists of a bee making a semicircle loop followed by a straight line taking the animal back to its starting point. This pathway is flipped on the second go around such that the two loops are in opposite directions and form a Figure 8. The straight middle line of the dance is the waggle part where the bee moves its hind end back and forth at a very high rate. The dance is performed by a returning forager after a particularly successful trip. Other potential foragers gather around the dancing bee and watch the performance. Just as in the mating dances, the movement of the bee creates information, but this information is about the location of the rich food supply rather than genetic fitness. After repeating the movements of the dance several times, the watching foragers turn away and fly out from the hive in search of food. Amazingly, the watchers are incredibly accurate in their ability to find the same patch of flowers that the dancer had visited.

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The bee’s dancing repertoire extends beyond the famous waggle dance. During many other activities, bees will perform a vibrating dance, and this dance often entails a partner. The dancing bee will grasp another bee and vibrate its entire body for a couple of seconds. If satisfied with the dance, the dancing bee moves off to other locations in the nest. As noted in a previous chapter, coordination of activities among hive mates is an important aspect of eusociality in insects. If all the bees were to forage at once, the hive would be defenseless, the queen unattended, and the larvae left to die. So, the communication of which activity is needed and where it is important is thought to be the purpose of this vibratory dance. The vibrations are produced at frequencies that exceed thousands of Hertz which is more than a thousand vibrations per second. The intense movement of the thorax during the dance can be modulated in both intensity and in the frequencies produced. The movement of the thorax creates sounds that travel through the air as well as surface vibrations traveling through the substrate. Both signals are detected and responded to by the surrounding bees which clearly indicates a message is being sent. To intensify the substrate vibrations, the bees can lower their thorax to the comb of the hive. Thus, this dance is a testament to the concept that the rhythm of the dance, rather than the visual waggle, is the real show.

30.1  Shaken, Not Stirred Inside an active hive, thousands of bees move all about performing the tasks necessary to keep the hive alive and functioning. Workers attend to the queen, repair the hive, and take care of the larvae, while at the entrance, foraging bees guard the hive from potential invaders. At the entrance, the other foraging bees return from their trips to the various food sources surrounding the hive. These small little fliers can make foraging trips as far as 10 km from the hive, but most of the trips stay within 3 km. The most successful trips result in the waggle dance that was described above, but the hive is full of activity in many different tasks. The vibratory signal is usually performed by one bee toward another bee that may be finishing up a task or is not quite as active as the surrounding bees. The adage “busy as a bee” is quite appropriate as lazy bees are not tolerated well within this community. If a lazy bee is spotted, other bees will move in to provide the appropriate motivation. After feeding larvae, the worker bees will tend to the various other tasks necessary to keep the hive clean and well repaired. The hive grows or dies with the queen’s eggs, but without these worker bees performing the routine daily tasks, there is no hive at all. Worker bees vary quite considerably with age, and often the younger bees are the ones that need to be motivated or redirected into different tasks. This difference in activity levels may be due to experience or laziness, but in most cases, the older bees are guiding the younger bees to jobs around the hive. After finishing one task, the younger bee may be drifting about or slowly walking to another area of the hive. Once the older bees see this, there is a recognition that action must take place.

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In many cases, the set of tasks bees perform change as they age. The younger ones tend to take care of the larvae, whereas older ones transition into foraging bees. Although not exclusive, most often the foraging bees are ones that deliver the dancing signal. The first step in this communicative dance occurs when the older bee grabs one of the younger bees. Perhaps to get the attention of the young bee, the grab redirects the younger bee’s attention toward its more experience hive mate. The older, and hence, signaling bee grabs the bee with its front two legs and begins a rapid vibration of her own body in a vertical fashion. A related motion would be if we grabbed someone’s shoulders and began bouncing up and down on our toes with excitement. For these two bees, the bouncing aspect of the signal is short in duration, but the vibrations are quite rapid. The signals can range as high as 3000 Hz or 3000 motions up and down per second, which is an incredible rate at which to send these types of signals. Despite this intensity, most of the signals are more in 200–400  Hz range for these bees. The signals typically last only 1 or 2 s, and the signaler then moves off to find other bees to transmit the signal to motivate others to work harder. Once the signaling bee has finished and her message has been relayed, the less active bee will now seem energized and active. Instead of being listless with no active task, the bee is now ready to work on a new activity. So, the younger bee heads off toward the entrance to help with a foraging run.

30.2  The Science of Hips Don’t Lie While the waggle dance of the bees has received a lot more attention than the vibratory signal, both are necessary for organizing activities within a thriving nest. The waggle dance seems solely aimed at communicating successful foraging locations to other bees; the vibratory dance has a much broader message. So broad that the exact meaning and function of the message in the nest has yet to be pinned down. In fact, the signal may carry a more general message for the bees that receive the signal. Vibratory signals are typically used by older bees as they patrol through the nest. These bees walk around and touch other bees with their antennae. What they are searching for with these antennae contacts is also unknown. When these bees do come in contact with a bee that is without a task, moving slowly, or appears to be either directed at the wrong task, the vibratory signal is employed. The delivery of the signal is deceptively simple. The signaling bee simply grabs the receiving bee with her front legs, and once a firm grasp is achieved, she vibrates her body up and down in a vertical motion. This motion achieves a couple of different outcomes. More directly, the motion, coupled with the grabbing of the other bee with the front legs, transfers this motion to the receiving bee. This transfer of physical energy, like a bartender preparing a martini, is the main part of the signal. The other part is transmitted through the floor of the hive. Just as surely as pounding your foot against the floor creates vibrations

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Fig. 30.1  The shaking signal. Related to the famous waggle dance, the shaking signal is used to maintain the efficiency of workers. A bee that is not active is approached by another bee, grabbed, and shaken

that travel outward, the intense motion of the bee also sends physical waves through the floor of the hive. These floor-based signals are received by the bee through its legs. Together, these two pathways of vibration (grasp and floor) create the totality of the signal being sent and received (Fig. 30.1). The reception of this signal appears to be somewhat of a mystery. Unlike the previous examples, where reception of vibration is done through the measurement of foot or leg movement, bees seem to have a different mechanism in play. One of the more prevailing theories is that the shaking of the entire body of the receiving promotes the release of hormones. These hormones, once within the circulatory system, would ramp up the activity levels of the receiving bee. This would definitely be a different take on the concept of signal and reception as this mechanism would bypass any traditional sensory apparatus of the bee. A broad general signal of “wake up!” would fit both the behavior exhibited by the receiving bees and the choice to use this signal by the sending bee. One of the most difficult aspects scientists face in attempting to understand this signal is the broad use and the wide range of behavioral responses. Most signal systems have evolved because there is intense selective pressure on both the sender of the signal to be precise and the receiver to obtain as accurate information from the signal as possible. Thus, signals are most often used in specific situations and contexts. A classic example would be mating signals. These signals are used only when both sexes are in a sexually receptive morphological or physiological state, in the right place near mating grounds, shelters, nests, or territories, and are directed toward organisms of the same species but opposite sex. This is a rather large list of qualifiers on when and where these signals are used. Even within the bee world, the famous waggle dance, that conveys information about excellent foraging locations, is performed in specific areas of the hive and only by successful foragers.

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Conversely, the vibrational signal is directed at a broad range of receivers as there is no specificity in the age, location, or current activity of the recipient. Certainly, there are trends in that the times and context that the signal is generated. The signal is most often delivered by older foragers toward younger and less active individuals, but the words “trends” and “most often” should clearly indicate the broad range of both signalers and receivers. There aspects of the signal have given researchers fits and have really limited the development of a clear signal and detection system that are present throughout this book. Regardless of this lack of definition, this type of signal is another way of viewing the natural world. As humans, we are accustomed to the solidity of the ground on which we walk, and certainly, we would not expect someone to walk up to us and give us a vigorous shake. Yet, vibrations are all around us in the world and a hidden part of our world that carries tremendous pieces of information.

Chapter 31

Tapping into Love

As I prepare to walk into work, I glance out the window and see rain has settled in. Most of my summer field season is spent mucking around in some form of aquatic habitat including lakes, rivers, bogs, fens, and marshes. It isn’t too much of a stretch to say that almost every day of my summer I am wet, so a little rain on my walk shouldn’t deter me. I grab my wide brimmed hat, pull the collar of my coat up, and ready myself for the trip. Exiting the house, I am met with both tiny droplets and a little breeze that drives the rain into my face. There always seems to be some form of wind here in northwest Ohio, so that bit isn’t unusual. I lower my head slightly to provide my face with some protection from the rain and start my daily commute. Although I am not particularly fond of walking with my head down, it does allow me the opportunity to see a different aspect of my world on my commute. Usually, I am glancing skyward at the trees, clouds, or birds that serve as fodder for my introspection. Today, the ground serves that same purpose. It is late March which means that winter is finally fading into the background and spring is pushing its way forward. As a result of this seasonal change, my pathway is dotted with the floral harbingers of spring. The purple and yellow petals of the crocus make a nice contrast with the gray cracks of the concrete sidewalk. The grass, that is greening by the day, and the small buds appearing on the trees coupled with the emerging flowers have brightened my walk despite the gloomy weather that forces my downward gaze. Certainly, an age old story, these colors are not here for my pleasure alone. The selective pressures that evolved these visual delights had no concern for the visual pigments in my eyes or the connections from the eyes to the pleasure centers of my brain. These colors are aimed at the pollinators of the world with a very specific purpose: sex. Pollinator is a fairly broad term that encompasses more than just the common insects that most likely pop into our head when thinking about flowers and their pollen. Besides the bees and butterflies, ants, beetles, wasps, and even mosquitos can act as pollinators. Beyond the insect world, bats, mice, birds, monkeys, and lizards are just a few of the animals drawn to flowers using their visual or chemical lures.

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The purpose of this coevolved game remains consistent in spite of the wide diversity of participants. The lynch pin in evolution by natural selection is reproduction and, in this case, sexual reproduction. Sexual reproduction is the process by which organisms pass along their genes, mixed with their partners, to future generations. In previous sections of this book, I wrote about the use of chemical, visual, and auditory signals in reproduction. The bright plumage of birds, the irresistible aromas of pheromones, and the nighttime calls of the vanishing frogs are mating signals familiar to most of us. Contained within the sights, sounds, and smells are signals that convey many different pieces of information about the mating game. Readiness to mate, strength of a potential mate, and sexual history are just a few of the elements of information that potential partners send to each other in hopes of engaging a mate. The decision to mate and with whom is arguably the most important decision sexual reproducing organisms can make. The game of evolution is won and lost by leaving, or failing to leave, the highest number of copies of your genes in the next generation, an elegantly simple game that can be won by implementing a large and diverse set of strategies. Most of life on this planet plays this game by reproducing asexually. A simple fusion or budding process can produce a prodigious amount of offspring rather quickly. Certainly, this method forgoes the arduous task of finding a mate, determining if they are reproductively active, assessing their quality, and then finally mating. In addition to all this effort, sexually reproducing organisms play a tremendous genetic cost by choosing this method. Only half of their genetic material is passed along to the next generation. Compared to the full complement of genes that asexually reproducing pass along, the 50% is a significant step down. Yet, there are benefits to the recombination of genes that occurs during sexual reproduction such as increased genetic diversity. The numerous other advantages that have led to the evolution of sex can be found elsewhere. Since these advantages do exist, the need to entice other organisms to mate has led to the evolution of mating signals. The tiger wandering spider, Cupiennius salei, has evolved a wonderful mating system that involves intricate drumming back and forth between potential mates. Unlike more familiar orb weaving spiders, the wandering spider truly lives up to its name and is commonly found wandering through the dense forests of Central America. Arboreal in its nature, this wandering spider is found living among the trees and bushes in its native range. Without a web to capture prey, this spider relies on its deadly venom to hunt and capture its prey. More importantly, without a web, females, who are much larger than the males, don’t have a permanent home to help attract in potential mates. This problem is solved with two evolutionary inventions. The first, quite common within the insect world, is the use of pheromones that will draw in the smaller males from the surrounding canopy. A single slender thread of silk is released along a tree trunk, and as the thread is released, the female impregnates the silk with its delicious perfume. While this trick certainly draws in the wandering mate, it is the second bit of courtship that will become apparent on our safari.

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31.1  Going Bananas Nocturnal organisms possess some of the most interesting adaptations to their sensory systems simply because light is such a powerful and informative cue. One of the more interesting aspects of sensory biology is how different animals have evolved mechanisms to cope with the lack of light. We are so dependent upon our vision that living in a world without light becomes a strange and alien concept. I would imagine that if humans didn’t possess eyes, our fascination with visual creatures would be significantly increased. The wandering spider does its mating dance at night and in the canopy of the forest, so visual signals provide very little help in the search for a female among the banana trees of Honduras. Much of the scientific work on the wandering spiders is done with an amazing piece of technology called a laser Doppler vibrometer. This machine shoots a laser beam at a surface and is able to measure and quantify the minute vibratory signals traveling through that surface. The wandering spider often generates its call on banana leaves, which are quite big. The leaves can grow longer than 2 m in length and over half a meter in width. The body of the male wandering spider is around the size of a quarter although the legs extend about three times that distance out from the body. The females are around 50% larger than the males with equally large legs. Even at these sizes, the vibrations they are capable of producing in the plant material are rather small. Despite the diminished vibrations, they are still strong enough for the animals to detect. The male wandering tiger spider searches the leaves of the canopy by simply walking around. There is little evidence that these animals are long-distance searchers like the male moths. The females do use pheromones which help draw the males to their vicinity. Unlike the moths, the pheromones are contact chemical signals, and the females use signal strands of silk, covered in pheromone, attached to the banana leaves as their calling cards. Females locate themselves on the large and long banana leaves in the canopy of the forest with the silk threads extending outward from their position. The females, after laying down a silk thread on the trunk and leaves, will settle down on a single leaf and wait patiently for her suitors to come calling. The length and size of the leaves are perfect substrates for the spider’s mode of communication (this will be explained later). The males will follow the silken thread and will cautiously approach the female from another leaf. The males search the leaves for these strands and are seen to periodically stop in their search patterns. During the stops, the males are smelling the surrounding leaves for any pheromone silks. Even during these initial searching stages, the males perform this part of the mating ritual with delicate care. If the right behaviors are performed by the male and the female is convinced of his quality, the consumption occurs after the mating. If the wrong behaviors are exhibited, then the male serves as a meal rather than a suitor. Once the male has located the female’s tree, the male spider will switch from an olfactory search to a mating dance dominated by his drumming. The male spider will place his legs on the leaf and move them rapidly up and down while remaining in contact with the leaf. Unlike the drumming of our fingers

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on a table, the legs remain in contact with the leaf as he is attempting to create a small-scale motion within the leaf as a whole. This is similar to the water striders presented in an earlier chapter. By performing these behaviors, the male spider produces a series of rapid pulses of vibration that are transmitted through this single leaf, across the trunk, and out to the other leaves of the tree. Each pulse itself, which can be visualized by the laser Doppler, is quite short, less than half a second, and he’ll repeat this over and over again for several seconds. Then he stops, and using the same legs that created the vibrational signal, he’ll wait for response from his potential mate. If the male signals are to her liking, the female will respond. She’ll perform her own set of undulations which will cause the leaves to vibrate. The male, who hasn’t moved since his signal was sent, will feel the waves move across his leaf. When he does, he’ll rotate his body in alignment with the female’s direction. The waves provide the male with directional information on the exact location of the female. Since the female is located on this plant, but on different leaf, his job is now to locate her position among the many leaves. To perform this spatial task, he’ll use these vibrations to continue communicating with her. The sets of vibrations, first by the male and then the female, give the male just enough information to track her position by following the increasing intensity of the waves. Once that direction is determined, the male moves toward the female by feeling the vibrations with sensors in his legs. Moving in the direction of the stronger vibrations, he uses the increasing intensity of the vibrations to determine whether he is getting closer or to make small-scale corrections in his approach. Stopping to send further signals, the male uses this back and forth wave generation to both locate the female as well as announce his intentions to mate. The female has very short responses to his signal, so he has to repeatedly respond to her calls and keep the signals coming toward him. This back and forth between the male and female allows the male to make his way across leaves and branches to the female’s location. Her vibrational responses to the male’s signals are used as guides as well as interpreted as her willingness to mate. If she accepts him as a mate, the communications will continue until they meet. The plant’s leaves serve as the medium for the message, and that message is a mating dance that will end in reproduction.

31.2  The Science of the Vibrating Leaves A life led walking along the forest floor or living among its leaves and branches is a world full of vibrations. Small leaves and blades of grass have excellent mechanical properties that will carry these vibrations incredible distances, at least incredible distances when compared to the scale at which these organisms live. For the wandering spiders, mating signals can travel distances close to a meter through the plants. While not quite far for us, this distance is far enough to determine the direction to the nearest mate. After about a meter or so, the signals decay to a point that

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they are undetectable for the spiders. This process by which a signal decays with distance is called attenuation. As I write this chapter, I am sitting at a small table in the student union of my home university. A chance to get away from the potential distractions in my office, the union provides a relatively quiet place to think about my writing. An interesting side consequence of choosing this location is that the size of the table is smaller than my desk and has a central pedestal that supports the table top. This physical arrangement causes the table to vibrate ever so slightly as I strike the keyboard. Given the uniform properties of the table top, the signal travels fairly homogeneously throughout the table top and is attenuated equally in all directions from the source of the tapping. It is a miniature version of the wandering spider communicating on a banana leaf. For wandering spiders that create signals on the leaves of plants, the attenuation of the wave is not equal in all dimensions. The leaves have veins, lamina, and a petiole that all have different thicknesses and densities. On top of these differences, signals traveling to leaves on the opposite side of the plant have to move through the more woody elements of the plant. These material properties of the plant determine the rate of attenuation of the spider’s vibratory signals. As a result of the differences between the leaf and trunk, signals propagating across the plant are attenuated faster than signals within a single leaf. Thus, environmental conditions can alter these animals’ signals. For example, the spider’s leaf situation is similar to calling to a friend at one end of a long hallway. The sound bounces off the denser walls and propagates down the air in the middle of the hall. Without the walls, your voice would travel outward in all directions, but in the hallway, the walls channel your voice toward your friend (Fig. 31.1). Fig. 31.1 Communicating across plants. The smaller male wandering tiger spider will communicate to the larger and deadlier female spider his intentions to mate. This love signal is initiated on different parts of a plant, and the signal travels down one leaf, through the trunk, and onto the leaf with the female

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Coupled with these environmental differences, the spiders can create two distinct types of signals that serve to modulate the “syllables” in those signals. The first signal, mentioned in the safari above, is called opisthosomal signals because these signals are generated by quickly vibrating the hind end of the spider called the opisthosoma. One of the distinctions between insects and spiders is their body construction. Insects have three body segments (head, thorax, and abdomen), whereas spiders only have two (cephalothorax and opisthosoma). Thus, this first signal is created by bouncing the hind end up and down to produce similar vibrations in the underlying leaves. These signals can be modulated to create differently timed vibrations (which are referred to as syllables). The opisthosomal signals are the ones to alert the female that the male is present on the same plant. The second signal is akin to drumming your fingers on the table and scratching your fingernails along the table top. These signals are called pedipalpal signals and are produced by drumming or scraping the pedipalp (or parts of their jaw) against the leaves. The ability to generate two different types of vibratory signals on top of the various attenuation properties of the surrounding leaves creates a rich and complex array of signals for both the males and females to detect and use for mating. Yet, the ability to produce a symphony of vibrations goes to waste without an equally complex mechanism to sense and decode these signals. In previous sections, including the head-banging moles and water striders, vibrations were detected with relatively simple mechanisms such as the measuring of leg movements in response to surface waves. The wandering spiders have a more complex detection system that is comprised of two very different and yet equally elegant mechanisms to sense their oscillating world. The first of these mechanisms is a common evolutionary strategy for the detection of particle movement, vibration-sensitive hairs. These hairs are located on the last segment of the legs of the spider. Arthropods, which include spiders, are segmented organisms, and the legs of spiders are prime examples of this segmentation. The last segment, or foot, is called the tarsus, and the segment right behind the tarsus is the metatarsus. The vibration-sensitive hairs are located between these two segments with the base of the hair embedded in the metatarsus. This connection point is a prime location as the tips of the hairs reach out and touch the tarsus of the spider. As the foot moves up and down in motion with the leaves of the banana tree, the angle between the tarsus and metatarsus changes, and these hairs are contacted. As the hairs are bend, the underlying neurons fire and send information to the brain of the spider. As the vibratory signal increases in intensity, the upward motion of the leaf, and the tarsus, also increases, which subsequently increases the deflection and stimulation of these hairs. In a similar fashion, as the frequency of the vibration changes, this change is transmitted to these receptor hairs and is encoded as a train of action potentials sent to the brain. The second way in which these spiders sense vibrations is through something called a slit sensilla. This particular sensilla is called the metatarsal lyriform organ. This organ looks like an upside-down slice of tangerine. The surface of the organ contains around ten small slits, and each slit is innervated by a single sensory cell. This organ, like the previous hairs, is also located at the joint between the tarsus and

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metatarsus. If a vibratory signal travels through the leaves of the tree and reaches the legs of the spider, the tarsus and metatarsus move in response to those vibrations, as described above. The metatarsal lyriform organ, due to its key location, is deformed by the differential movement of the tarsus and metatarsus. For example, some people have a tendency to bounce their legs when sitting, possibly as a result of nervous energy. This bouncing creates differential movements in the foot and leg that occurs right at the ankle joint. This is similar to the movement detected by this slit sensilla. As the tarsus is moved, the sensilla are deformed. Each of the slender slits is stretched by the bouncing movement which activates the neurons connected to the sensilla. The magnitude of the stretching deformation is in relation to the magnitude of the vibrations in the leaves of the tree. Thus, the neurons of this organ can encode the vibrations of leaves and send this signal on to the brain of the spider. As the spider, either the male or female, detects these vibrations, response signals are generated and sent out to the potential mating partner. The male uses the intensity differences across his legs to determine the direction of the female. If the right legs move more intensely than the left, the female is on the male’s right. Both the female and male spiders use the intensity and frequency of the vibrations to assess the mating quality of the other signaler. While it is true that particle movement or vibration is a way to describe sound, these spiders aren’t using acoustical signals to communicate their desires. Their desires for mating are literally carried by the ground beneath their feet, although in this case the ground is the leaves of the trees. In this world, the males have to have the right dance moves in order to mate.

Chapter 32

The Sensible Reverberations

Shoes have long been an essential accessory for human beings. The earliest known shoes date back around 10,000 years ago, but most likely the connection between our feet and protective coverings dates back much farther. Initially, shoes were plant material such as bark or hemp rope, but as crafting techniques increased in complexity, these materials gave way to wood and leather. Even with the increased sophistication of craftsmanship, some cultures preferred to travel barefoot and only wore shoes during ceremonial occasions. Although shoes protect our feet from injury, wetness, and cold, they also deaden our ability to remain in contact with the earth. It is this contact that enables many other creatures to sense their vibratory world. Even when we travel barefoot on beaches, in our backyard, or even in our homes, we are ignorant of the subtle vibrations that surround us. The rich world of tactile communication envelopes our feet and hands, and yet, the signals pass us by without even a hint of recognition. As I write in my office, often with the door closed, I am often visited by my graduate students who have questions about their classes or research. I can usually tell who is approaching my door because each student has a distinctive pace and intensity of their footfalls. I can label some of them as heavy walkers, while others are quite light afoot. Still, all of these detection abilities use my hearing, and if I am listening to music, this ability disappears as their steps are masked by the music. If I could view the world the way that many of the animals described in this section can, I could still determine who would be knocking on my door even with my music blasting away. Imagine the ability to lightly touch the trunk of a tree and determine how many birds and squirrels are sitting in its branches or how many insects are crawling beneath its barky surface. The ability to walk through a building and by focusing on the vibrations in your toes being able to tell who is present within the structure would be incredible. The auto mechanic who could simply lay their hands on your car and determine what ills lie in its engine would be rich indeed. These sensations are as musical as the mating calls of birds or the melodious songs of whales. The

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ability to sense the subtle fluctuations in the physical structures in our world is literally the ability to detect the pulse of nature. This is the world of spiders, water insects, and underground mammals. The pluck of a thin strand of a web could signal a potential mate or with a different frequency a hearty meal. Each step by a small insect, buried deep inside of a tree, sends cues to those birds seeking a lunch. The drumming of wolf spiders on a forest floor creates a physical melody that calls to females and advertises the worthiness of the drummer. Walking through their habitats, we are bulls in a china shop as our clumsy steps and heavy strides create a chaotic landscape upon which these animals attempt to communicate. What a wondrous adventure it would be to spend a day being aware of their world. To step through a forest or beach and to feel the faint signals would expose an environment full of life that would rival any inner city. Sadly, we are oblivious to these signals. Recent research on the effects of sound pollution have indicated that birds located near roads or cities have changed their songs structure and intensities as a result of the increases traffic noise. This effect occurs even in more rural settings if there is enough traffic on a road. Birds are not the only animals negatively impacted by noise pollution. Despite this knowledge on sensory pollution, there is absolutely no work on similar consequences for animals that use vibratory communication. Within larger cities, the constant presence of trains, large semitrucks, construction, and background traffic has to create a cacophony of vibrations that would make even the simplest of communications impossible. During my travels in these cities, I can feel the vibrations in my feet despite the cushioning in my shoes. I fear that our literal insensitivity to this illusive world will allow us to further degrade the vibratory world of many different animals. These animals are in many ways a unique combination of master musicians and expert engineers. They have innate knowledge of the physical properties of their environment in which they create or detect vibrations. These environments can range from the hard-packed walls of their subterranean tunnels, the fluctuating surface of a shallow pond, or the tiny tendrils of a silken thread. By modulating the intensity of their movements, these organisms can “play” their environments with as much virtuosity as the greatest classical guitarists. They could offer a master class that would truly enlighten.

Part VII

Other Senses

Owing to some peculiarity in my nervous system, I have perception of some things, which no one else has. —Ada Lovelace

Chapter 33

The Diverse World

Traveling the sidewalks of a busy city allows us to perceive a wide and diverse set of stimuli that many would consider to be the real world. The sounds of cars and trucks whooshing by us are mixed with the loud din of construction zones and the conversations of our fellow travelers. If we focus our visual attention on the people around us, the wide diversity of facial features, hairstyles, and clothing choices present us a cornucopia of patterns, textures, and colors. Our noses will sample the various aromas emanating from restaurants, street carts, exhaust fumes, and other odors arising from the underneath the city. This is a rich and complex environment that is often called the sensory landscape. Vision, audition, smell, taste, and touch, these are the five senses we commonly speak about when we experience the sensory landscape. These senses are accomplished with our eyes, ears, nose, tongue, and hands, and we often think these five define the limits of perception. All the preceding sections of this book have focused on these senses albeit with different animals and their unique ways of interacting with the world. We move through this landscape often guided by our five senses. As taught in grade school, our eyes, ears, nose, tongue, and hands represent the primary organs by which we see, hear, smell, taste, and feel our way around our world. The main theme running through this book is the erroneous thought that five abilities provide us a complete and accurate umwelt of the reality. Certainly, these five senses have allowed us to navigate the complex and varied worlds of our evolutionary history, so they perform a good enough job to survive. In the same spirit as the diverse abilities of animals, our grade school teaching of the five human senses isn’t quite right and isn’t as straight forward as it is usually presented. Senses serve an important purpose. That purpose is the ability to extract relevant information from all the different stimulus energies present in the sensory landscape. Some of those energies are noise, such as the background conversations occurring in a coffee shop. Other elements of the sensory landscape are critical pieces of information. For example, our acute ability to smell and taste can determine if our food has spoiled and our hearing warns us of approaching danger. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_33

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Evolution has worked to shape our ability to detect these important signals above the noise because these exact signals serve some survival function. We don’t see like an osprey or owl because the lack of this ability hasn’t been detrimental to our ancestor’s survival. Evolution has tuned our senses to those elements of the sensory landscape that are most important for us. This is the singular reason that there is a difference between the sensuous and illusive world. The extension from this basic concept is that animals with different survival needs will perceive the sensory landscape in widely diverse fashions. Predators have different sensory abilities than prey. Aquatic animals have contrasting sensory capabilities compared to terrestrial animals. There are even sensory differences between large and small animals. High-speed crashes are far more detrimental to elephants than they are to flies. Thus, their visual systems are designed to detect and extract differences in the visual world. If animals have different sensory worlds, what stimuli exist beyond the classical five senses that humans have? Part of the answer to this question lies in the physical world that encompasses animals. The ocean comprises approximately 70% of the earth’s surface, and given the depth of the oceans, greater than 90% of all livable habitats is likely aquatic. This large aquatic habitat is often quite featureless, at least in the visual, auditory, or even chemical senses. In coastal zones or shallow lakes, light can penetrate to the bottom of the habitat, but this penetration is usually limited to the first 200 m of depth. The average depth of the ocean is around 4000 m, and the average depth of the Great Lakes is around 150 m. So much of the habitat is unlit. Even in those habitats that are shallow, light is often limited by sediments, algae, or other particles in the water. Without light, animals have developed the ability to navigate, forage, and even communicate using magnetic and electrical stimuli. These stimuli and their interesting properties can allow animals to navigate thousands of kilometers to small islands located in the middle of the south Atlantic or detect the presence of potential prey underneath layers of sand and silt. Fortunately for us, electrical signals don’t move through the air as easily as water. If they did, every single power outlet would be a deadly addition to any home. One signal that does travel fairly well in aerial environments is heat waves. Most living things produce heat as a consequence of muscle movement, heart beats, and food metabolism. The detection of heat sources in terrestrial environments is often associated with predator-prey interactions. Because of the extremely high capacity of water, heat doesn’t travel very far in lakes or oceans and isn’t usually used as a stimulus in these environments. Thus, heat, magnetic, and electrical senses are some of the senses that extend many animals’ abilities to perceive the world beyond what humans can. This list is certainly not exhaustive though. Many different animals have the ability to sense gravity and acceleration (motion). Humans have this ability too, but it is often overlooked as a sense. The long lines for roller coasters at amusement parks are a testament to our ability to detect gravity and acceleration as well as derive pleasure from this sense. Animals display additional abilities to use pressure waves and current velocities in air and water as sources of information, communication, and with pressure, as sources of weapons.

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These stimuli and their associated senses can be considered relatively more rare than the more famous classical five outlined previously. Their use among animals is considerably more uncommon, and even when found, these senses often have a very specific and detailed role for the animal. Because these stimuli are far further hidden from our consciousness, it is worth a small delay in our next series of safaris to explain what these stimuli are and how they move through the sensory landscape.

33.1  Magnetic Fields Earth has a large magnetic field that encompasses the entire globe. As with any magnetic field, there is a north and a south magnetic pole which reside fairly close to the globe’s geographic north and south poles. There are three distinctive aspects about the earth’s magnetic field that make it particularly useful for largescale movement. First, there is a polarity, and as such, animals with magnetic senses can distinguish north from south. Second, the intensity of the magnetic field is strongest at the poles and decreases in a predictable fashion toward the equator but also has some variation across the globe. The smooth and predictable drop in the field strength allows animals to determine where they are along a latitudinal gradient. Finally, there is an aspect called the angle of inclination. The earth’s magnetic pole emerges from the earth at the south pole and returns at the north pole. In between these two points, the field exists as a giant arc connecting these two points. The angle of inclination refers to the relative angle between this arc and the earth’s surface. At the north pole, the magnetic field is perpendicular to the earth’s surface so that the angle of inclination is 90° and is pointing downward. The same situation exists at the south pole where the angle is also 90°, but here the force is pointing skyward. At the equator, the magnetic field is parallel to the earth’s surface, and the angle is 0°. As with the field strength, animals traveling through different latitudes can sense different angles of inclination. The global scale of the magnetic field and changes in that field make it an ideal cue for large-scale migration and movement.

33.2  Infrared Energy Infrared is a more appropriate name for the heat signals that some animals use to hunt. Using the term infrared places this stimulus, correctly, along the electromagnetic spectrum which contains visible light, microwaves, X-rays, as well as magnetism. Usually, the stimulus properties of this spectrum are denoted by the wavelength of the energy under discussion. Visible light, at least visible to humans, is defined as those energies that have a wavelength of 400–700 nm. Blue light is shorter wavelength light and is location at the 400 nm range, whereas red light is at the other end

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of the spectrum. A wavelength is the distance between two successive crests of a wave, and nanometer refers to one millionth of a millimeter. So, these are incredibly short distances. Infrared radiation lies just a bit past red light on the spectrum. As mentioned previously, living organisms generate heat and often have an elevated body temperature compared to the background temperatures. This is even true of the so-called cold-blooded organisms. As a side note, this term is antiquated and actually quite inappropriate. Some cold-blooded organisms can have body temperatures above those of warm-blooded animals. The more important distinction is not temperature per se but the variation of the temperature and the control of that temperature. Warm-blooded organisms have a more consistent temperature which is generated internally, whereas a large number of cold-blooded organisms have a highly variable body temperature that is determined by the surrounding environment. Infrared radiation gets absorbed rather quickly by the environment. This absorption is even quicker in aquatic habitats than terrestrial, so this sense is often used at very close distances.

33.3  Electrical Signals Electricity is even more ubiquitous among life than infrared radiation. Every beat of a heart, every muscle contraction, and every neuron that fires generates an electrical signal. While it may be easy for animals to produce visual camouflage or to move stealthily through their environments, they cannot mask or hide their electrical signals. Electricity means life and predators have evolved mechanisms to take advantage of this very fact. Yet, air is a really poor conductor of electricity, so animals only use these senses within aquatic or very moist environments. In addition, there are two types of electrical signals and electrical senses. One sense is called passive electroreception. In this mode, animals simply detect signals that exist in the world around them. The classical example of this ability exists in sharks and rays that use their electrical sense during hunting. This type of electroreception is not used in communication. The second mode is called active electroreception that functions similarly with bat sonar. In active echolocation, bats create a signal and use the echo (and its distortion) to sense their world. Electroreception works in a similar fashion in that animals create electrical fields and measure its distortion to sense the world around them. This mode can even be used for communication in a special group of fish, but this will be explained later. Electricity is similar to the magnetism in that the signals exist as fields. In addition, electrical fields have poles, but instead of north and south, there are positive and negative poles. The field flows from the positive to negative poles and also creates an arc around the source of the signal. Similar to the magnetic field, intensity and angles of inclination change in a predictable fashion along the body of an organism as well as with distance away from the organism producing the electrical field. For those animals using active electroreception, distortion of this orderly field allows them to identify objects in their environment.

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33.4  A Rose by Any Other Name Scientists love to play the naming game. Those in the field of systematics use various techniques to identify and name the different species that inhabit this planet. When new techniques evolve (such as molecular tools), the names and relationships of species often get revamped and redefined. Scientists invent names for both tangible and intangible objects (such vitreous humor for the fluid inside your eye or meme for the thought that you can’t get rid of), concepts (Occam’s razor), and even the small bits of organisms (the triangular fossa is the part of your ear under the ridge that covers the top of your ear). This focus on naming is sometimes important as clarity and precision are two key elements within the scientific discipline. Yet, underlying this appearance of precision is often a level of confusion and gray areas. The naming of the wide variety and diversity of animal senses is a gray area. For humans, the distinction between smell and taste appears straightforward. Smell or olfaction occurs within the nose, and taste or gustation occurs within the mouth via our tongue. Despite the fact that both of these senses are designed to interact with chemicals, olfaction is used for distant chemical, whereas gustation occurs when these chemicals come into contact with the tongue. Furthermore, olfaction is carried by bipolar neurons that generate action potentials, whereas gustation is produced by cells in taste buds that are not bipolar or are capable of generating action potentials. All of this seems quite clear, but complications exist upon further examination. Our sense of taste, or at least the enjoyment we receive during meals, is primarily constructed off of smells than tastes. In addition, we have an extensive set of chemical sensors within our body that send critical information to our brain. These sensors perform vital functions such as detecting the level of CO2 in our lungs, lactic acid in our legs, and sugar in our stomach. These sensors help determine our mood and motivations and are as important to our survival as our nose and tongue. Throughout our skin lies an extensive network of chemoreceptors that detect noxious chemicals. If you lick the wrapping from a piece of cinnamon gum and place it against your forehead or underside of your forearm, you can “taste” the cinnamon. The CO2 in carbonated drinks is also detected by this same system. Both of these chemical sensory systems are not placed within the five senses. Anyone who has ridden a roller coaster certainly knows that we have an exquisite ability to detect acceleration in three different dimensions. These signals are detected by a special organ in our inner ear and is called the vestibular system. The actual sensory cell that lies at the heart of this ability is identical to the hair cells that allow us to hear sounds, but we don’t call this system hearing. A large part of this confusion is due to the different perspectives that scientists take to study the senses. If one approaches sensory biology from a physical point of view, there are really only three senses, those that detect chemicals, mechanical, or something along the electromagnetic spectrum (which would include heat, light, electricity, and magnetism). In this classification system, smell, taste, trigeminal (hot peppers), CO2 receptors in our bodies, and hosts of other sensors are the same sense, but with different

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physical designs. Similarly, the lateral line system of fish, our hearing and touch, and the ability to detect accelerations all fall under the same heading. Using this system feels unsatisfying based on the many different ways that animals sense the world and use that information to make decisions. A more neurological approach would classify the senses either by the neuroarchitecture of the sensory cell or where in the brain of animals the signal is processed. This approach, as with all of them, is not very clean given the vastly different “brain” structures of vertebrates and invertebrates as well as leaving out plants, fungi, and microbes as organisms with sensory capabilities. A broader approach, one of behavior or sensory ecology, would apply a classification system based on how the animal uses the sense. Is the nose used for social behaviors or foraging? It could be argued that this is ultimately what evolutionary forces act upon for the design of senses, but even this type of classification system combines senses and sensory structures (the taste buds on the bodies of catfish, our tongues, and the hairy walking legs of crustaceans) that appear quite disparate. Here I will advocate an integrative approach that crosses field disciplines (physics, neuroscience, biology, and ecology). While this cross-disciplinary thinking is difficult and muddy to say the least, the broader approach enables different senses to be combined or split based on the necessity at hand. If we are interested in the ecological aspects of a sense, we can distinguish them by purpose or use. A more small-scale approach might be to focus on the structures that give rise to information used by animals, and finally, the transformation of stimuli from one type of energy (magnetic) to a more biological type of energy (electrical signals of action potentials) might be more fruitful. In the spirit of this integrative approach, this section covers the more rare type of senses and their unique uses by animals in their environments. Some of these senses (magnetism) are found quite broadly across the tree of life, whereas others, electrical senses, are narrowly focused on a few select species. With all of this out of the way, it is now time to dive deep into sensory worlds that are not commonly visited.

Chapter 34

The Pull of Home

One of the great pleasures of teaching field courses for students is the ability to travel and explore new habitats. Since my training lies in the aquatic realm, my field courses involve the exploration of the wide diversity of aquatic habitats. These can include the more familiar coral reefs, streams, and rivers but also bogs, fens, and marshes. Given their relative accessibility, most of these habitats are close to a shoreline and shallow in depth. The exploration of the open ocean or even some of the world’s large lakes is often difficult to perform for undergraduate or even graduate courses. It is not too much of a stretch to say that science knows more about the solar system than the ecology and biology of the deep ocean and large lakes. Still, opportunities to take students to these unexplored habitats are available if the right connections can be developed. One such opportunity arose for me when I became aware of an organization called the Inland Seas Education located in Suttons Bay, Michigan. An outstanding organization dedicated to the freshwater education of tomorrow’s citizens, Inland Seas operates a beautiful two-masted schooner that sails around Lake Michigan and Lake Huron with students of all ages. The boat is equipped to perform modern limnology (the study of lakes) and has an excellent crew trained to provide a learning environment for many different levels of students. One year, I had a group of eight students taking a week-long large lake limnology course that entailed a 3-day cruise aboard the Inland Sea’s ship called the Inland Seas. We set sail out of Petoskey, Michigan, which is located on the eastern coast of Lake Michigan. Most of the students hadn’t been on a larger boat or spent a lot of time on the Great Lakes, so they were all excited to get out into the open portion of the lake. Although the weather wasn’t particularly cooperative, we did manage to leave port and head out to open waters. Given the choppy nature of the water, the captain decided to stay within sight of land where water was a little bit calmer than the middle of the lake. Despite this choice, the boat was rocking back and forth at a pretty good rate which made the initial day a bit rough for those susceptible to motion sickness.

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When the lake finally calmed down, the captain decided to turn the boat away from shore and really head toward the deeper part of the lake. As we sailed away from shore, I watched the student’s reactions as the distant land faded from view. As the last bit of land disappeared beneath the horizon, many of the student’s became a little disoriented. A subtle, yet important, aspect of our interpretation of the world is driven by the combination of the detection of up and down by our inner ear and the visual perception of a horizon. Since our evolutionary ancestors evolved on land, the omnipresent horizon has been an excellent source of information about the vertical orientation of our world. Our reliance on this horizon is so important that “natural” illusions can occur like several geographic locations where cars appear to spontaneously role uphill. These spots are called gravity hills, and there are numerous locations across the globe where the eerie phenomenon of the car rolling uphill occurs. In Ayrshire, Scotland, a gravity hill named Electric Brae often throws visitors, and some locals, for a loop. Cyclists and cars appear to coast uphill, but those attempting to go downhill need a little gas or extra effort on the pedals of their bike. Although it might be a nice fantasy to think that magic is occurring at these spots, what really is happening is a conflict between the reality of up and down and the visual perception of the up and down as gathered from a horizon. At Electric Brae, the surrounding landscape creates an apparent downward line based on the trees and exposed geology of the hillside. Our eyes will use that visual line to determine what we think is the neutral or flat horizon. The road rises about 5 m over a length of 440 m, while the visual landscape drops several meters, and an illusion is created. The power of the visual horizon overrides any real perception of up and down. Although there is no gravity hill out at sea, the horizon can be quite misleading. This can be especially true when, in high waves, the horizon is above you at one moment in time and all you see is a wall of water in front of you. In the next instant, the boat rides up toward the crest of the next wave and all you see is sky. Thus, the students on this voyage were struggling with their vertical orientation. Even when the lake calmed down later than afternoon, an uneasy calm among the students was apparent. As explained previously, we use the horizon for a sense of verticality, but we also use objects in the horizon to orient ourselves. A distant hill, a clump of trees, or a skyscraper can signal a compass direction. We use these visual landmarks to help orient ourselves as we move through our different environments (home, city, or nature). Yet, out in the middle of Lake Michigan, there was no visual landmark that could provide the students with some sense of direction. My students would occasionally spin around in a circle trying to catch a glimpse of something that could be used as spatial landmarks. These landmarks can function as spatial anchors or points of reference during movement and provide some sense of calm. Sailing through open waters provides little landmarks to navigate. Certainly, the trained sailors can use the stars at night, and, during the day, the sun’s position in the sky can give a sense of each of the four compass points. Thankfully for our trip, we had a well-seasoned captain, and in addition to his exceptional navigational abilities, we had communication systems that provided us with a map and our precise location which was gathered by communication with orbiting satellites. While we cannot see the land with our eyes, the map clearly

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shows the boat’s location on a map of Lake Michigan. In addition, a set of coordinates (either latitude/longitude or universal transverse Mercator) is also displayed and creates a unique set of numbers that is tied to a singular global position. Once we know that global position (and the position of our destination), we can sail the boat toward our port regardless of the missing horizon. Although these modern techniques have certainly simplified the lives of sailors, humans have been navigating the globe for centuries without the use of electronics and satellite systems. The stories on how ancient sailors determined position, direction, and horizon are interesting in their own right but are beyond the scope of this book. Yet, there are even more ancient “sailors” who have been navigating the world’s seas for far longer without any sort of global positioning system. Whales, dolphins, and sea turtles are just a few organisms who take great migratory trips spanning oceans which appear to be quite featureless to us. The two champions among all of these creatures are the loggerhead and the green sea turtle. These large reptiles travel the vast distances across oceans from birth to sexual maturity. Most of that journey takes place in the open ocean. In America, loggerheads, Caretta caretta, begin their journey in the soft sandy beaches of Florida as hatchlings. These hatchlings make their way from the underground nests to the ocean shore by crawling along the sandy beach. After finishing this arduous path and finding the ocean, the young turtles dive into the water and begin a 20–30 year swim in the ocean to feed, grow, and mature. Loggerheads are voracious predators of arthropods (crabs and horseshoe crabs) and mollusks (whelks and conchs) and can grow to more than a meter in length and 150 kg in mass. Once they mature and mate, the females perform an amazing act of homing prowess. Without the aid of a Google maps or star charts, these females make their way from the North African side of the Atlantic Ocean to lay eggs on the very same beach where they were born two decades previously. Some more recent work has shown that these turtles are so accurate that they will lay eggs within 80 km of their natal beach. The scale and accuracy of this homing act is almost unimaginable. The adults can be found as much as 5000 km away from their Florida beaches which makes the total journey of the hatchling to adult around 10,000 km. With no landmarks or visual markers guiding their journey, they’ll return to their home beach with an error of no more than 1% of their total journey after 20 years. I have trouble locating my car keys in my house after setting them down an hour earlier. If I waited 20 years to search for those keys, I would never drive again. I described both my students’ journey to the middle of Lake Michigan and the sea turtle’s journey to the vast reaches of the ocean as forays into a featureless environment. Certainly, as theme of this book should be apparent by now, this statement isn’t entirely true. Our navigational mechanisms are based on visual cues such as shorelines, landmarks, or positions on maps. For the turtles, their visual landscapes are rather bleak, but another sensory landscape produces a map that is a clear as any sea chart. Their map relies on the magnetic field generated by the earth. Years of dedicated research have determined that sea turtles can use different features of the earth’s magnetic field to traverse the open ocean and return to their natal beaches. To gather this information, scientists have to control and manipulate something as

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large as the earth’s magnetic field which makes for challenging experiments. Often, researchers will build large magnetic coils that allow them to flip or alter a small local magnetic field. As they flip the magnetic field, they monitor the turtles’ swimming behavior. Decades of excellent research has demonstrated, without a doubt, that these massive creatures use these fields quite actively. This work has revealed that many other animals, from seabirds to small fruit flies, are also sensitive to magnetic fields. Thus, this ability is far more widespread in the animal kingdom than most of us think it is. Yet, despite the years of research and observation, the actual receptor for a magnetic field remains elusive. To see this ability in action, an undersea adventure is necessary. The loggerheads that we’ll be visiting are returning to the eastern beaches of Florida, so our travels take us to the Atlantic Ocean off the coast of this state. Large groups of loggerheads can be seen making their slow but deliberate way toward the coast. Each of them is ready to lay their eggs in hopes of producing the next generation of turtles. As the females approach land, the pull of the magnetic field will guide them safely to the beach they left decades earlier. Swimming beneath the waves, the animals have very limited visual cues to pilot them to their natal beaches.

34.1  Guidance by an Invisible Hand The adult loggerhead turtles feed primarily on fish and invertebrates such as crabs and whelks. Although they start their life as small hatchlings on the beaches of countries on the western rim of the Atlantic and Pacific ocean, they quickly make their way to the ocean and are swept into the massive gyres that encircle both the Pacific and Atlantic oceans. The gyres are large currents that travel along the coastlines of both oceans and form a continuous circular current. The young turtles use these currents to take them to their feeding grounds in the middle of the ocean. After completing an entire trip around the ocean, the juveniles have reached the adult stage and are ready for their migrations back to the coastal beaches. We’ll begin this journey observing the elegant swimming of a female loggerhead making her way in the vast nothingness of the open ocean. In late May, the females make the long journey to sandy beaches to dig nests and lay eggs. The female we are observing feels the draw of her home beach as she gently swims through the water. She is currently heading due west and is swimming along with powerful strokes of her flippers as well as surfing along the current of the north Atlantic gyre. At the end of her journey, she’ll have traveled thousands of meters, and any assistance she can gather from the ocean’s natural currents will certainly save her energy. The ability to use these currents to her advantage has been called smart swimming. Our loggerhead knows her directions quite well, and when she encounters a current heading west (toward her natal beaches), she’ll passively drift along with the current. By enjoying the free ride, she’ll conserve energy. If she detects that the currents are moving her in any other direction (east, north, or south),

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she’ll actively swim to make progress toward home or swim vertically to find a more directionally friendly current. Currently, the loggerhead is enjoying a strong homeward flow and is passively drifting along with the occasional stroke or two. Her hind two legs don’t participate during her drifting, and the powerful strokes with her arms are really only keeping her on course. If we focus in on her head, we’ll notice that the animal barely moves it. Pointing straightforward, the head appears almost fixed relative to its body position. She has a periodic movement to the left or right, but even this motion is ever so slight. She is focused forward, and, for the long journey ahead, she is conversing as much of her energy as possible. So, the head and hind legs are relatively motionless. All around us, we see nothing by ocean. Just like my students on the boat, the lack of landmarks that denote up or down, west or east, can be literally disorienting. Observing the loggerhead, she appears unfazed by this lack of visual cues. A subtle change is taking place in the loggerhead now. Her swimming strokes are slowly increasing in frequency, and she is moving her head to the left and back to center again. It appears as if she is turning her body, although it is difficult to know in this featureless environment. Her right flipper is moving with slightly more force than her left, and she holds her head off center and tilted to the left. Diving slightly in this direction, the female loggerhead is searching for something. It is as if some unseen force is gently pushing the turtle off to the left. As the giant animal finishes its turn, both the front and hind legs are now moving in unison. The female has picked up her swimming rate and is now moving in a different direction than she was before. The previous bout of drifting must have been taking her off course. Having completed the turn, the female’s head is now back to its former position, centered along her body. All her appendages are being used to move her forward through the water but with equal intensity all around. So, the animal is back to moving in a straight line, and that line points directly to its natal beach. The subtle course correction has been completed, and the loggerhead is now in a section of ocean where she can no longer drift. Despite the need for swimming, the animal senses that it is making progress toward her birth place. Over the next couple of hours of watching, we’ll see the loggerhead performs this same pattern of behavior over and over again. The first indication that a turn is about to be initiated is the increased movement in the head. To the left or right and then back to center, the animal moves its head as if to sense directional cues. We can imagine that her head is like a compass. Moving her head back and forth is similar to turning a compass in one’s hand. For the compass, the needle stays pointing toward magnetic north. For the animal, a sense organ is drawn magnetically to a similar destination. Unlike our compass that turns freely in our hand while the needle stays locked in to north, the animal’s internal needle turns with its head. The animal’s needle is drawn back to its original direction, and the animal can sense that pull. By turning her head even more, the animal should be able to feel an increased need for the needle to right itself. So, it is possible that these head movements are the animal’s way of sensing its direction home.

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With thousands of kilometers ahead of her, it is time to leave the female loggerhead behind. The turtle will eventually make its way to the beach using a combination of drifting and swimming. All of the while, its behavior and direction is controlled by sensing directional changes using a planet-wide magnetic force. Turning its head, sensing direction, and aligning its swimming are just as natural to the loggerhead as walking down a sidewalk is to us.

34.2  The Science of Animal Magnetism Magnetic compasses, at least of the human variety, are an elegantly simple piece of technology, a simple slice of metal that is sensitive to magnetic fields and a pin to balance it on. Put these two things together and the piece of metal will spin and turn until it faces north. Even if lost deep in the woods, a simple compass can be made to show the way north. A needle can be magnetized by rubbing a small magnetic along in a single direction. After a couple of times, the needle will have a north and south pole. Place the needle on a small leaf and gently lay this down in a puddle of water. The leaf and needle will slowly align themselves along the earth’s magnetic pole. Animals don’t have access to even this simple technology, but those that are sensitive to the earth’s magnetic field have built their own compass. Organisms ranging from small bacteria up to the largest of reptiles and birds display the ability to detect and respond to magnetic stimuli. Despite the wealth of organisms that perform this ability, the exact cellular mechanism of magnetic reception remains elusive but surprisingly similar to the field compass described above. Within magnetic bacteria, magnetic compounds have been discovered within the cell, and the compounds occur in long chains. Magnetite is a mineral composed of three iron atoms and four oxygen atoms and attracted to magnets. The material is interesting because it can also become magnetic itself. It is also the most magnetic material found on the planet. Thus, it is a perfect candidate for the basis of an internal compass. The material found in organisms is called biogenic magnetite and is actually produced directly within the organism. The production of magnetite into long chains constructs a biological version of the compass needle. Making the chains long increases the forces on either end of the “needle,” and the production of a thin “needle” decreases the amount of magnetic field force necessary to move it. In the sensory ecology world, this means that thin, long chain of magnetite is exquisitely sensitive to subtle changes in the surrounding magnetic field. Within vertebrates, which include our homing loggerhead, these deposits of magnetite have been found most often within the olfactory epithelium. The nose of these organisms appears to be capable of sensing magnetic fields as well as olfactory landscapes. While all of the basic elements of a compass appear to be present, there still needs neural connections that would allow the organism to read the compass (Fig. 34.1). While there are plenty of neurons within this region of vertebrate noses, the exact mechanism of detection is still unknown. It is possible that changes in the relative position of the magnetite chain and the earth’s magnetic field slightly distort the

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Fig. 34.1 The loggerhead’s voyage. Traveling thousands of miles to feed, the loggerhead turtle finds its way home by using the earth’s magnetic field. Small-scale anomalies in the magnetic field, like deformations in nets, allow the turtle to faithfully return to the beach where it was born decades earlier

tissue around the magnetite. The neurons may detect this distort as a sort of pull. As the magnetite aligns with the earth’s magnetic field, the pull would decrease. Conversely, as the magnetite shifts its position, possibly by the turtle turning its head, the magnetic field exerts a force and causes a pull on the surrounding tissue. By monitoring the direction (up, down, left, and right) and intensity of the pull, the animal may be able to determine its location on the globe. Even with all the magnetic sensory capabilities, what information allows the loggerhead to navigate such large distances? For this answer, subtle details about the earth’s magnetic field need to be explored. On the larger scale, and briefly covered in the previous chapter, the earth has a massive magnetic field that originates at the south pole, travels along the earth’s surface, and disappears into the ground again at the north pole. The geographic north pole is different than the magnetic north pole called the north dip pole. The field creates field lines that appear as giant arcing magnetic force lines covering the entire globe. Given the size of the field and the field lines, it seems difficult that loggerheads are using these sources of information to locate a small piece of beachfront property. As the magnetic field travels along the surface of the ground, another piece of information is generated. This source of stimulation is called the angle of inclination. The field lines are perpendicular at the magnetic poles, so the angle of inclination is 90°. At the equator, the field lines are parallel with the earth, so the angle of inclination is 0°. This information can be further subdivided into the horizontal component of the field (that part of the force that is traveling parallel to the earth’s surface) and the vertical component of the field (that part that is traveling into the earth’s surface). Loggerhead turtles, by moving their heads, create the ability to sense these two components of the magnetic field, and these components change in a predictable fashion from equator to pole. As a final piece of information, the earth’s magnetic field is not consistent across the globe. As the field travels along the surface of the earth, the field interacts with the material components in the local geology. Regional, and even more localized,

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differences in substrates will cause local distortions in the magnetic field. Imagine the surface of a trampoline with a number of heavy rocks scattered across it. Rich deposits of iron or other magnetic metals will cause the field to be drawn in toward those deposits, like the depressed areas of the trampoline with rocks. Other nonmagnetic substrates would cause the field to be stretched out as the field moves around, rather than through, those deposits. It is possible that loggerhead turtles imprint to the subtle variations in the magnetic field of its natal beach in a similar way that the salmon imprint to the olfactory smell of their natal streams. The loggerhead turtles, as they travel the gyres of the great oceans, are guided on their journeys by a simple and thin chain of magnetic material buried within their noses. This needle is turned and pushed by the regional and global changes in the earth’s magnetic field as the turtle circumnavigates its ocean. The animal surfs these magnetic fields almost as surely as it surfs the currents deep within the ocean. The pull of the needle, coupled with a distant memory, safely guides it home, year after year, to faithful lay eggs on the beach where it was born.

Chapter 35

Warmth of the Season

The taming of fire was certainly one of the most significant technological leaps for humanity. The ability to cook food which improved the quality of meat by destroying parasites and bacteria led to a longer lifespan. Some plant-based food is fairly unpalatable until cooked, and fire increased the diversity of consumable food. Fire warmed our early shelters against the harsh elements of seasonal weather and expanded the territory in which humans could live. At night, after the sun has retreated, fire led to light which increased the sociality of the human culture. Thus, it isn’t too surprising that our fascination with fire still continues to this day. One of my greatest pleasures is sitting outside around a roaring fire on a slightly chilly night. This might be why the fall is my favorite season. The summer heat gives way to cooler air which requires a light jacket or wrap to keep warm. The long days of the summer begin to shorten, and the earlier start to darkness creates the need for a fire to provide light. The hectic carefree days are gone, and the heart of the academic season has taken over. Fall is the season of change, and, in an academic environment, that change is signaled by new students, new challenges, and new opportunities. All of these changes set the perfect stage for a night around fire with friends, a good mead, and meaningful conversation. During these nights, I noticed occasional periods of long silence during which everyone’s gaze is locked onto the fire. From a sensory perspective, the fire provides an excellent stimulus for almost all our senses. The dancing tongues of yellow and orange hues can entrance even the most jaded individual. The flames erupt and flicker as they rise from the base of the fire only to fade into the chilly night air. The chaotic motion and blending of colors is quite mesmerizing to our eyes. As the wood in the fire pit is heated, the wood is turned to water vapor and alcohol which in turns burns. If this gas trapped within the wood, the pressure exerts an outward force, and the wood is cracked or popped. Just as our eyes are captivated by the flames, the occasional crackling of a hearty fire tells us that warmth is there to be had. The aroma of a clean fire triggers powerful odor memories that flood our mind. Coupled with the visual show and auditory popping, the smells envelope us and enhance the moment in time. Although there isn’t © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_35

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really anything in this scene to stimulate our sense of taste, we can cheat a little and imagine that a marshmallow is turning golden brown at the end of a long stick. This toasted treat, when finished, will be placed between two squares of a graham cracker and chocolate. We actually add a subtle twist to this familiar treat and add a single juicy raspberry or a slice of banana between the warm marshmallow and piece of chocolate. Once the s’more is finished, our taste buds will come alive with the warm gooey sweetness. Thus, the eyes, nose, ears, and tongue are all provided with a delightful landscape in which to lose oneself. The sensory list above is missing the one sense tied to the original function of fire: warmth. As a breeze kicks up, standing closer to the fire certainly increases the feeling of heat arising off the flames. Stretching out your hands and dancing your fingers nearer the coals further increases the sensation of warmth. Depending on what you are wearing, the feeling of heat can be noticed in the arms, chest, and, particularly, the face. Taking a step back from the fire demonstrates how quickly the heat dissipates in the cold night air. Heat, or temperature, as a signal is really a close range stimulus. The ability of a substance to absorb and maintain heat is called the heat capacity. Although the heat capacity of air is relatively small compared to water, heat still doesn’t travel very far away from a fire. The heat capacity of water is over four times greater than air, and, as a consequence, water is exceptionally quick at absorbing or maintaining heat. Because of these physical limitations, the ability to sense heat is a rather localized ability. Humans sense temperature based in a variety of ways, and hot is sensed differently from cold. Here, the terms hot and cold and the ability to detect these temperatures are based on the human physiology. Warm receptors are sensitive to temperatures around 30–43 °C, whereas cold are sensitive to 15–30 °C.  These receptors provide information on our comfort and allow us to alter our clothing or our home’s thermostat. More intense cold or heat is actually sensed through different neuronal channels. These channels are tuned to pain and are generally termed noxious stimuli. These stimuli are sensed by a very general sensory system called nociception (or pain reception). So, it isn’t all that surprising that temperatures above 43 °C and below 15 °C are considered painful. Thus, standing too close to the fire will change the sensation from a comfortable warmth, mediated through the innocuous temperature sensor, to painful heat, mediated through the noxious heat sensors. Designed this way, our thermal receptors are essentially tied to protecting our body temperature and keeping us from thermal burns. This isn’t a very complex sensory system, and certainly the behavior evoked by this sensory information is relatively simple. This simplicity does exist in the animal kingdom, where organisms have evolved a complex set of sensory processes and behaviors to take advantage of thermal signals in the environment. Reptiles and insects have the ability to determine temperature signatures in order to sun themselves without getting burned. Vampire bats have thermal detectors surrounding their face that allows them to find blood vessels on their intended victims. The champion of thermal detection, though, has to be the pit vipers.

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Pit vipers are a group of venomous snakes found in the Americas, Europe, and Asia and are a subfamily of vipers. Most are nocturnal, ambush-style hunters that live across a wide variety of habitats. These two characteristics, nocturnal activity and ambush-style hunting, create the need to be able to detect the presence, approach, and even size of any prey that happen to be close to their location. Their moniker, pit vipers, arises from a heat-sensing organ or pit that is located between the nostril and eyes. This is used to hunt their prey which tend to be small mammals and birds, animals with high body temperatures which provide the vipers with the ability to detect heat signatures in their environment. Other snakes have pit organs, but these have evolved independently in some nonvenomous snakes like pythons and boas. On this safari, we’ll focus on the family of snakes in the pit vipers group and, specifically, on the beautifully named fer-de-lance viper, Bothrops asper.

35.1  In the Heat of the Night This viper is one of the larger vipers and can reach lengths of 2.5 m. Found in the southern part of Mexico to parts of Columbia, it is an abundant predator among the wet forests within this region. Highly venomous, the pit viper is quite dangerous to humans and accounts for a large number of health issues and death among the local inhabitants. Preferring the wetter regions of its range, the snake can be found near rivers, swamps, and moist agricultural areas. Like most vipers, it is an ambush predator and will attack almost any prey item small enough to be swallowed. The flattened head and brown coloration of the snake make it especially difficult to spot among the darken plants and substrate of the swampy areas of Costa Rica. This camouflage is important for its hunting style as any conspicuous coloration would surely provide warning cues to any potential prey. The diet of these animals changes as they mature, and the adults feed on mammals, birds, and amphibians but will occasionally consume fish. Luckily for our search, the viper has a small home range and a very high rate of site fidelity. This means that the animals return to the same spots within their home ranges. Working through the dense foliage, a large female fer-de-lance viper can be seen slithering up the bank of a river. As night falls, the female viper moves into a secluded spot among the leaves, some distance away from the river bank. As an ambush hunter, the female will sit and wait patiently for any small mammal that comes through the forest at night. Slowly, she coils her long and lithe body into a circle while leaving the portion of her body closest to her head shaped as an “S.” The characteristic shape is the ready position for a strike. If the snake is threatened or about to attack, this shape is a clear indicator to stay away. The animal can quickly straighten her body and strike with amazing and lethal speed. Once prepared, the fer-de-lance viper settles for a night of hunting. As the twilight gives way to the deep darkness of night, the visual landscape around our snake disappears. Completely cut off from the use of her eyes, the viper shifts its attention from visual cues to thermal cues. The surrounding forest and the

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animal’s own body are at lower temperature and do not create heat signatures. The lack of thermal cues provides an excellent backdrop for the snakes hunting method. The ability to detect signals doesn’t depend so much on the intensity of the signal itself. What really matters is the signal-to-noise between the stimulus (signal) and background environmental stimuli (noise). For example, a quiet voice is loud enough to have a conversation in an elevator. Despite the low volume of the signal, the noise of the environment is also quite low. Place that same quiet voice in a crowded train station and communication becomes impossible. For the pit viper, the thermal signatures of its prey are like those low voices in an elevator. In the heat of the day (like the crowded train station), the small mammals will be thermally invisible. Yet, here in the dark and cool forest, the thermal cue of the prey is as loud as a shout within an elevator. Even with leaves, twigs, and an uneven terrain, the pit viper has an excellent thermal view of its environment. As the animal patiently sits, small and distance spots of activity are detected. The nighttime world of this forest is dominated by mice and rats. As they emerge from their shelters, they scurry about attempting to find tempting morsels for their own consumption. Despite the mice’s excellent vision, the poor light conditions allow the viper to be hidden from the prey while the predator is quite aware of their activities. The numerous heat signatures move about within the forest, and the viper begins to take note of which images are moving toward it and which ones are out of range. Unlike more active hunters, the snake is performing a different style of tracking. Instead of moving through space and following a prey (like the kingsnake and its vomeronasal system), the pit viper is “watching” the small heat spots move within its thermal field of detection. As the spots move to and fro, the snake tracks their movements and focuses its attention of those heat signatures closer to it. As the mice disperse in the random directions, a single prey begins its movement toward the hidden predator. Running and stopping to search for food, a mouse slowly approaches the pit viper. Without moving its body, the female viper shifts its head to center the prey within its field of heat vision. She sits and waits. Despite the hunger and the desire to eat, she can sense that the prey is not quite where it needs to be for a successful strike. The prey is just a little ways outside of its strike zone. The thermal image of the mouse dances in front of her. The heat rising off the mouse mixes with the cold night air and creates an unsteady sensory image. The word image here is not to denote a visual field but refers to the spatial distribution of heat detected by the viper. While not as finely tuned as eyes, the pit organs do produce a sensory image of the thermal field in front of the animal. The mouse draws closer to the predator. The viper knows that the animal is getting close to striking distance, so the powerful muscles running along its body begins to tense. Everything is ready for a strike when the mouse enters into the snake’s danger zone. The viper’s attention is on this singular thermal image. Mentally comparing the intensity of heat detected by her left and right pits, she knows exactly where the animal is in space. The mouse, obvious of the waiting danger, finds nothing to eat at its feet and decides to move. Unfortunately, the movement is toward the waiting viper. As the mouse takes a few steps, the viper pulls its

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head back ever so slightly and unleashes itself. The strike is blindingly fast and true. The female viper has connected with the mouse and has sunk her fangs in deeply. The quick-acting venom is injected, and soon the fer-de-lance viper will eat its nightly meal.

35.2  The Science of Thermal Vision Pinhole cameras are wonderfully simple pieces of technology and prime examples of how ancestral eyes (and some modern eyes) work. These cameras are very old in their design but are a frequently searched term when a solar eclipse is eminent. As the name implies, all that is required to build this camera is a flat or curved plane on which the image will be projected and a pinhole that functions as the lens. During the last solar eclipse, I was out in the field doing research, so my students were quite creative about the construction of their cameras to watch the eclipse. A snack box, a shoe box, and old cardboard shipping container were all the basic starting elements of different cameras. From a sensory perspective, the pinhole lens is comparable to the lens of an eye, and the cardboard plane at the back is the functional retina. The pinhole is surprisingly functional as a lens because of the small aperture of the pinhole. The hole restricts how light enters into the box or retinal portion of the camera. Due to the small aperture, light arriving from different directions is projected onto the cardboard “retina” in an inverse fashion. The key to the image formation is that light from a single spot outside of the box lands on a single spot on the back of the box. The smaller the aperture, the better the image that is formed on the back of the box. The downside of this type of evolutionary design of an eye is that smaller aperture allows less light into the eye. While the image may be of better quality (less blurry), it is much more faint. Pinhole cameras are only really functional in environments with intense sunlight. Thus, cameras and eyes with lens that focus the light onto film or a retina solve the issue of image quality and brightness. The connection between pinhole cameras and thermal sensitives in snakes becomes apparent when heat is not really thought of as heat but as a form of light. Snakes do not detect heat in a similar fashion as we do while sitting around a campfire. We can extend our hands out and certainly feel the heat of the flames. In addition, we can detect differences in the temperature of the tips of our fingers that are closer to the fire than the palm of our hands. We do not form a spatial image of the heat coming off the fire like we do the visible light emanating from the flames. Yet, heat is a form of light. This stimulus is infrared light and lies on the electromagnetic spectrum. Infrared light is located beyond red light on the visible spectrum and has much longer wavelengths than the light we see with our eyes. The energy contained in heat travels as a light wave and can be detected with an “eye” that is sensitive to those longer wavelengths. If that eye is probably constructed, then a spatial image of the thermal patterns of an environment can be formed. This precisely what pit vipers do (Fig. 35.1).

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Fig. 35.1  Sensing the heat. The pit of pit vipers is a highly sensitive thermal organ. The opening at the outside of the pit serves to focus thermal energy on a membrane at the back of the organ and gives the snake the ability to determine the direction and distance of its warm prey

The pit organ is a pinhole camera with a small aperture and a heat-sensitive retina. The pit organ is an indentation in the skin of the snake. The pit is divided into two sections, an inner chamber and an outer chamber. Stretched across this division is a membrane that contains a series of receptor cells sensitive to thermal radiation. The top and bottom side of this membrane contains receptor cells, and the suspension between the inner and outer chambers increases the sensitivity of the pit organ in two ways. First, moving the membrane and the receptive surface away from the animal’s body (a source of heat) decreases the amount of heat noise that the receptors receive. Second, the suspended membrane allows the dense packing of receptor cells on both sides of the membrane as opposed to having a single layer of receptor cells against the snake’s body. Increasing the number of receptor cells increases the overall sensitivity of the organ. These two adaptations greatly enhance the ability of the pit organ to detect minute changes in the thermal landscape of the snake. Estimate of the sensitivity of these cells is 0.001° Celsius (or one one thousandth of a degree), certainly enough to detect small mammals against a darkened background. The adaptations listed above certainly make the snake’s pit organs unique within the animal kingdom but do not necessarily produce an organ that is helpful for the hunting of prey. The fer-de-lance viper (as well as other snakes with pit organs) has paired structures on their head with one on either side of their nostrils. The field of sensitivity of each organ extends outward from the organ in a cone shape that increases in size away from the animals’ body. This is similar to the visual field of each eye for those organisms with paired eyes. One of the main benefits of having two eyes with overlapping visual fields is the creation of three-dimensional vision. Visual information from a single eye does not allow the brain to produce a three-­ dimensional visual image. The brain needs to compare the relative locations of objects in space as perceived by the left and right eye. This can be demonstrated quite easily by staring at two objects in your visual field. Pick objects where one is

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closer to your eyes and the other one more distant. Now, close one eye and note the relative position of these two objects to each other. Switch the closed and open eye and you’ll notice that the relative position of the two objects changes. This change allows your brain to reconstruct a three-dimensional world for that part of the visual field that is overlapping. The snake performs the same reconstruction using the two thermal images from its left and right pit organs. By having paired pit organs with overlapping thermal fields, snakes have a three-dimensional thermal view of their world. The neural information from the pit organs is carried to the snake’s brain by its trigeminal nerve, which is the same nerve that carries thermal information from our fingertips to our brain. This information is shunted to a part of the brain that only appears within snakes that have pit organs. Finally, the information is passed along to the optical processing areas of the brain so that the animal can construct an image of its thermal world. The thermal world is a part of our own world, but we are really only aware of it as we shiver or seek warmth from a heater or fire phenomenon. Even then, the perception is strictly a two-dimensional world. The fer-de-lance snake has a temporally dynamic world of heat surrounding it. The snake’s precise perception of this world allows it to navigate this world as seamlessly as we navigate our visual world. To be far more precise, the snake has the ability to predict movement to such a degree that it has become a lethal night time predator.

Chapter 36

I Go to Die, You to Live

We think of death in many ways: the shedding of a mortal coil, the transition to a different state of being, a return to Earth in a form based on the karmic load, or for some, the end. For those loved ones, left behind, it certainly appears to be the end of a life together. Even the terminology of “left behind” denotes some sort of finality. Certainly, for the collection of atoms and molecules that came together in some miraculous way to produce a living, breathing individual, they shall part their molecular ways most likely to never meet again. Ashes to ashes and dust to dust should be atoms to atoms, molecules to molecules. In the grand scheme of nature, death and life are simply two sides of the same coin. Nature is the original and greatest recycler. The death of one organism means the release of those atoms and molecules that will be used by other organisms to grow and thrive. On the forest floor, insects consume fallen leaves which release precious nitrogen and phosphorus into the soil. Fallen timber is decomposed by hosts of fungi that send mycelium deep within the wood to break it down. Within the aquatic realm, a guild of organisms, called shredders, break down terrestrial plant matter that has fallen into lakes and streams. Without these shredders, this material and the nutrients contained within those leaves would be bound up and unavailable for other life-forms. In the natural world, death and life are intimately intertwined. In a similar fashion, disaster and opportunity are braided together as a singular event. The diversity and abundance of organisms found in any ecosystem is a result of many different factors that drive the life and death of individuals and populations. One of the most powerful factors is competition among organisms. Resources within an ecosystem are often quite limited. The light at the bottom of the forest is significantly more dim than the light in the canopy. So, plants compete for that critical resource by either growing as tall as possible or finding patches of sunlight that filter through the leaves. On the rocky coasts of the world’s oceans, space is at a premium. Organisms actively dislodge competitors from their claimed spot on a rock like a slow-motion version of king of the hill. Of course, nature is rarely fair, and often, these ecosystems can reach a point where a single organism, known as a superior competitor, drives other organisms almost to local extinction. © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_36

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In one of the most extreme examples of superior space competition, an invasive cattail has taken over in the coastal marshes of the Midwest of the United States to such a degree that the entire marsh is a monoculture of the invasive species. The native population of crayfish within Northern Europe has almost been extirpated by invasive species. From a historical and ecological perspective, the most egregious example of superior competition was a human mistake. The introduction of the rabbit to the Australian continent resulted in the unchecked population of grazers decimating millions of acres of land like millions of lawn mowers. These superior competitors take over an ecosystem because of an opportunity for growth and expansion, whereas the presence of the invasive is a disaster for the native species. If competition were the only factor at play, then the world’s ecosystems might be dominated by just a few species each. Disasters and death intervene to allow ecosystems to maintain their diversity. In old-growth forests, ancient trees dominate the landscape and shade out young saplings inhibiting their growth. Yet, trees perish and when they succumb to the ravages of time, the mighty trees fall. The death of this tree creates a gap in the canopy which allows light to enter the forest floor. The light creates an opportunity for saplings to compete and grow toward the sky. The tree, itself, creates a new habitat for beetles to lay eggs and fungi to begin decomposition. In the numerous rivers in the world, a flood event scours the bottom of the river and opens up new habitat to be colonized by algae and plants. In the rocky intertidal shoreline, winter storms pound the rocks and loosen barnacles to create new space for young invaders to take. In grasslands, a lightning strike starts a brush fire that burns acres of plants but leaves behind virgin ground for opportunistic plants to conquer. Death for one group of organisms is the opportunity of life for others. This last example, fire, is a particularly intriguing one. In the previous chapter, fire was a symbol of warmth as well as a symbol of life for the fer-de-lance snake. Fire, when properly controlled, heats our homes, cooks our food, and warms our baths. Untamed fire is as dangerous and deadly as any predator on the planet. One of the greatest fears for mariners on wooden ships or dwellers in skyscrapers is a fire. Across grasslands and deep in forests, the presence of a fire can spread quickly by igniting the previous year’s growth that has started to decay. Unlike most predators, fire is nondiscriminatory. It will burn and consume everything within a habitat and leave behind quite a barren landscape. Most creatures will attempt to escape the deadly blaze, but few animals can outrun the threat. One would think that with all of this death and destruction, fire would be universally feared, but there are some organisms that will welcome the intense heat. For some organisms, the heat and destructive nature of fires are the only ways that they can reproduce. The jack pine produces pine cones that are sealed shut with a strong resin. The seeds and future lives of young plants are locked in that pine cone until the resin melts and releases them. The pine cone only opens under the intense heat of a forest fire, and because of this, jack pines are often the first trees to reestablish a habitat after a fire. The jack pine is not alone as the lodgepole pine and eucalyptus trees also have seeds encased in a heat-sensitive resin. Of course, adaptations of plants to fires are probably not too surprising since they can’t move when a

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fire approaches. There are animals, though, that move toward a forest fire rather than run away. For these animals, the death of the tree means life for their offspring. One such animal is the black fire beetle, Melanophila acuminate. This beetle is one of many beetles in the family Buprestidae called the jewel beetles. Jewel beetles are absolutely beautiful creatures because of the iridescent colors on their exoskeleton. These beetles range in color from sublime greens and blues to brilliant patterns of yellows, oranges, and reds. The black fire beetle is so named because of its deep dark elytra (wing casing) which almost appears burnt or charred. The “fire” part of its name arises from its unique behavior of seeking out and traveling toward forest fires as opposed to the more sensible decision employed by most animals which is to run away. This behavior is tied to some particular requirements of its life cycle, and because of these requirements, the beetle is usually found within freshly burned forested areas. To observer this peculiar behavior, we shall travel to the forests of Germany, northwest of Berlin.

36.1  Finding a Romantic Fire Succession is an ecological term that captures the concept that the species composition of ecosystems evolve over time. As explained above, competitors within an ecosystem are rarely evenly matched, and because of this imbalance, superior competitors usually begin to dominate in undisturbed habitats. The destructive and deadly nature of fire is undeniable, but within forest communities, fire serves a useful and ecological purpose. Patches of forest dominated by superior space competitors are cleared out, and new species can colonize the newly opened habitat. As we search for the black fire beetle, we’ll actually be searching for a forest that is going through this dramatic change. Certainly one of the best indicators of a forest fire is the presence of smoke in the air, and just such a plume is about 10 km off in the distance. The smoke is probably the most visible aspect of the forest fire from this distance, as the flames have not risen over the tops of the trees. The black fire beetle has the ability to detect heat of the forest fire from this distance as it ignores the visible smoke. The journey can take some time at this distance, but the beetles are not deterred. The ultimate prize in regard to evolution and reproduction awaits in the forest that has been ravaged by fire. To watch the final legs of their journey, we’ll move closer to the trailing edge of the forest fire and search for any approaching beetles. As we get closer to the damaged area, darkened brush and smoldering trees are seen sparsely dispersed in this area. To be honest, the husks of trees left behind and charred ground and soil don’t appear to be valuable at all. The succulent leaves and grasses that could serve as food are consumed by the intense heat of the fire leaving nothing but ash behind. The skeletal remains of any trees left standing lack any resources for nests or shelter. Within this desolate landscape, we catch as a small black object flying into this heated wasteland. Moving closer to the flyer, the black fire beetle becomes visible and readily identifiable. Unlike other flying insects,

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b­ eetles have a protective covering over their wings (elytra), and, in order to fly, the beetle needs to open the wing casings like giant garage doors. Lifted using a hinge near the head of the animal, the beetle keeps this paired structure open to allow the wings the necessary space for movement. The elytra gently rock back and forth with the ferocious wing beats, and the iridescent colors of the elytra create mesmerizing reflections as the animals fly. Beetles aren’t the most graceful flyers as they appear to be struggling to keep themselves aloft. Despite the apparent struggle, beetles are among the most successful groups of insects on the planet. The beetle is heading straight toward the middle of the barren landscape. The fire just finished burning in this area and small spots of glowing coals are still visible. The beetle is ignoring these coals and is focused on the vertical remnants of the trees. Some trees are completely dark and are almost cool to the touch. Others still burn, bright with fire and flames. A third group of trees falls in the middle of this temperature spectrum. Not quite cooled, these trees have wisps of smoke arising from them and are still fairly warm. The beetle is actively flying in and around these trees and appears to completely ignore the trees that fall within the first two categories, burning and burnt. What draws the animal into specific trunks are the trees exhibiting the intense warmth of a fire recently finished. Glancing around the landscape, it becomes apparent that other black fire beetles are making similar decisions. Trees that have flames are avoided as well as the trees that have finished their burn. The other trees, the ones still steaming, have a scattered few beetles on them. Returning our gaze to the focal animal, this particular beetle has begun its final approach to a tree. The bobbling and randomness of the previous search flight is missing. The beetle has locked onto this singular tree and is approaching the exposed surface quickly. The animal lands with a light touch and gently closes its elytra, protecting its wings from the singed surfaces of the tree. Its transformation from aerial flier to terrestrial walker is complete, and it switches to a patterned search on the trunk of the tree. About a meter above the walking beetle is another black fire beetle. This beetle is a female that landed on this tree just moments ago. The two beetles approach each other, and, after a short period of assessment, the two animals begin to copulate. What occurs may appear to some as macabre as any scene written by Edgar Allen Poe or to others as a romantic dalliance near an open fire. These two beetles are using the destructive force of the fire to reproduce and lay eggs. The larvae of the black fire beetle survive only on the exposed and fire-charred remains of trees. Full healthy trees and completely burned trees will not do. So, these two creatures have used their extraordinary ability to perceive the infrared energy of the intense heat to locate just the right tree to reproduce and lay their eggs. Among the dead and dying forest, new life will spring forth as the larvae grow and feed upon the remains of these trees.

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36.2  The Science of Tracking the Heat The larvae of the black fire beetle feed exclusively on the exposed wood of freshly killed trees. Without many of defenses, the larvae are helpless to protect themselves against the physical and chemical defenses that trees use against invading insects. In addition, the larvae are susceptible to competition from other wood-feeding insects. So, the heat of the recently burned tree provides the larvae with protection from the trees and other competitors. As such, the ability of the adult fire beetles to detect and respond quickly to forest fires is highly favored. It is not an uncommon sight to see both the male and female beetles in great numbers on the tail end of forest fires. The sexes are drawn in by the infrared radiation being emitted by the fire, and, once on the same tree, the adults will copulate even if the tree is still burning. Forest fires burn at immensely high-temperature levels. Fires burn at temperatures ranging from 600 to 800 °C and these temperatures create the infrared radiation to which the black fire beetles respond. Other organisms that sense infrared radiation are tuned to much lower temperatures. Pit vipers, blood-sucking insects, and vampire bats are sensitive to signals closer to animal’s body temperatures which are between 30 and 40 °C.  The higher temperature of forest fires creates long-­ wavelength radiation that travels great distances from the source of the fire. This radiation is not scattered as easily as smaller wavelength light (like blue and ultraviolet) which increases the distances these signals travel before they become undetectable. Radiation can be described in a number of different ways, but from a sensory perspective, wavelength is the most important. Forest fires emit radiation that has a wavelength between 3 and 5 μm. This length is quite small in absolute terms, but compared to blue (480 nm) and green (550 nm), the wavelengths are ten times longer than other colors. This wavelength (3–5 μm) is precisely located within an atmospheric window where water vapor and CO2 fail to absorb the radiation. The beetles have been shown to track these fires from tens of kilometers away, and some reports have indicated a distance of up to 80 km. To capture these invisible signals, the black fire beetle has evolved a pair of specialized sensors that are tuned to this high-temperature thermal signal. Interestingly, the sensors are not located on the head of the animal. Since most animals move through the world with their head leading the way, sensory systems are often located on the front of the animal. In the black fire beetle, the infrared receptors are located next to the coxae of the mesothoracic leg. The coxae is the small joint that connects the leg of the beetle to the body and functions similarly to the human hip. The beetle’s body is composed of three different sections from the anterior to the posterior of the animal: the head, the thoracic, and the abdomen. The head of the beetle has most of the other sensory appendages. The thoracic has two pairs of the legs, while the remaining pair of legs rests on the abdomen. The mesothoracic legs are the middle legs since meso means middle. So, the sensor rests near the middle of the beetle’s body, and they have a single sensor on either side of the body (Fig. 36.1). The sensor is a small oval opening on the side of the beetle. Within the opening are numerous small domes that appear like a large tray of dinner rolls. Each dome

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Fig. 36.1  Sensing a forest fire. The black fire beetle has a specialized organ that appears as a series of raised bumps (left-hand drawing). Slicing one of the bumps in half reveals a layered organ that serves to funnel the energy from heat waves to the tip of a dendrite. The heat causes a small-scale expansion of the layered organ which activates the dendrite

is an infrared sensor and there are over 50 sensors per organ. If one were to remove a single dome from the animal and slice it in half, the sensor would take on the appearance of an onion on top of a thin stalk. The dome, or onion-shaped structure, is called a spherule. At the top of the spherule is a small pore that allows the infrared radiation to enter the sensory structure. The layers of the “onion” are different structural components that help funnel the radiation downward through the spherule to the tip of the stalk. Although not completely worked out, the central core of the spherule appears to contain a substance that absorbs infrared radiation which acts to amplify the incoming signal. Finally, the base of the spherule is connected to the stalk where the dendrite of a single receptor cell is housed. So the infrared radiation travels outward from the fire and eventually impacts the 50 or so spherules on the black fire beetle’s side. The radiation travels through the pore and is absorbed by the material in the middle of the spherule. When the material absorbs enough radiation, the dendrite is activated and sends a message to the beetle’s brain that a forest fire is near. Unlike visible receptors or even the modified receptors in the pit organs of vipers, the black fire beetle doesn’t detect the infrared radiation as part of a visual field. Most materials will expand when exposed to heat. The old kitchen trick of running the lid of a stuck jar, say pickle jar, is an example of this phenomenon. Both the metal lid and the glass jar expand, but the lid expands faster. So, placing the jar in hot water expands everything including the space between the lid and jar. This increased space allows one to open the jar and gain access to the delicious pickles inside. That mysterious substance in the middle of the spherule is no different. As infrared radiation passes through the pore, the heat is transferred from the air into the substance in the middle of the spherule. As the entire middle of the dome expands, the spherule touches the dendrite and deforms the end of the nerve cell.

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The simple act of deforming the tip of the dendrite turns on the neuron and generates signals for the beetle’s nervous system. As the intensity of the heat increases, the spherule expands more quickly and to a greater extent which activates the neuron even more. Thus, the rate and size of the expansion is directly proportional to the amount of heat arriving through the pore. With over 50 sensors on either side of the beetle, the animal can determine the direction and intensity of any forest fires in the region. Placing the sensors behind the middle legs is not the best of locations though. If the legs are held downward, their presence blocks any thermal energy from striking the sensors. So, the black beetle, while searching for a romantic fire, flies with its legs held aloft. This keeps the sensory window open and allows any infrared radiation access to the awaiting spherules. Holding the legs in a vertical fashion while flying makes the beetle fly a little awkwardly. By moving the legs up and down, the beetle can regulate when the infrared sensor is open or closed. This could be the beetle’s version of blinking or even blocking the intense heat when it eventually lands on a smoldering tree. The ability to control stimulus access to the receptors probably helps the beetle compare the intensity of stimulation between its paired sensors to determine the best path of flight toward the fire. With this incredible sensor, the male and female black fire beetles gather together with warm and crackling fires all around them. Despite the death and devastation that surround them, they come together, after a tremendous journey, to propagate and give their larvae the best possible chance at survival.

Chapter 37

A Shocking Discovery

It is hard to imagine a modern culture without electricity. Lights, computers, cell phones, and other modern conveniences are such a central part of our daily existence that the use of electricity is hardly noticed. Most of the items in our lives use a form of electricity called AC which means alternating current. The prevalence of this type of electricity was almost universal until recent technological advances. Now, LEDs, computers, and electric vehicles are all powered by direct current or DC electricity. Today, these two forms of electricity are increasingly interwoven together, but not too long ago, these two types of electricity were the center pieces of one of the most epic societal battles, and it involved two of history’s greatest inventors. In the corner promoting DC was the famous Thomas Edison. Holder of other one thousand patents, Edison certainly left his mark on history with the invention of the light bulb, the phonograph, and the movie camera. A fierce competitor and defender of his patents, Edison promoted DC electricity as the wave of the future. His enemy was Nikolas Tesla. Lesser known than Edison, Tesla was as much a genius and innovator as Edison. Tesla created the Tesla coil, induction motors, and neon lamps among other things. Tesla was convinced that AC electricity was safer and a better version of electricity to move the world forward. These two titans clashed for years, but the battle came to a head at the Chicago’s World Fair at 1893. The fight over the right to power the world was called the war of the currents. In DC electricity, the charge flows only in one direction, and the voltage or current is held constant. Batteries that power our computers, toys, and cars are forms of DC current. AC current is a bit more complex. In AC electricity, the flow of current or charge changes direction periodically. This change, termed alternating, occurs quite rapidly, over 60 times a second. The rate of change varies across the globe, but most power outlets in buildings have AC power. One of the biggest advantages of AC power is that less energy is lost with the transmission of high voltages, so the wires conducting the power heat up less than wires that carry DC power. The lower heat decreases the fire hazard generated by electrical wires. Edison and Tesla fought on both economic and political fronts to ensure that their method of power (along © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_37

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with the inventions they created for their power) would win the day. Ultimately, Tesla won this war, but sadly, Edison remained far more visible within the annals of history until quite recently. Today, the war is over, and companies are developing technology that seamlessly uses both forms of electricity. Humans aren’t the only animals that depend upon electricity for survival. Elasmobranchs are a group of aquatic organisms composed of sharks, skates, and rays. These animals are typically top-level predators in their environments. Probably because of our fascination with sharks as a predator, it is fairly a common knowledge that these voracious animals can detect electrical signals emanating from prey items. Sharks have an abundance of electrical sensors near their eyes and mouth and use this sense during their final attack run. Skates and rays also have this sensory ability and use their electroreceptor to detect prey hidden underneath sand and substrate on the ocean floor. Although these animals are quite sensitive to electrical signals, their abilities pale in comparison to other creatures of the deep. The prehistoric-looking paddlefish is a relative of the more famous and caviar-­ producing sturgeon. Only two species of this fish are still in existence across the globe: a Chinese paddlefish found in Yangtze River basin and the American paddlefish endemic to the Mississippi River. Both fish consume small planktons, like daphnia and copepods, which are swimming in the water column of these massive rivers. In most areas of the river, the water is either dark and murky, so the visual detection of these small and transparent prey is extremely difficult. This is where the paddle from their name comes in handy. The paddle is a hardened structure that extends forward from the mouth of the animal. The edges of the paddle are lined with millions of electroreceptors that are quite sensitive to any electrical currents in the rivers. As the animal swims along, any daphnia or copepods that are near the paddle are detected by the electroreceptors. The tiny muscles in the zooplankton create minute electrical currents. These currents are picked up by the electrical sensors in the paddle, and as the paddlefish swims forward, toward the zooplankton, the current travels down the paddle toward the animal’s head. This signal, and its change over space and time, provides accurate information about the spatial location of the prey, and the paddle fish alters its swimming to easily catch the zooplankton. While the animals, in the examples above, detect electrical signals, they cannot produce their own signal. Probably the most famous animal to produce its own electricity is the electric eel, which creates a strong enough electric current to stun prey. Along with the electric eel, there are catfish and electric rays that also produce strong enough electrical currents to stun underwater prey. As a group, these animals are called strongly electric fish due to the intensity of these currents. More interesting than the strongly electric fish are a group of animals known as the weakly electric fish. These animals produce their own electrical current, but, as their name implies, that current is much less powerful than those of the eels, catfish, and rays. These animals produce their signals to sense the electrical landscape of their world which allows them to navigate, detect objects, and communicate with each other. From a sensory perspective, the weakly electric fish have a much more diverse set of behaviors, abilities, and signals than sharks, paddlefish, or eels.

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While the war of the currents was wholly a terrestrial, and human, phenomenon, the aquatic environment had its own version of the war of currents that occurred over an evolutionary time period. The knifefish are gymnotiform fish found within the freshwater environments of South America. This group of fish is called knifefish because of their body shape: large at the head and tapering back on a constant line like a carving knife. The animals swim by undulating their anal fin that runs the entire length of their body. This adaptation may make them slow swimmers, but the lack of any large-scale muscular contraction to swim reduces the background electrical noise. The knifefish are called weakly electric fish because they detect and generate electrical currents but use it for navigation and communication rather than prey stunning like electric eels. In the Gymnotiformes are two interesting newly discovered species of knifefish that play the role of Edison and Tesla. The knifefish, Brachyhypopomus walteri, produces an AC electrical signal to communicate with its fellow species, while Brachyhpopomus bennetti plays the role of Edison by producing a DC electrical signal. Although not really in a war of currents, the fact that the animal world uses both types of electrical signals further displays the diverse sensory environment that lies beyond our capabilities. Despite the presence of both AC and DC signals within the animal kingdom, most species produce DC-type signals. Thus, the discovery of the AC-producing knifefish is intriguing and could provide new insight into the evolution of electrical communication in fish. To understand how knifefish sense electrical signals and use them for communication, we’ll turn to a well-researched third species of knifefish, Brachyhypopomus pinnicaudatus the pintail knifefish, for our safari. These animals are found deep within the Amazonian rainforest in the murky and muddy waters of the famous river.

37.1  An Electric Soul Many electrically sensitive fish are found in habitats with relatively slow-moving water. In addition, these habitats tend to be quite muddy which will limit the transmission of visual signals. These two elements, slow moving and muddy water, describe the freshwater habitat of the pintail knifefish. Most of the organisms that use electrical signals in complex ways are found in freshwater habitats. Their saltwater counterparts almost always use electrical signal only for the detection of prey and rarely produce electrical signals for navigation or communication. Freshwater has a relatively high resistance to current flow as compared to saltwater. Because of the high resistance, currents produced in freshwater habitats are confined to small localized areas around the fish and are drawn toward biological objects. This is because animals have a lower resistance to electrical current than the surrounding water. In saltwater habitats, electrical currents flow quite easily and are dispersed over larger distances. The organisms that live in saltwater have about the same resistance to electrical current flow as the surrounding water, so any currents produced are not attracted to biological objects. All of this means that freshwater habitats are

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excellent environments to use electrical signals to distinguish living from nonliving objects and to send focused signals to other organisms. The pintail knifefish constantly produces electrical pulses for these two reasons. We’ll find the pintail knifefish in the nearshore environment in the Amazon River. Floating and moving among the roots of trees and fallen branches, the pintail is difficult to spot. Still, with enough searching, a male can be found making his daily foraging trip among these roots. This particular male pintail is a greenish brown fish and is roughly 15  cm in length. Like all Gymnotiformes, the animal moves slowly through its environment using its long anal fin. While not a very powerful propulsion system, this style of swimming allows the animal to keep the rest of its body motionless in order to produce and detect its own electrical field. The animal produces a characteristic electrical signal that is a single wave. Repeatedly generating this signal, the animal produces an electrical field around it that is similar in structure to the magnetic field for the earth described earlier. Moving through its habitat, the animal perceives distortions in this waveform field to detect living objects from the various rocks, dead branches, and other obstacles in its environment. This is called electrolocation. Our pintail, despite the lack of clear visual cues, is easily moving around the dense roots that cover this part of the Amazon. The pintail moves slightly to the left and swims forward through a couple of roots. The waves of undulation moving through its anal fin gently redirect the animal as it swims forward. As we watch the animal move through its environment, we see no discernable change in the behavior of the animal. There is no movement of the animal’s head or other fins, and yet, it easily glides through this complex labyrinth of rocks and roots. It is mating season for the pintail, and this male, as it swims along, is waiting for the right type of distortion of its electrical field. The animal is producing a constant signal in order to electrolocate, but the signal has a secondary purpose also. Our focal male is advertising its readiness to mate through its signal. The waveform is a broadcast signal and the male is hoping that any females in the vicinity will detect his signal and respond. The focal male continues his journey through the darkened waters of the river in hopes of finding a suitable mate. Female knifefish in the area will detect his navigational signal and determine if the signal matches the characteristics that she desires in a potential mate. If the female is gravid, she’ll be ready to mate to have her eggs fertilized. The male knifefish is swimming through the environment and calling to any potential mates with his electrical signal. Over and over again, he generates his waveform waiting for a gravid female to find him attractive. Ducking under a mass of roots, the male knifefish emerges on the other side and senses something new in his environment. A disruption in his electrical field clearly indicates that another knifefish is nearby. The male and female knifefish produce subtly, but importantly, different electrical waveforms, so the focal male can easily tell that the nearby fish is a female. In addition to these sex differences in signal production, the mating season brings changes in the hormones of both fish. These hormonal changes also alter the waveform of the electrical signal. Due to these signal differences, the male knifefish uses the other animal’s waveform to determine not only the sex of the other animal but its reproductive state. Using the pattern of

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distortion in his own electrical field, the male locates the female and moves closer. The focal male continues his calling in hopes of convincing the female that he is a worthy mate. The female, in turn, analyzes the male’s electrical signal, responds to his calling, and moves toward the male. As we observe this interaction, all that is visible is two fish turning to face and slowly swim toward to each other. Once the two animals are close to each other, they remain motionless except for the constant undulating pattern of the anal fin. What appears to be a stare down contest is really a complex series of communications using electricity. The focal male calls forth and the female responds in kind. Inherent in the male’s electrical pattern are, yet unknown to researchers, cues to his fitness. The female knifefish examines both the waveform and the electrical field it generates to make her decision on whether to mate or move on. The two animals slowly circle each other while maintaining their relative positions and distance. After a seemingly endless period of a face off, the female moves closer to the male and indicating a willingness to breed. The male responds with his own movement toward her and the female turns to head to the bottom of the river. As external spawners, the female will lay her eggs at the bottom of the river, and the male will swim past releasing his sperm at the right moment. While not quite the romantic encounter envisioned in movies with “electricity in the air,” these two animals have used the electricity in the water to make one of the most important decisions an animal can make.

37.2  The Science of Sensing Electricity Electroreception has been identified in a wide group of animals including egg-­ laying mammals, insects, and amphibians. Animals in this group can use this sense for predator detection, prey detection, navigating through their complex environments, territorial defense, identifying individuals, and sexual selection. The widest use of electroreception, as well as the production of electrical signals, is found in the three main groups of fish: Agnatha (jawless eels), Chondrichthyes (sharks and rays), and Osteichthyes (bony fish). Electric fish have a diverse set of behaviors that rely on their ability to produce and detect electrical signals. The ability to perform all the behavioral tasks outlined above depends on two distinct features: first, the ability to create a controlled, unique, and reproducible electrical signal and, second, the ability to detect subtle differences in the structure of electrical signals. The first task, the production of an electrical signal, is carried out by a structure known as the electric organ, and the signal is known as an EOD (electric organ discharge). The aptly named electric organ is found either in the tail or the posterior part of the fish’s body. The organ itself is constructed of modified muscle tissue. The cells of the organ are called electrocytes and can be thought of as a series of batteries stacked end to end. The size and number of the batteries determine the intensity of the signal that the animal can produce. In addition, the electrocytes have a polarity, just like batteries, and the alignment of the batteries determines the polarity of the

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electric field that is produced by the animal. If the electrocytes are reversed, then the resulting polarity of the electrical field will also be reversed. The firing of the EOD is controlled by a group of cells in the fish’s brain called the pacemaker nucleus. These central nervous system cells innervated the electrocytes and determine when they discharge. The pacemaker cells also control the synchrony of the battery-like electrocytes. The synchrony of the discharges helps shape the waveform that is produced by the animal and allows for the development of species-specific as well as individually specific waveforms of the EOD. As a final bit of control, the membrane properties of the electrocyte cells help shape the types of waveforms that the organ can produce. So, with differing alignments of their batteries, precise control by pacemaker cells, and control over electrical waveforms by patterns of firing and membrane properties, the different weakly electric fish can create a wide diversity of EODs including the AC and DC patterns of the two recently discovered knifefish. All of this control and fine-tuning of the EOD is wasted unless the fish can perceive all of these subtle differences in the electrical signal. Knifefish and other electroreceptive organisms sense electrical fields through one of two types of receptor cells. The first type of receptor is called a tuberous organ and consists of receptor cells buried beneath the skin. These organs have five to ten receptor cells in a small pocket that is surrounded by supporting cells. The surrounding cells have a type of coupling called a tight junction that prevents electrical current from flowing out through these cells and into the body. The tight junctions serve to focus and funnel the electrical current down to the receptor cells. The cells directly above the receptor cells are connected with a different type of juncture that allows the electrical current to travel through them and to the receptor cells. The receptor cells are connected to nerve fibers that send information along to the brain of the animal. The second type of receptor cell is more common and is designed to carry more information about the electrical landscape for the knifefish and other electroreceptive fish. These receptors are called ampullae of Lorenzini after the Italian physician that discovered them in the late 1600s. These are the main receptor types for the detection of electrical signals used in navigation, prey finding, and social communication. The ampullary organ consists of a lumen, or channel, through the skin to the surface of the receptor cells. In some species the lumen is filled with a conductive gel and, in others, the lumen is empty. Along the walls of the lumen are cells with tight junctions that, like the tuberous receptors, serve to confine the electrical current to the lumen which funnels the signal to the receptor cells. At the base of the ampullae are three to five larger receptor cells with microvilli on their apical surface. As the electrical current strikes the upper surface of the receptor cells, the cells depolarize and activate secondary neurons (called primary afferents). Both the tuberous and ampullae receptor cells do not have axons and connect to the brain of the animal through these secondary neurons. The ampullae of Lorenzini are the electric receptor organs found in a wide variety of teleost fish including sharks, skates, and the weakly electric fish (Fig. 37.1). In those animals that use electroreception to navigate and communicate socially, the primary afferents carry their information to the brain of the animal in a

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Fig. 37.1  The ampullae of Lorenzini. The electrically sensitive cells of weakly electric fish are located at the bottom of a tube in the skin of the fish. The cells that line the tube are sealed together which funnels the electrical signal down to the waiting receptor cells

s­ omatotopic manner. Similar to the information from the visual system, the touch sense in our face and hands, as well as the catfish taste system, the somatotopic map means that spatial information of the signal is available to the animal. For example, a primary afferent from the lower right side of the knifefish innervates a particular area in the brain that signals lower right side. The brain creates an electrical map of the animal’s body which allows the fish to reconstruct a three-dimensional map of its electrical world. Thus, the knifefish knows exactly where the electrically important objects are in its environment which includes potential mates, predators, and competitors. With the ability to produce a variety of electrical signals and then detect these signals in other animals, the knifefish can easily navigate its darkened and murky watery world. Finding prey, avoiding predation, and swimming through complex structures are all done via its electrical map that is constantly being updated. When the seasons change and mating time arrives, the knifefish uses precise control of its electrical current to generate a signal to call to gravid females. Certainly, the knifefish has an amazing set of signals and detection techniques that have allowed the animal to thrive in a depauperate sensory environment. The knifefish evolved these abilities many millennia before Edison and Tesla even began to think about any war of currents.

Chapter 38

Chasing Ghosts

When I was much younger, around my early teen years, I must confess that I had quite the fascination with ghosts. I had an unquenchable thirst for books, movies, and stories about these intriguing “beings.” The budding scientist in me wondered what was their material composition, what sort of properties did they exhibit, what caused their appearance and disappearance, and why couldn’t anyone capture good hard evidence of their existence? As I have written elsewhere in this book, I was also captivated by Jacque Cousteau and his ability to find and quantify the numerous organisms beneath the surface of the ocean. If he could dive to great depths and record previously unseen organisms, why couldn’t someone easily get hard evidence to the existence of ghosts? As I grew older, read more, and began my scientific training, the answers to many of my questions of ghosts became quite apparent. It is difficult to acquire hard evidence on something that doesn’t exist. Despite this conclusion, I am occasionally drawn to watch any of the numerous TV shows where a set of supposed experts take their high-tech equipment and head out to find some evidence of hauntings. I watch these shows with a sense of amusement rather than any scientific curiosity about finding any evidence of ghosts. The training of the paranormal experts definitely doesn’t follow any normal concepts of training. The background of the experts range from filmmaking, acting, plumbing, and other various careers unrelated to anything scientific. The formula for the shows is basically identical regardless of the expert, location, or type of haunting. The host readies  the audience (which is called priming) by interviewing the haunted individual while displaying various creepy images or eerie sounds. The host and their crew of equally “well-trained” individuals then assembles various visible light and infrared cameras, audio recorders, and even some gadgets designed to measure electrical fields. After the equipment is appropriately spaced around the house, nightfall arrives, and the crew walks through the house with handheld cameras. Calling out the spirit’s name, the crew hears and records various noises and blurry images and are routinely scared by random sounds. Finally, in the big reveal, the host shows two to three pieces of weak evidence of the haunting. The video and audio recordings would hardly qualify as proof and are nothing compared to the images and audio © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_38

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tracks produced by real scientists finding rare and hidden organisms in the most remote locations on the globe. Maybe the most intriguing aspect of these shows for me is the concept of measuring or detecting the presence of something that is long gone. Organisms leave imprints of their presence, and for those with the right sensitivity, it is possible to identify the organism that created them. Rather than traveling to a haunted house and seeking traces of nonexistent beings, walking through a forest is just as exciting. Broken twigs or slightly worn-down plants provide clues to potential pathways or trails used by grazers. Footprints on a shoreline can give a clear picture to the waterfowl that might be hunting in that area. Bits of feather or fur are clues to the puzzle of a predator-prey interaction. A whole scientific field exists that uses the presence of scat (excrement) from predators to determine the ecology of a habitat. Even the aroma of different habitats can provide information on the presence or absence of different organisms in an area. Here, chasing the ghosts of organisms is a far more fruitful exercise than chasing fragments left behind by imaginary creatures. All of the above examples are terrestrial. The terrestrial environment has many advantages when using traces and imprints to determine the presence of an organism. In essence, the terrestrial environment is a two-dimensional environment. All organisms, even the long-distance flying birds, need to contact solid ground at some point in their lifespan. Nesting, mating, and even foraging are often performed either on the ground or on something connected to the ground (trees and shrubs). Life’s connection to the earth in the terrestrial environment leaves behind obvious indicators of activity. In addition, the lighter density of air allows feathers, fur, scat, and broken twigs to fall to the ground which can be found later by the searching scientist. In the aquatic realm, there are numerous creatures, ranging from the microscopic algae to the enormous blue whale, that never come into contact with the bottom of the ocean. The greater density of water creates a habitat where scat, scales, and other bits of organisms float away. Even if these bits ever end up on a beach or ocean bottom, it is usually kilometers from where the organism lived. Thus, tracking the footprints of organisms in the aquatic realm is almost impossible. One advantage that the aquatic realm holds over the terrestrial world is related to the increased density of water. Water is approximately 800 times denser than air, and this difference creates a truly three-dimensional world in which its organisms can live completely within the medium. As animals swim, float, and move through their aqueous world, they leave behind hydrodynamic footprints. The same occurs in the terrestrial environment, but because of the lightness of air, these footprints are hardly noticeable and easily dissipated. Depending on the size and speed of the aquatic organisms, these footprints can be turbulent and chaotic at large scales and fast speeds (most fish), laminar and predictable at small scales and slow speeds (small algae), or somewhere in-between these two extremes (larval organisms). Any object that interacts with a moving medium leaves behind a wake which is a disturbed section of flow. There are wakes behind tree trunks in a breeze, cars driving along highways, and whales and fish as they swim in water. Because of the higher

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density of water, compared to air, these wakes have a more defined structure and longer lifetime than those produced in air. Fish swimming in the dark waters of the deep ocean may disappear from sight just as quickly as any ghost, but the wake is as powerful of a trace as any footprint. If a stimulus exists, then there is undoubtedly an animal that has evolved to take advantage of it. As individuals or schools of fish make their way through the world’s oceans, they leave behind thousands of wakes. Each wake is a set of hydrodynamic footprints that lead right to their source. Predatory pinnipeds, such as seals, walrus, or sea lions, are carnivorous mammals that hunt in the dark, cold waters of the oceans in the northern hemisphere. While walrus focus on benthic mollusks, the seals and sea lions use their impeccable agility to hunt down and catch fish. In the lightless depths, these animals rely on these invisible wakes to guide their search. On this safari, we’ll focus on the harbor seal, Phoca vitulina, and its prodigious hunting skills. Located near the rocky shorelines of the north Atlantic and Pacific, we’ll head to the rough waters of the North Sea to find our animal. When on land, these animals often rest on the rugged boulders of the coastline of Norway. On these boulders, the animals crawl and hop awkwardly across the shoreline, but once in the water, the seal glides through the water effortlessly. While not as fast as dolphins, harbor seals are far more flexible and agile. Their swimming skills along with their tracking abilities create a formidable predator for any North Sea fish.

38.1  Fleeting Curls of Water Both male and female harbor seals readily hunt for a variety of fish in the North Sea. They have a diverse diet of fish comprising of sea bass, salmon, menhaden, and cod as well as the occasional shrimp, crab, or squid. These prey are excellent swimmers and require quick reflexes to attack and capture. Typically found sunning themselves on large rocks on the coast, the seal only spend time in the water to forage. The seals are easily seen both on land and in the water as their spotted pattern and brownish colors stand out from their surroundings. Harbor seals have excellent eyes, a pair of nostrils, and ear holes that are visible from quite a distance. All of these “basic” sensory organs help the seal locate prey, but the final capture is done through its remarkable ability to track the hydrodynamic wakes of escaping prey. Besides the eyes, ears, and nose, the most obvious feature on the seal’s face is its prominent whiskers. These sensory organs are the key to the tracking behavior of the harbor seal. As we approach the rugged coastline of Svalbard, a number of harbor seals can be seen on the shore. The barren and treeless landscape is uninhabited by humans but makes for an excellent habitat for the harbor seal. The seals are currently sunning themselves in an attempt to warm their body against the frigid weather. The copious layers of blubber help keep in their body heat which is an essential adaptation when they plunge into the icy waters to hunt. Several large female seals are together on some rocks fairly close to us and, as one slips off, an opportunity to

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watch the behavior of the seal presents itself. The seal ducks into the water and is off on its hunt for the day’s meal. Under the water, the harbor seal is transformed from an awkward walking land mammal to a gifted swimmer. The streamlined body allows the seal to glide through the water after powerful strokes with its flippers. The female brings its hind flippers together to form a single large flipper and moves its body side-to-side to create its forward momentum. Swimming downward in a straight line, the harbor seal uses its front two flippers to instantly change direction and is now moving laterally in the water column. Its speed and agility is at odds with the blubbery shape of the animal. The female effortlessly spins and rotates through the water as she hunts for prey. A school of cod begin to take shape ahead in the murky and frigid waters. The cold waters of this fjord are crystal clear, but even under these conditions, the light transmission is quite diminished. While visible, the far end of the school of cod fades into the background of the ocean waters. The female seal must have seen the school because she has altered her swimming direction and is heading straight toward the middle of the school. With two massive thrusts of her lower body, she has picked up speed and is quickly approaching the school. The cod in these waters can grow over a meter in length and up to 20 kg in mass, a great find for the female seal and definitely a hearty meal if she manages to catch one. The schooling cod, made up of a hundred or so fish, twist and turn as a single entity. It appears as if some unseen guiding force directs the school through the environment. The elegant and cohesive nature of the flowing school is quickly disrupted by the approaching seal. The female harbor seal heads straight toward the middle of the school in its initial attempt to capture a single fish. The school, with its hundreds of eyes, has early warning of the predator’s arrival, and, just as the seal dives into the mass of fish, the school scatters and reforms. For the seal, the scattering behavior creates a confusing mixture of images as the jumbled masses of fish fan out in random directions. The visual landscape of the seal is now awash with chaotically moving silver blips punctuated against the darkness of the oceanic background. Yet, amidst this visual anarchy, each individual fish has created a hydrodynamic wake trailing behind it. This wake is a series of small curling water currents that lead directly to the fish. In a flash, the seal changes its direction and heads directly at a subsection of the school while the fish attempt to find their places in the newly reformed formation. Invisible to us as we observe the action, the seal is intimately aware of the hundreds of wakes behind the scattering fish. Each trail is slightly different from the next and, as sure as footprints in the sand, leads directly back to the fish that has created it. Pulling its front flippers to its side, the seal prepares for another pass through the school of fish. During this pass, the seal’s agility is highlighted. The ability to twist and turn on a moment’s notice gives the seal the ability to track the fish’s wakes. As each individual fish peels off during its furtive attempts to flee the approaching hunter, curls of icy water are left behind as tiny trails. The seal effortlessly changes its heading again as she tracks the wakes trailing the fleeing fish. As she makes her final approach to the school, she randomly chooses to follow a single wake. While the visual image created by the school may mask the

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presence of any individual fish, the wake leads the seal right to its intended prey. The seal’s whiskers, its deadly tracking organ, are creating a hydrodynamic landscape with this singular wake serving as a beacon leading the hunter straight to its victim. The seal, reading this map, uses its right front flipper to make one last correction to its direction and opens its mouth in preparation for the final capture. The final moments are a blur as the cod makes one last mad dash. In doing so, the prey creates an enormous wake which alerts the seal of its sudden movement. She turns her body to the right to counteract this escape maneuver and sinks her teeth deep into the sides of the cod. As she closes her mouth, the hunt ends, and the successful seal swims off to consume her meal on shore.

38.2  The Science of Sensing Wakes The definition of a wake, a disturbance in the flow, is fairly ambiguous. Yet despite this ambiguity, wakes behind moving boats, ships, or even swimming fish are well-­ studied topic. As an object moves through water (or as water moves around an object), the flow patterns in the water are interrupted, and the exact way that they are interrupted is based on the shape of the object. The interaction between water and the object is based solidly in physics, and the power of physics to influence biology is readily apparent by examining the shape of fish. Boats and fish tend to be streamlined in their shape because this reduces the amount of energy needed to move through water. Except for a few outliers, most fish have the same type of shape which is called streamlined. Fish are pointed at the front, widen to where their eyes are located, and then gently taper off toward the tail. As fish swim, they generate the greatest force by moving their caudal tail to the left and then the right. During this sideways motion, water is shed off the tail differently as the fish moves the tail to the right and then the left. If the fish turns to the right, the animal produces more force on its rightward tail swing and vice versa. The shedding of water produces vortices which are circular rings of water movement whose size and intensity depend upon the force of the movement of the fish’s tail. An easy way to visualize this is to imagine any car commercial where the vehicle moves through fog or smoke. After the car passes out of camera range, circular rings of cloud or smoke are left behind. These are the vorticities of the wake produced by the car, in other words, the ghostly footprint indicating that a car was just here. In the air, the smoke rings dissipate quite quickly, but in the waters inhabited by the harbor seal, they persist. This persistence, which can be tens of meters in length and last several minutes, produces a watery trail that the seal can track in any direction. The harbor seal, as well as other pinnipeds, have a wonderful set of sensory structures near the tip of their nose. These sense organs are their whiskers (vibrissae), and, as their technical name alludes to, they are sensitive to vibrations in their environment. These vibrations are significantly different than the type of vibrations discussed in the chapters in the tactile section of the book. These aquatic vibrations are the differential movement of water due to the wakes that fish produce when they

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swim. Pinnipeds actually have three locations for vibrissae: near the nose, on the eyes, and on their snout. The number range from a measly 15 on Ross seals to the overwhelming 350 on the mustached walrus. Harbor seals have approximately 5 near their eyes (supraorbital), a lonely 1 in their nose (rhinal), and the vast majority, over 40, on their snout (mystacial). The placement of these vibrissae around the face of the harbor seal allows a wide sensory array over which to measure differences in flow patterns. The wide spread of vibrissae occurs laterally across the face of the seal as well as vertically. This is important because the vorticities created by the escaping fish are spatial signals. The seal doesn’t care that much of the signal changes over time but needs the spatial information to determine the direction where the fish is headed. The seal compares the intensity of the hydrodynamic disturbance across its various facial vibrissae and extracts directional information from the intensity differences. In the example above describing the fish swimming, the fish needs to generate more force on the right side of its caudal fin to turn right. The trailing seal can detect these side to side differences and quickly alters its swimming direction to intercept the fish. This spatial dimension is in contrast to the sense of smell. Chemoreception is a temporal signal as information is extracted about our odorous world based on the changes in signal intensity over time. As such, the two nares of vertebrate noses effectively sample approximately the same air. For the harbor seal, the long vibrissae on the right side of its face are in a different wake than the vibrissae on the other side of its face (Fig. 38.1).

Fig. 38.1  The seal’s whiskers. Many marine mammals have whiskers that are located all around their mouth, cheeks, eyes, and face. These whiskers are sensitive to curling water currents known as wakes. As their prey (fish) swim forward, they create wakes of different sizes depending on which direction the prey are turning. The seals can detect these small differences to hunt down their prey

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The harbor seal, as well as other pinnipeds, has such a great sense of wake detection that even blindfolded, the animals can follow miniature submarines in a laboratory setting. There are even reports of blind harbor seals, in the field, being found well-fed and in great health. All the hunters covered in the visual section of the book would perish quite quickly if they lost their senses of vision. The structure of the vibrissae is equally as impressive. By visually examining vibrissae, it could be concluded that these are just extended hairs of solid keratin. Yet, inside each vibrissa is a complex series of layers that provide protection for the neurons located in the middle of the hair. The unique structural properties of these layers allow the vibrissae to bend and react differently to water flow. Located in the heart of the oval-shaped vibrissae are a set of neurons that provide the sensory function for the whisker. Surrounding the neurons are cavities for blood flow, sheathes of material that provide protection against abrasion as well as mechanical properties for bending appropriately to flow, and an outer dermal capsule that covers the vibrissae. Each of the 40 vibrissae on the snout of the harbor seal has over 1000 axons arising from the nerve cells. This vast innervation is three to four times the number of axons found within the highly sensitive whiskers of rats. How all this innervation carries its information to the central nervous system of the seal is still unknown. The rarity, size, and habitat of the harbor seal make these types of studies hard to carry out. Yet, from a behavioral perspective, much is known about the seal’s ability to use this sensory system to gather information about its environment. Harbor seals can detect and discriminate the size and shape of objects simply by running their whiskers over an object. This ability is akin to feeling an object with your hand to determine its shape. This fine-scale discrimination is why seals and sea lions are so efficient at balancing balls on their snouts in aquariums. Their whiskers provide direct and detailed information about the weight, size, and movement of the ball with as much detail as humans would have when carrying a ball in their hands. The speed of this processing matches that of the animals visual processing, so their vibrissae are really capturing a mechanical picture of their world. Harbor seals are unlikely to balance rocks in the wild, but their ability to detect differences in water currents is just as impressive. With sensitivities of water velocities down to the microns per second, harbor seals have very little difficulty in following much larger prey and larger wakes in the field. The complex sensory organ that is the vibrissae of the harbor seals is an incredible piece of evolutionary adaptation. Their sensitivity to disturbances in flow essentially provides them with underwater hands and eyes that allow them to go with the flow.

Chapter 39

The Uncharted World

To see the unseen and to hear the unspoken; most often the concepts of extrasensory perception contain lots of drivel about activating the third eye or some other mystical nonsense. We have our senses and those senses created reality. Yet, as this section has touched upon, there is far more to this world than what we can perceive. There are wonderful sensory landscapes that exist for many other animals where we blithely, and ignorantly, travel. At the largest scales, the world has fields that guide animal movement across the entire globe. To tap into a stimulus energy this massive seems to be quite an improbable task, but organisms as small as bacteria surf the world’s magnetic field. At the smallest of scales, tiny electrical currents are used to send messages about individual identity and reproductive readiness. Thinking about these types of stimuli draws my mind to some Star Wars fantasy. Within this fictional universe, the famous Jedi knights can sense and tap into an unseen stimulus called the Force. The more honorable knights use the Force to move objects by simply concentrating on them. This is not unlike the Marvel villain, Magneto, who uses the Earth’s magnetic field to move and control metal. The evil Jedi knights can develop the ability to shoot electricity out of their fingers which is eerily similar to what electric eels do to their own prey. In reality, these heroes and villains are not demonstrating any more sophisticated abilities than animals. Yet, having these abilities would definitely open up a new world and alter one’s perception of nature. Beyond the fantasy concepts, I can imagine how useful these sensory abilities could be within human society. I can easily imagine wonderful applications in the construction trades. Simply running one’s hand over a wall could provide useful information to electricians rewiring rooms. Walking along an area and detecting underground power lines would be important before beginning a dig. The importance of thermal detection within military operations is so great that heat vision goggles are fairly commonplace. Maybe firefighters could use a similar sense to detect unattended fires before they light up an entire forest or to locate critical hotspots within a burning house. If pilot (and their planes) had the ability to detect the fine-scale flow structures ahead of the aircraft, they might be able to avoid the © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_39

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more dangerous turbulence during flights. The common thread to all these ideas is that there is a sensory world that exists outside of our seeing, hearing, smelling, tasting, and touching. This world is the illusive world that organisms have evolved to take advantage of and that we ignore. Given the possibility of life on distant planets, even more fantastical senses could exist. On this planet, there exist animals that have never been seen or categorized, and they may hold secrets on how they perceive their world. The list of animals that can sense electrical signals is growing tremendously fast as well as those that are sensitive to magnetic fields. Interestingly, it is our inability to ask animals the right questions that often leads to our ignorance on their perceptual abilities. If you never test an animal’s ability to sense heat, electricity, or flow, you’ll never find out if they can. As our concepts of what a stimulus is expand, so too does our discoveries of animal’s capabilities. Here, on the edge of scientific discovery, is where the interplay between the science fiction and science may provide insight. Fantasy worlds contain organisms beyond belief, that is, until we discover a new animal on Earth. Turning to the creative minds of authors and artists could expand the repertoire of questions that a scientist is willing to ask of our animal companions. This, in turn, could then lead to technological advancement such as thermal vision or advance fire warning systems. Even within this section of the book, the handpicked examples of different sensory systems have left thousands of other examples out. Many animals have the ability to detect thunder or earthquakes before they occur, and others can identify the scratching sounds of insects buried deep within the trunk of a tree. Density gradients within the ocean, temperature differences in lakes, and inclines on hills are all source of stimuli for animals as they move, hunt, and reproduce. This section, and even the entire book, barely scratches the surface on the amazing perceptual abilities of animals. If something exists, there is an animal that can sense it.

Part VIII

The Illusive World

There are things known and there are things unknown, and in between are the doors of perception. —Aldous Huxley

Chapter 40

The Illusive World

The world is a lie, at least according to what I tell my students in my sensory ecology class. What we believe to be the world, the one we perceive with our senses, is at best an incomplete version of reality. Our limited sensory capability, coupled with the perceptual biases and filtering of the neural networks in our brain, constructs a world that really isn’t there. Yet, it is there for me, and I believe that everything I sense to be the truth. Every story in this book has demonstrated that this truth is a pale comparison to an unbiased reality. When I see a red rose, insects do not. When I bend to smell its fragrance, the aroma is not the same for mice. When I prick my finger on its thorn, the fox feels something different. In essence, the fox, mice, and insects live in different worlds than I do. At the start of this book, I attempt to explain these concepts of different worlds. I also presented several questions pertaining to reality and our ability to understand what it means to be another organism. So maybe I should answer those questions. (I recently read a book on the analysis of big data, and one of the more surprising results was that a full 90% of readers do not finish the book that they are reading. This means that very few last chapters will impact the few readers that are brave enough to finish that last part of a book. Despite that low percentage, I feel it is my duty as the author to finish the book, answer some questions, and perhaps provide a little insight into the thoughts that their book hopefully provoked within the readers mind.) So, for those few that have made it this far, I think it is time to answer some of those questions that were started back in Chap. 1.

40.1  What Is Reality? Reality, in one way, is a deep and philosophical concept that has troubled thinkers for thousands of years. In another way, the technology arising from physics, engineering, and material science provides some really good answers into the fundamental nature of reality. Like many complex and deep questions, the right answer © Springer Nature Switzerland AG 2019 P. A. Moore, Into the Illusive World, https://doi.org/10.1007/978-3-030-20202-6_40

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depends on what is meant by the question. In Douglas Adam’s Hitchhiker series, the answer to the meaning of life, provided by a planet-sized computer after millennia of consideration, was 42. It turns out that the questioners had asked the computer the wrong question. For our question, a simple and probably unsatisfying answer would be reality is whatever you perceive it to be. This is unsatisfying because I could have stated this answer in Chap. 1 and be done with the book. The book would have been a quick read. This answer, lack of satisfaction notwithstanding, might be the most correct one because we think and act on what we perceive to be reality whether this matches some absolute or even someone else’s reality. Thus, we construct our own version of reality from our perceptions and act accordingly. The unsatisfactory nature of the answer arises because of our sociality and the consequences of our actions are played out in an “absolute” reality. If my version of reality comes into conflict with your version of reality, problems arise. In addition, if my version of reality (such as eating 15 bars of chocolate a day is healthy) comes into conflict with any “absolute” reality, problems arise. So, maybe we’ll put a pin in this answer and look for a deeper one. To find enlightened answers to complex questions, at least any really good questions, one needs a starting point. Usually, the starting point is an assumption or definition. Given the many different layered aspects of the question, “What is reality?”, a good assumption almost seems like a prerequisite. Within the sciences, we have to make a fundamental assumption about the world around us. That assumption is that a singular reality exists and there is potential to detect and measure that reality. Without this basic assumption, a philosophical wild west is created where anything goes. Within this wild west, science becomes just one of many ways to answer questions about the natural world. Want to know how a neuron works? Read some tea leaves, roll some bones, or stare at the stars because there are always more than one single answer for the neuron question. While some might doubt the importance of science, we can check that doubt by simply asking people if they would rather fly in a plane built by an engineer trained in physics and material science or a witch doctor reading messages in a fire. So, point 1 is that a reality exists, and with the development of the right technology, we can measure it. Even if this reality exists, how do we, as faulty thinking machines, know that the “absolute” reality exists? The answer, and the purpose of this book, is through our senses. Our senses are the only window through which our brain has access to any reality. Without that window, we are just a brain with nothing to think about. That is probably the definition of a zombie, a brain with no senses. Our senses provide information, experiences, and, by definition, sensations for our brain to learn, grow, think, and reject. Without our sensory window, as biased and faulty as it is, the brain starves and regresses. As such, our senses make us who we are. They form our memories. They form our experiences. They form the sensations that provide us feedback on our behavior. If I reach out and touch a hot stove, it is my sense of heat and pain that allows me to learn. Without my senses, I continue to touch the stove and wonder why my hand is turning to ash. The original and unsatisfying answer about reality, whatever you perceive it to be, now has an added element: feedback. I can believe, and hence perceive, the stove as not dangerous, but the singular reality

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provides me feedback to alter my perception. Thus, the dissonance between my perception of reality and the testing of that reality through action allows me to update my view of reality, if I choose to use that feedback. Through our senses and through the feedback that reality provides me through our senses, I construct a reality. Thus, my “whatever I perceive it to be” is constrained or tested against the singular reality. Reality is, then, an interplay between the sensory window of the world and my processing of that world with my brain. In the section on vision, I stated that we see the world as much with our brain as we do with our eyes. This statement is also true for the construction of reality. I make a reality with my senses and my brain and then test this version of reality. This addition to the original answer makes a more fluid and complex answer but doesn’t fully solve the problem of multiple, subjective realities that arises from the “whatever I perceive it to be.” With the recent advances in understanding how the human brain works, we now understand more how poorly the brain is constructed to interface with reality. With cognitive biases, faulty memories, irrational thinking, and perceptual biases, it is surprising that humans are able to construct any functional version of reality. We do have a set of skills that helps us work around these biases. The first set is the recognition that these biases exist and need correcting. The second set is our ability to communicate. Imagine a crime scene or perhaps an auto accident. Both drivers are physically fine, but their cars have some significant damage. Each driver would like to have the other driver blamed so that the other driver’s insurance will pay for the repairs. As the police arrive to the scene of the accident, the physical evidence doesn’t provide clarity on which driver is at fault. The physical evidence is, at best, ambiguous. The police need to find the singular reality of what happened in order to correctly assess fault. When the officers interview the first driver (Joe), Joe spins a tail of attempting to turn and that the other driver came out of nowhere. This is reality for Joe. He fully believes his version because he experienced the crash firsthand. Through Joe’s biased senses, he could see the other car not giving him the right of way. Joe recalls, using his faulty memory, the exact details of the incident. The police officer carefully writes down all the details that Joe provides. In talking to the second driver (Olga), amazingly, the police hear the exact same story except that the right of way has been switched. Olga tells her story as if she were in the right. Now, the police are stuck. They have two accounts of the accident except the fault has been reversed. They need to find further evidence of reality. So, being dutiful officers, they interview all the witnesses that are still standing around on the sidewalks. Incredibly, there are 26 witnesses, and each witness gives a slightly different version of the events from every other witness and the two drivers. The officers understand that there is only a singular reality but have 28 different versions of the event. The officers, serving as our questioning mind, should examine each of the versions and look for commonalities. If the same set of events has occurred and been reported across a number of different biased perspectives, the officers know that those common events are probably closer to reality than those events that appear in only single stories. Notice the phrase, closer to reality in the previous sentence. The maddening part of our biased senses and fallible brain is that we will never know for

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certain what that reality is. By interviewing and engaging with as many different perspectives as possible, we can get close, close but no cigar used to be the phrase.

40.2  Walk a Mile in Someone’s….Brain? Now, after laying down the foundation on a concept of reality, we can begin to answer Thomas Nagel’s question on “What it is like to be a bat?” First, though, I would like to focus Nagel’s question on humans. Can we really know what it is like to be someone else? It would seem that the answer to this falls in line with a Zen-­ like concept, yes and no. Supporting the no answer is the idea that each of us is genetically distinct which creates subtle but important differences in our sensory capabilities. Color-blind individuals certainly view the world differently than those without it. Deaf or hearing-impaired people have a unique sensory landscape when compared to those without those deficits. These differences, one could argue, are neither worse nor better but create a distinct window to the world for the brain. The interpretation of these windows is also filtered and changed by the experiences lived by individuals. Each of us has a set of unique experiences from childhood to adulthood that have shaped our cognitive biases and values. These biases and values are the basis from which we create meaning from the signals perceived in our sensory landscapes. As the biases change, so too does the meaning that is created from the perception of the world. Thus, the variation in our sensory perceptions coupled with our highly tuned cognitive biases seems to create a distinctive version of reality. It seems that the answer is a resounding no to Nagel’s question and to our own ability to understand another human’s perspective. Yet, a large majority of people laugh at the same jokes, cry during the same tragedy, and are scared by many of the same fears. If we can’t know what it is like to be someone else or, at least, share common experiences, then it would seem a large number of human constructs fall apart. Entire fields of sociology, philosophy, medicine, and even the humanities require an ability to understand what someone else is thinking or experiencing. How can someone create art if the experience of the audience member is unknown? How can a therapist help an individual if they cannot get inside of their mind to see what is happening? How can a mentalist be a mentalist without reading other people’s minds? Maybe here, the police approach can help us. Engaging with mindsets and perspectives that are different from our own gives us the ability to project a little bit into the other person’s world. Shared experiences of birthdays and deaths, health and illness, may allow us some insight into the reality created by a different set of perceptions and sensory capabilities. So, the second part of the Zen answer is yes; we can get close to understanding what it is like to be another person. We have a similar sensory landscape and similar sensory tools from which we construct our realities. The subjective experiences of sensory perception are different across all of humanity. Each of us uses those sensory experiences to construct our own version

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of reality. Maybe, just maybe, some of the shared experiences and our ability to communicate about those shared experiences allow us to partially understand the reality of another individual. Thus, we might safely conclude it is possible to know what it is like to be another human. Is it possible to move beyond the human experience? Can we answer Nagel’s question on “What’s it like to be a bat?” with a yes?

40.3  To Be or Not to Be… Throughout this book, I have introduced stories on how animals use their senses to perform a host of different behaviors that we often perform using our eyes and ears. Whether this is hunting for food with feet or tentacles, responding to lover’s calls with legs or noses, or avoiding predators by jamming radars, animals have some amazing capabilities. It would seem that these subjective experiences are so disparate from our own that it would be impossible to understand what their cognitive state is like. Yet, for those animals that serve as our companions, maybe those distinctions and differences aren’t so great. As a dog sniffs the grass, I wonder if that experience is fundamentally any different than smelling a bouquet of flowers or even sniffing leftovers to tell if they are still good enough to eat. As a cat nudges a hand to be petted, is this any different than the relaxing sensation of a deep muscle massage? Just as we can extend our own sensory experiences to understand that of another human, I see little distinction in continuing that extension to our closest animal friends. Although we may touch or hear with different appendages, information is carried in signals produced by these appendages, and the brains that receive those signals, whether human or other animal, need to extract meaningful information. These animals are using different senses in an attempt to reconstruct the same reality that we all live under. Certainly, these animals have nervous systems that filter information in different ways, but the extraction of information critical to survival is the same. Senses are the brain’s window to the world, but all animals, including humans, have similar basic needs. These are to eat, to not be eaten, to find shelter, to find mates, and to have in- and out-groups within a society. A bat reconstructs a three-­ dimensional world using sonar, whereas other animals use visual cues. It is, ultimately, the same three-dimensional world, although one has sound-reflecting surfaces and the other has light-reflecting surfaces. Food, whether tasted with feet, tongues, bodies, or intestines, is measured for calories (sweet) and poison (bitter). As our understanding of how animals sense the world increases through scientific exploration, we will be able to assemble more complete models of an animal’s perceptual world. Combining molecular, cellular, and physiological work with behavioral, ecological, and evolutionary studies provides a detailed understanding not only of how a sensory system works but how the animal uses those senses and perceptions to survive and reproduce. When Nagel wrote his famous essay in 1974, neuroscience was still a young field, and the recording of neurons only had occurred two decades previously. In the half century since that essay, our understanding on

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how animal’s minds work has blossomed almost to the point where we can build robots that act just like real animals. In addition, the technological advances have further increased our understanding of an animal’s perceptual abilities. In a previous chapter, I mentioned the creation of thermal vision. Heat-sensing eye pieces are now readily available for anyone with the money to purchase them. Once done, you can have thermal vision just like a pit viper. Camera filters allow us to photograph flowers in the same way that bees see them, and eyeglasses with polarized lenses would allow us to navigate deserts in the same way as ants. Our underwater vessels are equipped with sonar, and as a result, the soundscape of the undersea world of dolphins is perceptible. It would seem that advances in our scientific understanding of an animal’s senses and the ability to replicate those senses with technology would open the door to understanding the conscious experience of other animals. Science fiction is a genre of writing that both entertains as well as attempts to predict the future world. A quick glance across the entire genre reveals an amazing ability of these authors to predict advances in technology. In 1888, Edward Bellamy wrote about little cards that carried credit for people to make purchases, and Hugo Gernsback created video calls in 1911. From Dick Tracy’s smart watch, Star Trek’s communicators, and Philip K. Dick’s mood-enhancing technology, science fiction either predicts or influences the development of human society. In the James Cameron 2009 movie Avatar, the characters could experience the sensory landscape of an alien being as their minds were temporarily transplanted into the body of an alien. The characters’ minds could register all of the sensory feedback including some additional senses that humans don’t have. While I am not a science fiction writer, I think that there will be a time where we will know what it is like to be a bat, an octopus, an osprey, or any other animal covered in this book and that may be by hijacking the brain of those animals.

40.4  One Final Plea Before that day arrives, when we’ll be able to experience the world as our favorite animal, it is my hope that this book, and the stories contained within it, has provided both some enjoyment and wonder and enlightenment about the creatures that we share this planet with. To recognize that seeing is not believing and that we cannot hear all that is worth hearing brings about a little humility in regard to our interactions with nature. It is not a secret that humans, and all our various activities, are altering the world in dramatic ways. Apart from the more obvious toxic chemicals that we dump into oceans and the climate that we alter, human activities are significantly changing the sensory landscape for animals. As with most of our interactions with the natural world, that change doesn’t bode well for nature. A surprisingly underappreciated type of pollution is sensory pollution. As we light our beachfront houses, the nesting sea turtles turn away from the ocean and walk toward the light to their death. As we increasingly fragment habitats with roads, we create vehicle

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traffic that produces noise pollution. The effect of this pollution on songbirds is incredible. Traffic noise changes the types of songs birds sing as well as their ability to perceive those songs. The songs are used to build and guard territories as well as attract mates, and we are changing the bird’s abilities to do these activities. We drill in the oceans and create boat traffic which alters the soundscape for aquatic fish and mammals. Finally, chemicals we release into the air and water can alter the smell and taste receptors of organisms. Without the ability to sense their chemical world, these animals will starve and die. Maybe this is the saving grace to the overarching question on whether we can understand the conscious experiences of animals. Regardless of the answer, our attempt to find out will help us understand how animals perceive their world and how our actions alter that perception. Even if we can’t understand what it is like to be an animal, maybe we can understand how we impact their perception and their behavior. If so, maybe these stories aren’t about how animals perceive their world but are lessons on how we negatively impact that perception. These lessons, if applied, might allow us to see a different reality and make that reality a little less noisy and a lot more natural.

Further Reading1

Part I: The Sensuous World Barlow RB, Hitt JM, Dodge FA (2001) Limulus vision in the marine environment. Biol Bull 200(2):169–176 Chabris C, Simons D (2010) The invisible gorilla: and other ways our intuitions deceive us. Harmony, New York Nagel T (1974) What is it like to be a bat? Philos Rev 83(4):435–450 Panksepp J (2004) Affective neuroscience: the foundations of human and animal emotions. Oxford University Press, Oxford Patriquin KJ, Hogberg LK, Chruszcz BJ, Barclay RM (2003) The influence of habitat structure on the ability to detect ultrasound using bat detectors. Wildlife Soc Bull 31:475–481 Thorndike E (2017) Animal intelligence: experimental studies. Routledge, New York (First published in 1999) Von Uexküll J (2013) A foray into the worlds of animals and humans: with a theory of meaning, vol 12. University of Minnesota Press, Minneapolis, MN (Originally published in 1934) Wald G, Brown PK (1965) Human color vision and color blindness. Cold Spring Harb Symp Quant Biol 30:345–361

Part II: Vision Andel D, Wehner R (2004) Path integration in desert ants, Cataglyphis: how to make a homing ant run away from home. Proc R Soc Lond B Biol Sci 271(1547):1485–1489 Braekevelt CR, Smith SA, Smith BJ (1996) Fine structure of the retinal photoreceptors of the barred owl (Strix varia). Histol Histopathol 11(1):79–88  The information in this book would not be possible with the hard work, dedication, and peerreviewed writing of numerous scientists. I have tried to capture most of the work that has influence my thinking and writing on the senses of animals in this section. Each chapter is a synthesis of over a dozen sources and I have chosen not to include such a large number of papers and books. Consequently, I have only included two or three fundamental references for each chapter. So, this list of readings is not an exhaustive list. 1

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Cronin TW (2012) Visual optics: accommodation in a splash. Curr Biol 22(20):R871–R873 Cronin TW, Marshall NJ, Caldwell RL (1996) Visual pigment diversity in two genera of mantis shrimps implies rapid evolution (Crustacea; Stomatopoda). J Comp Physiol A 179(3):371–384 Cronin TW, Johnsen S, Marshall NJ, Warrant EJ (2014) Visual ecology. Princeton University Press, Princeton, NJ Douglas R, Djamgoz M (2012) The visual system of fish. Springer, New York Jones MP, Pierce KE Jr, Ward D (2007) Avian vision: a review of form and function with special consideration to birds of prey. J Exotic Pet Med 16(2):69–87 Kevan PG, Chittka L, Dyer AG (2001) Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. J Exp Biol 204(14):2571–2580 Lisney TJ, Iwaniuk AN, Bandet MV, Wylie DR (2012) Eye shape and retinal topography in owls (Aves: Strigiformes). Brain Behav Evol 79(4):218–236 Menzel R, Backhaus W (1989) Color vision honey bees: phenomena and physiological mechanisms. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin, pp 281–297 Sivak JG (1976) Optics of the eye of the “four-eyed fish” (Anableps anableps). Vis Res 16(5):531–534 Thoen HH, How MJ, Chiou TH, Marshall J  (2014) A different form of color vision in mantis shrimp. Science 343(6169):411–413 Wehner R, Räber F (1979) Visual spatial memory in desert ants, Cataglyphis bicolor (Hymenoptera: Formicidae). Experientia 35(12):1569–1571

Part III: Audition Au WW, Pack AA, Lammers MO, Herman LM, Deakos MH, Andrews K (2006) Acoustic properties of humpback whale songs. J Acoust Soc Am 120(2):1103–1110 Boyle KS, Tricas TC (2010) Pulse sound generation, anterior swim bladder buckling and associated muscle activity in the pyramid butterflyfish, Hemitaurichthys polylepis. J  Exp Biol 213(22):3881–3893 Corcoran AJ, Barber JR, Conner WE (2009) Tiger moth jams bat sonar. Science 325(5938):325–327 Fine ML, Parmentier E (2015) Mechanisms of fish sound production. In: Ladich F (ed) Sound communication in fishes. Springer, Vienna, pp 77–126 Hristov NI, Conner WE (2005) Sound strategy: acoustic aposematism in the bat–tiger moth arms race. Naturwissenschaften 92(4):164–169 Khan S, Chang R (2013) Anatomy of the vestibular system: a review. NeuroRehabilitation 32(3):437–443 Ladich F (2004) Sound production and acoustic communication. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fish. Springer, Dordrecht, pp 210–230 Langbauer WR Jr (2000) Elephant communication. Zoo Biol 19(5):425–445 Nelson MD, Koenig CC, Coleman FC, Mann DA (2011) Sound production of red grouper Epinephelus morio on the West Florida Shelf. Aquat Biol 12(2):97–108 O’Connell-Rodwell CE (2007) Keeping an “ear” to the ground: seismic communication in elephants. Physiology 22(4):287–294 Parmentier E, Boyle KS, Berten L, Brié C, Lecchini D (2011) Sound production and mechanism in Heniochus chrysostomus (Chaetodontidae). J Exp Biol 214(16):2702–2708 Payne KB, Langbauer WR, Thomas EM (1986) Infrasonic calls of the Asian elephant (Elephas maximus). Behav Ecol Sociobiol 18(4):297–301 Schärer MT, Rowell TJ, Nemeth MI, Appeldoorn RS (2012) Sound production associated with reproductive behavior of Nassau grouper Epinephelus striatus at spawning aggregations. Endanger Species Res 19(1):29–38

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Seikel JA, King DW, Drumright DG (2009) Anatomy & physiology for speech, language, and hearing. Cengage Learning, New York Yamato M, Ketten DR, Arruda J, Cramer S, Moore K (2012) The auditory anatomy of the minke whale (Balaenoptera acutorostrata): a potential fatty sound reception pathway in a baleen whale. Anat Rec Adv Integr Anat Evol Biol 295(6):991–998

Part IV: Olfaction Breithaupt T (2010) Chemical communication in crayfish. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 257–276 Dittman A, Quinn T (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199(1):83–91 Gemeno C, Yeargan KV, Haynes KF (2000) Aggressive chemical mimicry by the bolas spider Mastophora hutchinsoni: identification and quantification of a major prey’s sex pheromone components in the spider’s volatile emissions. J Chem Ecol 26(5):1235–1243 Harari AR, Sharon R (2017) Chemical communication. In: Gordon R, Seckbach J  (eds) Biocommunication: sign-mediated interactions between cells and organisms. WSPC, Berlin, pp 229–256 Haynes KF, Gemeno C, Yeargan KV, Millar JG, Johnson KM (2002) Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey? Chemoecology 12(2):99–105 Krasnec MO, Breed MD (2013) Colony-specific cuticular hydrocarbon profile in Formica argentea ants. J Chem Ecol 39(1):59–66 Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc Lond B Biol Sci 275(1640):1271–1278 Mokkonen M, Lindstedt C (2016) The evolutionary ecology of deception. Biol Rev 91(4):1020–1035 Moore PA (2016) The hidden power of smell. How chemicals influence our lives and behavior. Springer International Publishing, New York Moore PA, Bergman DA (2005) The smell of success and failure: the role of intrinsic and extrinsic chemical signals on the social behavior of crayfish. Integr Comp Biol 45(4):650–657 Pekár S, Toft S (2015) Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol Rev 90(3):744–761 Quinn TP (2018) The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle, WA Schneider RAZ, Huber R, Moore PA (2001) Individual and status recognition in the crayfish, Orconectes rusticus: the effects of urine release on fight dynamics. Behaviour 138(2):137–153 Strasser B, Gostner JM, Fuchs D (2016) Mood, food, and cognition: role of tryptophan and serotonin. Curr Opin Clin Nutr Metab Care 19(1):55–61 Tyson JJ, Alexander KA, Manoranjan VS, Murray JD (1989) Spiral waves of cyclic AMP in a model of slime mold aggregation. Phys D Nonlinear Phenom 34(1-2):193–207 Ueda H (2016) Physiological mechanisms of imprinting and homing migration of Pacific Salmon. Aqua-Biosci Monogr ABSM 9(1):1–27 Vickers NJ, Baker TC (1996) Latencies of behavioral response to interception of filaments of sex pheromone and clean air influence flight track shape in Heliothis virescens (F.) males. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 178(6):831–847 Vickers NJ, Baker TC (1997) Flight of Heliothis virescens males in the field in response to sex pheromone. Physiol Entomol 22(3):277–285

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Part V: Gustation Atema J (1971) Structures and functions of the sense of taste in the catfish (Ictalurus natalis). Brain Behav Evol 4(4):273–294 Caprio J, Brand JG, Teeter JH, Valentincic T, Kalinoski DL, Kohbara J, Kumazawa T, Wegert S (1993) The taste system of the channel catfish: from biophysics to behavior. Trends Neurosci 16(5):192–197 Dethier VG (1968) Chemosensory input and taste discrimination in the blowfly. Science 161(3839):389–391 Dethier VG (1976) The hungry fly: a physiological study of the behavior associated with feeding. Harvard University Press, Harvard, MA Dethier V (2012) To know a fly. Literary Licensing, LLC, Whitefish, MT, USA (Originally publish in 1962) Filoramo NI, Schwenk K (2009) The mechanism of chemical delivery to the vomeronasal organs in squamate reptiles: a comparative morphological approach. J Exp Zool A Ecol Genet Physiol 311(1):20–34 Gu Q, Joe D, Gilbert C, Gabriel S (2016) Activation of bitter taste receptors in rat pulmonary sensory neurons augments capsaicin-evoked TRPV1 responses. FASEB J 30(1):772–772 Halpern M (1992) Nasal chemical senses in reptiles. Biol Reptilia 18:423–523 Kohl KD, Stengel A, Dearing MD (2016) Inoculation of tannin-degrading bacteria into novel hosts increases performance on tannin-rich diets. Environ Microbiol 18(6):1720–1729 Rozengurt E (2006) Taste receptors in the gastrointestinal tract. I.  Bitter taste receptors and α-gustducin in the mammalian gut. Am J Physiol Gastrointest Liver Physiol 291(2):G171–G177 Schwenk K (1994) Why snakes have forked tongues. Science 263(5153):1573–1577 Schwenk K (1995) Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol Evol 10(1):7–12 Villanueva R, Perricone V, Fiorito G (2017) Cephalopods as predators: a short journey among behavioral flexibilities, adaptions, and feeding habits. Front Physiol 8:598 Wells MJ (1963) Taste by touch: some experiments with Octopus. J Exp Biol 40(1):187–193 Wells MJ, Freeman NH, Ashburner M (1965) Some experiments on the chemotactile sense of octopuses. J Exp Biol 43(3):553–563 Witt M, Reutter K (2015) Anatomy of the tongue and taste buds. In: Doty R (ed) Handbook of olfaction and gustation, 3rd edn. Wiley, Hoboken, N.J, pp 637–663

Part VI: Tactile Gordon SD, Uetz GW (2011) Multimodal communication of wolf spiders on different substrates: evidence for behavioural plasticity. Anim Behav 81(2):367–375 Heth G, Frankenberg E, Pratt H, Nevo E (1991) Seismic communication in the blind subterranean mole-rat: patterns of head thumping and of their detection in the Spalax ehrenbergi superspecies in Israel. J Zool 224(4):633–638 Hölldobler B (1999) Multimodal signals in ant communication. J  Comp Physiol A Neuroethol Sens Neural Behav Physiol 184(2):129–141 Hu DL, Chan B, Bush JW (2003) The hydrodynamics of water strider locomotion. Nature 424(6949):663 Krausa K, Hager FA, Kiatoko N, Kirchner WH (2017) Vibrational signals of African stingless bees. Insect Soc 64(3):415–424 Nevo E, Heth G, Pratt H (1991) Seismic communication in a blind subterranean mammal: a major somatosensory mechanism in adaptive evolution underground. Proc Natl Acad Sci 88(4):1256–1260

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Pielström S, Roces F (2012) Vibrational communication in the spatial organization of collective digging in the leaf-cutting ant Atta vollenweideri. Anim Behav 84(4):743–752 Roces F, Tautz J, Hölldobler B (1993) Stridulation in leaf-cutting ants. Naturwissenschaften 80(11):521–524 Römer H (2018) Acoustic communication. In: Córdoba-Aguilar A, González-Tokman D, González-Santoyo I (eds) Insect behavior: from mechanisms to ecological and evolutionary consequences. Oxford University Press, Oxford, pp 174–188 Rovner JS, Barth FG (1981) Vibratory communication through living plants by a tropical wandering spider. Science 214(4519):464–466 Schleich C, Francescoli G (2018) Three decades of subterranean acoustic communication studies. In: Dent M, Fay R, Popper A (eds) Rodent bioacoustics, Springer handbook of auditory research, vol 67. Springer, Cham Schürch R, Ratnieks FL, Samuelson EE, Couvillon MJ (2016) Dancing to her own beat: honey bee foragers communicate via individually calibrated waggle dances. J Exp Biol 219(9):1287–1289 Von Frisch K (2014) The dance language and orientation of bees. Harvard University Press, Harvard, MA (Originally published in 1967) Wilcox RS (1988) Surface wave reception in invertebrates and vertebrates. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York Wilcox RS (1995) Ripple communication in aquatic and semiaquatic insects. Ecoscience 2(2):109–115 Young SL, Chyasnavichyus M, Barth FG, Zlotnikov I, Politi Y, Tsukruk VV (2016) Micromechanical properties of strain-sensitive lyriform organs of a wandering spider (Cupiennius salei). Acta Biomater 41:40–51

Part VII: Other Senses Atema J, Fay RR, Popper AN, Tavolga WN (eds) (1987) Sensory biology of aquatic animals. Springer, New York Chen Q, Liu Y, Brauth SE, Fang G, Tang Y (2017) The thermal background determines how the infrared and visual systems interact in pit vipers. J Exp Biol 220(17):3103–3109 Dehnhardt G, Mauck B, Hanke W, Bleckmann H (2001) Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 293(5527):102–104 Denny MW (1993) Air and water: the biology and physics of life’s media. Princeton University Press, Princeton, NJ Hanke W, Dehnhardt G (2016) Vibrissal touch in pinnipeds. In: Scholarpedia of touch. Atlantis Press, Paris, pp 125–139 Hanke W, Witte M, Miersch L, Brede M, Oeffner J, Michael M, Hanke F, Leder A, Dehnhardt G (2010) Harbor seal vibrissa morphology suppresses vortex-induced vibrations. J Exp Biol 213(15):2665–2672 Jørgensen JM (2005) Morphology of electroreceptive sensory organs. In: Electroreception. Springer, New York, pp 47–67 Knight K (2018) How pit vipers see (infra) red. J Exp Biol 221(17):jeb188870 Lohmann KJ, Cain SD, Dodge SA, Lohmann CM (2001) Regional magnetic fields as navigational markers for sea turtles. Science 294(5541):364–366 Lohmann KJ, Lohmann CM, Endres CS (2008) The sensory ecology of ocean navigation. J Exp Biol 211(11):1719–1728 Lohmann KJ, Putman NF, Lohmann CM (2012) The magnetic map of hatchling loggerhead sea turtles. Curr Opin Neurobiol 22(2):336–342 Newman EA, Hartline PH (1982) The infrared “vision” of snakes. Sci Am 246(3):116–127 Schmitz H, Bleckmann H (1997) Fine structure and physiology of the infrared receptor of beetles of the genus Melanophila (Coleoptera: Buprestidae). Int J  Insect Morphol Embryol 26(3–4):205–215

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Schmitz H, Trenner S (2003) Electrophysiological characterization of the multipolar thermoreceptors in the “fire-beetle” Merimna atrata and comparison with the infrared sensilla of Melanophila acuminata (both Coleoptera, Buprestidae). J Comp Physiol A 189(9):715–722 Schmitz H, Schmitz A, Kreiss E, Gebhardt M, Gronenberg W (2008) Navigation to forest fires by smoke and infrared reception: the specialized sensory systems of “fire-loving” beetles. Navigation 55(2):137–145 von der Emde G (2013) Electroreception. In: Galizia C, Lledo PM (eds) Neurosciences—from molecule to behavior: a university textbook. Springer Spektrum, Berlin Wasko DK, Sasa M (2009) Activity patterns of a neotropical ambush predator: spatial ecology of the Fer-de-lance (Bothrops asper, Serpentes: Viperidae) in Costa Rica. Biotropica 41(2):241–249 Zupanc GK, Bullock TH (2005) From electrogenesis to electroreception: an overview. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 5–46

Part VIII: The Illusive World Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-­ altered sensory environment on animal perception and performance. Biol Lett 11(4):20141051 Rivlin R, Gravelle K (1984) Deciphering the senses: the expanding world of human perception. Simon and Schuster, New York Schwartz BL, Krantz JH (2017) Sensation and perception. Sage Publications, Thousand Oaks, CA

Index

A Acuity, 41, 42, 44–48, 157 Adaptations, 6, 13, 20, 23, 24, 30, 45–48, 50–54, 60, 69, 70, 75, 76, 88, 90, 118, 152, 161, 167, 177, 178, 187, 215, 244, 248, 257, 265, 269 Aggression, 57–59, 88, 89, 125–127, 137, 203, 204 Ampullae, 260 Anableps, 22, 23, 25, 26 Antennae, 35, 36, 109–111, 128–131, 136, 137, 196, 197, 210 Ants, 5, 34–38, 40, 64, 126–131, 195–199, 203, 213, 280 Aroma, 109, 113, 114, 117, 122, 145, 146, 148, 239, 264, 275 Attention, 8, 12, 13, 22, 28, 51, 52, 64, 73, 86, 105, 106, 137, 147, 195, 210, 225, 241, 242

Colors, 8, 14, 19–21, 24, 26–31, 38, 51, 53–61, 64, 71, 97, 105, 108, 114, 127, 152, 154, 161, 208, 213, 225, 239, 249–251, 265, 278 Compass, 33–35, 37, 39, 40, 232, 235, 236 Cones, 38, 41, 45, 53, 54, 60, 72, 109, 135, 244, 248 Crayfish, 4, 5, 49, 50, 57, 59, 85, 86, 126, 135–139, 154, 156, 248 Crustaceans, 23, 49, 56–59, 136, 137, 154, 155, 161, 162, 190, 230 Cues, 6, 8, 15, 28, 34, 35, 40, 80, 88, 96, 97, 109, 110, 113, 115, 122, 130, 135, 136, 138, 153, 175–177, 179, 186–188, 191, 195, 196, 202, 215, 222, 227, 233–235, 241, 242, 258, 259, 279

B Bass, 43, 44, 71–78, 105, 106, 136, 201–206, 265 Bees, 6, 27–30, 56, 60, 64, 108, 126, 202, 208–211, 213, 280 Bitter, 145, 148, 150, 152, 153, 164, 165, 167–171, 182, 279 Body odors, 120, 127, 128, 134, 173, 175, 176 Burrows, 21, 34–36, 58, 59, 85, 86, 202

D Depth perception, 43, 45, 46 Desert ants, 34–36, 38, 39 Direction, 22, 24, 33–41, 51, 58, 60, 69, 70, 81, 86, 92, 109, 110, 115, 135, 153, 164, 176, 179, 190, 199, 208, 216, 217, 219, 232–237, 242–244, 253, 255, 266–268 Dogs, 7, 12, 44, 49, 56, 61, 134, 142, 166, 173, 175, 205, 279 Drum, 87, 89–91, 105, 106, 111, 187, 201–203

C Cochlea, 68–70, 77, 92 Colony, 27, 126–128, 131, 195–197, 204, 206

E Ear drum, 74, 75, 77, 92, 190 Edge detection, 10

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290 Electrical, 15, 68, 111, 187, 226, 228, 230, 255–261, 263, 271, 272 Elephants, 73–79, 87, 101, 126, 226 Emotions, 6, 63, 79, 96, 101, 106, 107, 113, 119, 134, 138, 185, 201 Energies, 9, 11, 24, 25, 30, 37, 71, 75, 108, 110, 116, 120, 127, 129, 145–147, 150, 152, 170, 187, 205, 210, 219, 225, 227, 228, 230, 234, 235, 243, 250, 253, 255, 267, 271 F Fights, 49, 57, 59, 60, 89, 126, 134–139, 141, 166, 167, 188, 189, 255 Filters, 9–11, 13, 21, 60, 61, 247, 279, 280 Fires, 30, 117, 197, 218, 228, 239, 240, 243, 245, 248–253, 255, 271, 272, 276 Flavors, 19, 105, 114, 115, 145, 146, 148, 150, 152, 162, 165, 169, 171, 181, 182 Flehmen response, 174 Flick, 175, 176, 178, 181 Flicker fusion, 45–47 Flowers, 6, 9, 27–31, 64, 68, 81, 185, 208, 213, 279, 280 Focal, 46, 53, 88–90, 189, 250, 258, 259 Food, 4, 6, 21, 23, 34, 35, 43, 50, 51, 57–59, 64, 72, 77, 81, 96, 106, 115, 119, 120, 126, 128, 129, 135, 136, 141, 142, 145–155, 157, 159–162, 164–171, 173, 177, 178, 181, 188, 195, 208, 225, 226, 239, 242, 248, 249, 279 Foraging, 29, 34, 35, 50–52, 64, 74, 75, 81, 98, 126, 128, 129, 135, 194, 195, 197, 202, 208–211, 230, 258, 264, 265 Fovea, 21, 41, 42, 46, 47 Frequency, 46, 71–77, 79, 81, 83, 87, 89–91, 98, 99, 101, 109, 111, 187–191, 198, 205, 209, 218, 219, 222, 235 G Goggles, 51, 271 Guards, 58, 127, 128, 195, 209, 281 H Hair cell, 68–70, 75, 92, 186, 229 Hearing, 9, 15, 21, 51, 68–70, 72–77, 80, 83, 84, 92, 93, 97, 98, 100, 102, 105, 146, 152, 153, 163, 190, 198, 205, 221, 225, 229, 230, 272, 278, 280

Index Heat, 9, 15, 25–27, 30, 34, 35, 155, 174, 187, 226–229, 239–245, 248–253, 255, 265, 271, 272, 276, 280 Homing, 9, 29, 36, 39, 151, 233, 236 Hydrocarbons, 130, 131 I Imprint, 114, 116, 117, 238, 264 Infrared, 25, 37, 61, 71, 227, 228, 243, 250–253, 263 Infrasonic, 71, 76 Inner ear, 77, 92, 93, 99, 186, 205, 229, 232 Intensity, 10, 24, 30, 38, 47, 58, 59, 71, 72, 74, 76, 80, 88, 89, 96, 98, 110, 122, 137, 187, 189–191, 198, 199, 205, 209, 210, 216, 218, 219, 221, 222, 227, 228, 235, 237, 242, 253, 256, 259, 267, 268 Intestines, 169, 170, 279 J Jamming, 82–84, 279 Jaws, 9, 77, 79, 154, 204–206, 218 K Kinocilia, 69 L Landmarks, 33, 34, 36, 41, 232, 233, 235 Landscapes, 3, 9, 15, 21, 29, 34, 41, 55, 58, 60, 68, 116, 137, 141, 142, 153, 174, 176, 179, 222, 225, 232, 233, 236, 240, 241, 244, 248–250, 256, 260, 265–267 Leaf, 19, 20, 55, 110, 136, 195–198, 203, 215–217, 236 Learning, 14, 166, 168, 170, 173, 231 Lens, 20–26, 30, 38, 41, 45–48, 50, 53, 54, 58, 60, 64, 161, 243, 280 Light, 3, 6–11, 15, 20, 22, 24–26, 28, 30, 31, 34, 37–42, 44–50, 52–54, 56, 59–61, 63, 71, 102, 108–110, 128, 134, 135, 141, 153, 156, 160, 174, 176, 177, 196, 203, 215, 221, 226, 227, 229, 239, 242, 243, 247, 248, 250, 251, 255, 263, 266, 271, 280 Lingual, 169, 170 Love, 8, 63, 79, 93, 98–100, 107, 108, 110–112, 134, 208, 213–219, 229, 247 Lumen, 163, 164, 178, 260

Index M Magnetic, 15, 33, 34, 37, 38, 40, 187, 226–228, 230, 233–238, 258, 271, 272 Mantis shrimp, 56–60 Mating, 9, 49, 73, 86, 88, 96, 97, 100, 107, 117, 122, 126, 135, 146, 189, 208, 211, 214–216, 218, 219, 221, 258, 261, 264 Microvilli, 163, 260 Migration, 114, 117, 227, 234 Mole rat, 202–206 Mound, 127, 128, 194, 197 Music, 67–69, 79, 80, 83, 95, 96, 101, 105, 201, 202, 207, 221 N Natal, 114–118, 233–235, 238 Navigation, 33, 34, 41, 232, 233, 257, 258, 260 Nose, 3, 5, 9, 15, 49, 109, 110, 113, 115, 118, 134, 137, 138, 142, 148, 151, 152, 169, 178, 181, 206, 225, 229, 230, 236, 238, 240, 265, 267, 268, 279 O Octopus, 160–164, 280 Odors, 3, 105–117, 120–122, 128, 134, 137, 141, 142, 145, 147, 151, 153, 173, 175, 176, 225, 239 Ommatidia, 38, 39, 58, 60, 61 Opsins, 20, 38, 39, 54 Orientation, 34, 38, 232 Osprey, 42–46, 48, 52, 226, 280 Otolith, 92 P Path integration, 36 Perceive, 4, 5, 8–15, 30, 45, 46, 53, 72, 105, 111, 124, 127, 135, 151, 156, 169, 175, 181, 182, 225, 226, 244, 250, 258, 260, 271, 272, 275–278, 281 Perception, 3, 4, 9, 14, 15, 19, 30, 43, 45, 46, 106, 122, 124, 145, 168, 170, 173, 175, 181, 202, 225, 232, 245, 271, 276–279, 281 Pheromone, 106–111, 120, 122–124, 174, 179, 214, 215 Photoreceptors, 7, 10, 11, 20, 26, 30, 38, 39, 42, 46, 47, 53, 54 Physiology, 5, 106, 114, 120, 134, 137–139, 166, 167, 171, 211, 240, 279 Pigments, 20, 26, 30, 56, 57, 61, 105, 213

291 Pit, 178, 239–242, 244, 245, 251, 252, 280 Pitch, 46, 71, 76, 80, 193 Plume, 109–112, 122, 147, 249 Poison, 121, 145, 147, 148, 150, 152, 161, 162, 165–168, 170, 171, 182, 197, 279 Polarized light, 34, 37–40 R Radiation, 29, 228, 244, 251–253 Reality, 9–15, 27, 29, 30, 58, 64, 107, 108, 119, 225, 232, 271, 275, 277–279, 281 Reptiles, 15, 175–178, 233, 236, 240 Resume, 35, 133–139 Retina, 20, 21, 23–26, 30, 38, 40–42, 47, 48, 50, 53, 54, 60, 64, 153, 161, 243, 244 Retinular, 38 Rhythm, 67, 72, 91, 96, 105, 187, 191, 197, 201–212 Rods, 38, 39, 45, 53, 54, 60, 205 S Salmon, 114–118, 151, 238, 265 Salt, 21, 67, 114, 145, 148, 152, 164, 169, 182 Scatter, 19, 25, 26, 37, 38, 108, 167, 238, 250, 251, 266 Scent, 107, 109, 110, 113, 116, 122, 124, 128, 148, 151, 175, 176, 197 Semicircular canals, 92 Sensilla, 152, 218 Sensillum, 131, 149, 150 Sensitivity, 9, 20, 30, 46, 47, 51, 53, 56, 69, 72, 74, 75, 93, 155, 164, 179, 244, 264, 269 Sensory ecology, 5, 174, 230, 236, 275 Sensory landscape, 9, 21, 106, 149, 225–227, 233, 271, 278, 280 Serotonin, 120, 135, 138, 139 Sex, 13, 88, 107, 119, 122, 123, 134, 173, 174, 188, 211, 213, 214, 251 Signals, 5–10, 15, 36, 49, 55, 58, 59, 69, 74–76, 79, 82, 84, 86, 89, 92, 98, 100–102, 105–111, 114–116, 118, 120–122, 124, 127–129, 131, 136–138, 141, 142, 145, 156, 164, 168, 173–175, 177, 178, 186–191, 194–199, 203–207, 209–212, 214–219, 221, 222, 226–230, 232, 239, 240, 242, 251–253, 256–261, 268, 272, 278, 279 Smell, 3, 4, 7, 9, 15, 35, 85, 105–118, 121, 122, 128, 130, 134, 135, 138, 142, 145, 151–155, 162, 166, 169, 173–178, 214, 215, 225, 229, 238, 239, 268, 272, 275, 279, 281

292 Sniff, 107, 129, 137, 142, 173, 176, 279 Social, 5, 49, 59, 72–74, 86, 88, 96, 101, 106, 107, 119, 120, 126, 127, 133–139, 141, 147, 181, 188, 193–195, 197, 199, 202, 203, 260 Social behavior, 127, 135, 138, 141, 146, 194, 230 Somatotopic, 153, 156, 160, 261 Sound waves, 68, 69, 71, 76, 77, 86, 91–93, 98, 100, 190, 195, 198, 205 Sour, 145, 148, 151, 152, 164, 169, 182 Spiders, 4, 15, 121–124, 152, 175, 198, 208, 214–219, 222 Stereocilia, 69 Stomatopod, 56–58, 60, 61 Stretch receptors, 82, 186, 191 Stridulations, 90, 198, 199 Suckers, 161–164 Sugar, 19, 20, 129, 147, 148, 150, 153, 229 Sun compass, 232 Sweet, 9, 28, 116, 121, 145, 147, 148, 150–157, 164, 169, 182, 279 Swim bladder, 87, 90–93, 98–100, 190 T Tapetum lucidum, 7, 53, 54 Taste buds, 146, 152–157, 163, 164, 168, 169, 181, 229, 230, 240 Taste cells, 163, 164, 168–170, 174 Taste tester, 165, 181 Tentacle, 163–164, 182, 279 Thermal, 15, 240–245, 251, 253, 271, 272, 280 Thomas Nagel, 8, 14, 278 Tiger moth, 80–84 Tongue, 15, 28, 118, 142, 146, 148, 152–154, 156, 162–164, 168, 169, 173–179, 181, 225, 229, 230, 239, 240, 279

Index Touch, 13, 21, 23, 36, 41, 128, 137, 152, 156, 159–163, 176, 185, 186, 190–191, 196, 210, 218, 221, 225, 230, 250, 252, 261, 271, 272, 276, 279 Tunnels, 9, 194–199, 203, 204, 222 Turbulence, 50, 108, 272 Tymbal, 83 U Ultrasonic, 7, 14, 71, 76, 80–84 Ultraviolet, 29, 30, 37, 59–61, 64, 71, 251 Umami, 145, 152, 169, 182 Umwelt, 5, 7, 13, 26, 63, 187, 225 V Vibrates, 27, 37, 74, 76, 83, 87, 88, 91, 93, 99, 190, 191, 198, 209, 210, 216, 217 Vibrations, 9, 37, 39, 72, 74, 76, 77, 87, 89–93, 99, 185–191, 197–199, 202–206, 209–212, 215, 216, 218, 219, 221, 222, 267 Vibrissae, 267–269 Vipers, 240–244, 251, 252, 280 Visual field, 19, 21, 33, 42, 45–47, 51, 53, 64, 242, 244, 252 Vocal chords, 74–76, 86, 87, 100 Vomeronasal organ (VNO), 174, 176, 178, 179 W Wakes, 57, 211, 264–269 Waveform, 37, 258–260 Waves, 9, 21, 24, 25, 30, 37, 43, 67–72, 74–77, 79, 80, 85–93, 97–101, 115, 136, 187–189, 191, 195, 205, 211, 216–218, 226, 232, 234, 243, 255, 258 Whales, 14, 86, 87, 125, 194, 208, 221, 233, 264