Treatise on Zoology - Anatomy, Taxonomy, Biology. the Crustacea, Volume 5 [1 ed.] 9789004232518, 9789004190849

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THE CRUSTACEA R EVISED

AND UPDATED , AS WELL AS EXTENDED FROM THE

TRAITÉ DE ZOOLOGIE VOLUME 5

Cover: Male of Curtipleon heterochelatum Larsen, 2002; see fig. 59.1j on p. 253 of the present volume. [After Larsen, 2002, fig. 4B.]

T REATISE ON Z OOLOGY – A NATOMY, TAXONOMY, B IOLOGY

THE CRUSTACEA R EVISED AND UPDATED , AS WELL AS EXTENDED FROM THE

TRAITÉ DE ZOOLOGIE [Founded by P.-P. GRASSÉ (†)] Edited by J. C. von VAUPEL KLEIN, M. CHARMANTIER-DAURES and F. R. SCHRAM

VOLUME 5

With contributions by J. E. De Assis, D. Bellan-Santini, M. L. Christoffersen, M. Gu¸tu, K. Larsen, G. C. B. Poore, J. Sieg (†) English translations by J. C. von Vaupel Klein and F. R. Schram

BRILL LEIDEN · BOSTON 2015

Original edition published as: Traité de Zoologie – Anatomie, Systématique, Biologie. [Series editor P.-P. Grassé.] Vol. VII, Crustacés (fasc. II [pro parte]), edited by J. Forest. ISBN 2-225-84973-0. Masson Publishers, Paris, 1996. Traité de Zoologie – Anatomie, Systématique, Biologie. [Series editor P.-P. Grassé.] Vol. VII, Crustacés (fasc. III (A) [pro parte]), edited by J. Forest. Mémoires de l’Institut Océanographique, Monaco, n° 19. ISBN 2-7260-0202-1. Musée Océanographique, Monaco, 1999. English edition by Brill Academic Publishers, 2015, updated and enhanced by the original authors and/or additional authors and by the editors. Edited by J. C. von Vaupel Klein (former affiliation: Division of Systematic Zoology, Leiden University, c/o Naturalis Biodiversity Center, P.O. Box 9517, NL-2300 RA Leiden, Netherlands); Mrs. M. Charmantier-Daures (former affiliation: Equipe Adaptation, Ecophysiologique et Ontogenèse, UMR 5119 Ecosym, Université de Montpellier 2, Cc 092, Place Eugène Bataillon, F-34095 Montpellier Cedex 05, France); and F. R. Schram (current affiliation: Burke Museum of Natural History and Cultures, University of Washington, c/o Post Box 1567, Langley, WA 98260, U.S.A.). Translated from the French by J. C. von Vaupel Klein (Bilthoven, Netherlands).

Despite our best efforts, we have not been able to trace all rights holders to some copyrighted material. The publisher welcomes communications from copyrights holders, so that the appropriate acknowledgements can be made in future editions, and to settle other permission matters. This book is printed on acid-free paper. Library of Congress Cataloging-in-Publication Data The Library of Congress Cataloging-in-Publication Data is available from the Publisher. ISBN-13: 978 90 04 19084 9 E-ISBN: 978 90 04 23251 8 ©Copyright 2015 by Koninklijke Brill NV, Leiden, The Netherlands Koninklijke Brill NV incorporates the imprints Brill, Brill Hes & De Graaf, Brill Nijhoff, Brill Rodopi and Hotei Publishing. All rights reserved. No part of this publication may be reproduced, translated, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without written permission of the publisher. Authorization to photocopy items for internal or personal use is granted by Brill provided that the appropriate fees are paid directly to Copyright Clearance Center, 222 Rosewood Drive, Suite 910, Danvers, MA 01923, USA. Fees are subject to change.

CONTENTS

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Editors’ note: Devoting a chapter to Pentastomida . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M ARTIN L. C HRISTOFFERSEN & J OSÉ E. D E A SSIS, Class Eupentastomida Waloszek, Repetski & Maas, 2006 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G ARY C. B. P OORE, Orders Bochusacea, Mictacea and Spelaeogriphacea . . . . . . D ENISE B ELLAN -S ANTINI, Order Amphipoda Latreille, 1816 . . . . . . . . . . . . . . . . . ¸ & J ÜRGEN S IEG (†), Order Tanaidacea Dana, K IM L ARSEN , M ODEST G U TU 1849 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . List of contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Taxonomic index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Subject index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 3 5 77 93 249 331 335 349

This work has been published with the help of the French Ministère de la Culture – Centre National du Livre.

PREFACE

This volume 5 comprises the eighth fascicle in the present series Treatise on Zoology – Anatomy, Biology, Taxonomy – The Crustacea. The contents are, for the better part, constituted by the translated, revised, and updated texts from the Traité de Zoologie – Crustacea. The chapters in this book originated from those in the French edition volumes 7(II) and 7(III)(A), with the exception of chapter 45B, which has been newly conceived and was never published in French. What is herein denoted as chapter 51, treats three orders of crustaceans and emanated from two original French chapters, to which a third order has been added, as explained in that chapter. The current book was preceded by seven volumes already published in this English series, viz., volumes 1 (2004), 2 (2006), 9A (2010), 9B (2012), 3 (2012), 4A (2013), and 4B (2014). As stated in the Preface of vol. 4A, we have abandoned publishing the chapters in the serial sequence as originally conceived, because the various contributions become available in a more or less random order. After the Treatise will have been concluded, an overview of the total series will be published to ensure quick reference throughout the series as a whole. We trust that also this volume will prove to be a useful compendium for carcinologists world-wide, not only as a guide in investigating aspects of the taxonomy and biology of Crustacea, but just as well in carefully interpreting their results. January, 2015 Bilthoven, J. C AREL VON VAUPEL K LEIN Langley (WA), F REDERICK R. S CHRAM Montpellier, M IREILLE C HARMANTIER -DAURES

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CHAPTER 45A

DEVOTING A CHAPTER TO PENTASTOMIDA1 )

E DITORS ’ NOTE The systematic position of the group known as Pentastomida or Linguatulida has long been enigmatic; they were most often considered an “appendix” to the phylum Arthropoda without, however, much further specification, e.g., Meglitsch & Schram (1991). Although successive authors on the basis of a variety of morphological characters proposed connections with various taxa, their actual affinities, as those of the likewise enigmatic Tardigrada, remained unresolved. Thus, when Wingstrand (1972) published a comparative spermatology of a pentastomid and a branchiuran crustacean that most plausibly indicated a direct link between the two groups, many biologists, including most carcinologists, honestly believed the dilemma had been satisfactorily solved. As a result, two of the present editors (JCvVK and FRS) of this series succeeded in convincing the late Prof. Jacques Forest, earlier editor of the French edition of the Crustacea volumes of the Traité, to include a chapter on Pentastomida in this new English edition. That decision was taken during the period the first volumes of the series were composed, between 1999 and 2004. In the meantime, much research has been done on the postulated roots of Arthropoda, and along this track the position of Pentastomida as a taxon of Crustacea has by no means become any clearer. On the one hand, it might appear eroded based on newly acquired, mainly morphological, data from fossils that suggest Pentastomida could not have direct affinities with any taxon that is classified under Crustacea (Castellani et al., 2011). On the other hand, it might have gained strength from a series of molecular studies (Abele et al., 1980, 1992; Zrzavý, 2001; Koenemann et al., 2010; Regier et al., 2010) as well as from further, more detailed investigations into spermatology (Storch & Jamieson, 1992) that decidedly seem to indicate a close connection between Pentastomida and Branchiura. Yet, as will be shown in the following chapter, no. 45B (see the section Conclusions) many questions remain about the phylogenetic position of these exclusively parasitic, worm-like animals. Because of this, we consider it all the more justified to include such a chapter: biologists, and notably carcinologists, should judge for themselves the hypotheses of whether or not Pentastomida could be aberrant crustaceans. For that purpose, they will 1 ) First conceived November 2014; final amendments made January 2015.

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need to be aware of the morphology and biology of the representatives of the group — and what better way to achieve that than including these enigmatic organisms in a book series devoted specifically to the crustaceans. J. C AREL VON VAUPEL K LEIN, Bilthoven F REDERICK R. S CHRAM, Langley, WA

BIBLIOGRAPHY A BELE , L. G., W. K IM & B. E. F ELGENHAUER, 1980. Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. — Mol. Biol. Evol., 6: 685-691. A BELE , L. G., T. S PEARS , W. K IM & M. A PPLEGATE, 1992. Phylogeny of selected maxillopodan and other crustacean taxa based on 18S ribosomal nucleotide sequences: a preliminary analysis. — Acta Zool., 73: 373-382. C ASTELLANI , C., A. M AAS , D. WALOSZEK & J. T. H AUG, 2011. New pentastomids from the Late Cambrian of Sweden — deeper insight into the ontogeny of fossil tongue worms. — Palaeontographica Beitr. Naturgesch. Vorz., (Paläozool. – Stratigr. / Palaeozool. – Stratigr.) 293 (4-6): 95-145. KOENEMANN , S., R. A. J ENNER , M. H OENEMANN , T. S TEMME & B. M. VON R EUMONT, 2010. Arthropod phylogeny revisited, with a focus on crustacean relationships. — Arthr. Struct. Dev., 39: 88-110. M EGLITSCH , P. A. & F. R. S CHRAM, 1991. Invertebrate zoology. — Pp. 347-357. (Oxford University Press, New York.) R EGIER , J. C., J. W. S HULTZ , A. Z WICK , A. H USSEY, B. BALL , R. W ETZER , J. W. M ARTIN & C. W. C UNNINGHAM, 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. — Nature, Lond., 463: 1079-1083. S TORCH , V. & B. G. M. JAMIESON, 1992. Further spermatological evidence for including the Pentastomida (tongue worms) in the Crustacea. — Int. J. Parasit., 22: 95-108. W INGSTRAND , K. G., 1972. Comparative spermatology of a pentastomid, Raillietiella hemidactyla, and a branchiuran crustacean, Argulus foliaceus, with a discussion of pentastomid relationships. — Kong. Dansk. Vidensk. Selsk., Biol. Skr., 19: 1-72, pls. 1-23. Z RZAVÝ, J., 2001. The interrelationships of metazoan parasites: a review of phylum- and higherlevel hypotheses from recent morphological and molecular phylogenetic analyses. — Fol. ˇ Parasit., Ceské Budˇejovice, 48: 81-103.

CHAPTER 45B

CLASS EUPENTASTOMIDA WALOSZEK, REPETSKI & MAAS, 20061 ) BY

MARTIN L. CHRISTOFFERSEN AND JOSÉ E. DE ASSIS

Contents. – Introduction. Historical overview – Highlights from the five periods of classification. Taxonomy. Classification of the Pentastomida – Phylogenetic position. Morphology and function – Body tagmata and appendages – Body wall, body cavity, and locomotion – Moulting and growth – Sensory systems – Nervous system – Digestive system, food, and feeding – Reproductive system, reproduction, and chromosome number. Development and life histories – Embryonic development – Larval development – Life cycles. Pentastomid infestations of animal groups, pathology, and diseases – Pentastomiasis, a clinical perspective – Pentastomes and pentastomiasis in man. Ecology. Physiology, biochemistry, and immunology. Biogeography. Systematics: current classification. Conclusions. Acknowledgements. Appendix – Checklist of species of Recent Pentastomida cited in this review – Authorities and dates of non-pentastomid species names. Bibliography.

INTRODUCTION Almost 150 species and subspecies of obligatory endoparasites of terrestrial tetrapods, some also using fish and insects as intermediate hosts, are now included in the Class Eupentastomida. These extant pentastomids are remarkable because they still have a well-developed cuticle without notable adaptations to an internalized mode of life in a host (Maas & Waloszek, 2001). They make up the Phylum Pentastomida, alternatively known as Linguatulida, together with eight stem-group Palaeozoic, immature parasitic fossils. Their body plan apparently lacks arthropod synapomorphies, but places them phylogenetically within the Ecdysozoa (cf. Nielsen, 2001). Pentastomida constitute a five-fold, five-hundred-million year-old mystery: present in the five vertebrate classes, cosmopolitan and abundant on the five continents, and ten1 ) First conceived in this form in 2012; updated by the authors November 2014.

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tatively connected to five phyla along their classification history: Platyhelminthes (Cestoda (Chabert, 1787) and Trematoda (Rudolphi, 1809)); Nematoda (Nørdmann, 1832; Diesing, 1850); Acanthocephala (Von Humboldt, 1809); Annelida (Heymons, 1935); and Arthropoda (Crustacea (Van Beneden, 1848), Acarina (Schubärt, 1853; Sambon, 1922), and Myriapoda (Osche, 1963)). They have also been associated with five highlevel taxa: Stelechopoda (for Pentastomida, Myzostomida, and Tardigrada (Graff, 1877)); Oncopoda (for Onychophora, Tardigrada, and Pentastomida (Cuénot, 1949)); Ichthyostraca (for Branchiura and Pentastomida (Zrzavý, 2001)); Oligostraca (for Ostracoda and Ichthyostraca (Lim & Hwang, 2006), and expanded to include also Mystacocarida (Regier et al., 2010)); and Mysopharyngea (Ecdysozoa) [for Tardigrada, Pentastomida, and Nemathelminthes] (Almeida et al., 2008). Furthermore, they are enigmatic in at least five different areas of research: (1) Life cycle. Why are only larval pentastomids known from fish? Which were the hosts of adults before the appearance of Tetrapoda? Did the endoparasitic life cycle in the respiratory system of the host coevolve with the tetrapod conquest of land? (2) Phylogeny. The phylogeny and systematic position of the pentastomids has remained enigmatic for a long time (Waloszek et al., 2006; Jenner & Littlewood, 2008). Which are the closest relatives of Pentastomida within the Ecdysozoa? Are pentastomids stem-group ecdysozoans, stem-group arthropods, or derived crustaceans? Why do they share sperm and molecular similarities with branchiurans, but present few characters in their morphology that may be hypothesized as mandibulate apomorphies? (3) Biogeography. Did the group originate in the northern Holarctic (location of known fossils), southwestern Gondwana (the cephalobaenids are distributed in South America), or was the group originally cosmopolitan and Pangaeic? (4) Palaeontology. Why does the fossil record of adult parasites and their hosts remain unknown? Have palaeontologists searched the respiratory tracts and viscera of vertebrates for pentastomid remains, i.e., of both adults and larvae? Alternatively, maybe the stem-group fossil pentastomids were not yet fully specialized as parasites, being still detritus feeders, symbiotic, or ectoparasitic, having developed their complex life cycles much later? (5) Parasitology. Why does a medically important parasite of vertebrates, including man, remain largely unknown or neglected by parasitologists? Do pentastomids fail to attract general interest just because their morbidity in humans is generally low? Pentastomids are nevertheless a group of great antiquity, being cosmopolitan, very abundant, and clinically important as disease-provoking parasites of man and other vertebrates. Yet they remain unperceived, understudied, and (largely) misunderstood. The parasitic pentastomids are worm-like, haematophagous ecdysozoans that lack both respiratory and circulatory systems and live as adults in the respiratory tract of their mostly reptilian hosts (Thomas & Böckeler, 1992a). They remain very poorly understood and enigmatic, even to those working with them (Trainer et al., 1975). They originated in the sea, being recorded in Cambrian and Ordovician times, but are restricted as adults to the respiratory tracts of terrestrial tetrapods. In contrast to most other taxa of arthropods (but much like parasitic cirripedes and copepods), they do not possess any mouthparts in the form of modified extremities, e.g., for piercing or cutting the capillaries (Thomas & Böckeler, 1992b), or sensory antennae, like other, mandibulate arthropods do. Pentastomida cause visceral and respiratory pentastomiasis in all major vertebrate groups,

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with nymphs even occurring in some insects (orthopteran cockroaches and chrysomelid coleopterans), and have economical importance (they cause reduced health in several vertebrates, including man, and may be important in regulating the size of tetrapod communities). We herein summarize previous knowledge of the Recent Pentastomida, with emphasis on the evolution of the group. As a basis for the present enterprise, a monograph of the extant pentastomids and their hosts has been published elsewhere (Christoffersen & De Assis, 2013).

HISTORICAL OVERVIEW Almeida & Christoffersen (1999) delineated five important periods in the systematic history of Pentastomida. The first goes from the pioneer descriptions and first efforts to understand the pentastomids (Frölich, 1789; Von Humboldt, 1811; Van Beneden, 1849a, b; Diesing, 1850), ending with the proposal of Linguatulidae (Leuckart, 1860). The second period culminates in the system of Sambon (1922). The third period encompasses the revisions of Heymons (1935, 1941a, b, c). The fourth period starts with the proposal of Fain (1961), Nicoli (1963), Nicoli & Nicoli (1966), and Self (1969) produced an excellent synthesis on the systematics, taxonomy, and geographic distribution of Pentastomida during this period. The fifth and last period consists of important taxonomic revisions, updates, and the proposal of a phylogenetic system.

Highlights from the five periods of classification F IRST PERIOD Diesing (1836) described about 24 species. Leuckart (1860) produced a pioneering historical monograph, with a detailed account of the anatomy and development of Linguatula serrata, and lists the then known species, with original Latin diagnoses. S ECOND PERIOD Stiles (1891a, b) presented a complete bibliography with 143 references. Shipley (1898) attempted to revise Linguatulidae, and later Shipley (1909) gave a concise account of the group. Sambon (1922) completed a systematic review of Linguatulidae. Hett (1924) provided 103 references. T HIRD PERIOD The work of Heymons (1935) constitutes an authoritative and influential monograph on pentastomid biology, being the main treatise of the group up to the present date. It contains a synopsis of anatomy, embryology, and taxonomy, an extensive treatment on phylogeny, and lists 218 references. Instead of mites, Pentastomida were considered a class of Annelida and subdivided into two orders: Cephalobaenida (including Cephalobaenidae and

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Reighardiidae) and Porocephalida (with Linguatulidae and Porocephalidae) (Heymons, 1935). Heymons & Vitzhum (1936) slightly elaborated this classification scheme, thereby rejecting the possibly arthropod origin of pentastomids. Hill (1948) provided a total of 388 references. F OURTH PERIOD This period is preceded by the elucidation of the life cycle of Sambonia clavata (cf. Fain & Mortelmans, 1960). Fain (1961) provided a revision, based on extensive field work, with a critical analysis of features considered important in taxonomy. Osche (1963) gave an extensive and detailed study of the embryos in the eggs of a single specimen. He argued for mandibulate affinities. Nicoli (1963) provided a history of the group and dealt with phylogeny. Doucet (1965) detailed adult morphology, especially of the nervous system. Nicoli & Nicoli (1966) dealt with biogeography and life cycles. Kästner (1968) gave a concise textbook-account. Self (1969) furnished a key to the genera and a bibliography of already 955 references. F IFTH PERIOD Riley (1986) provided an extensive review of pentastomid biology. Andres (1989) discovered Palaeozoic fossil pentastomids. Riley (1992a, 1993) dealt with reproductive biology. Storch (1993) furnished an overview of microscopic anatomy. Waloßek and coworkers described several new Palaeozoic fossils (Walossek & Müller, 1994; Walossek et al., 1994). Almeida & Christoffersen (1999) provided the first tentative phylogeny of the Pentastomida. Röhlig et al. (2010) presented an annotated catalogue based mainly on Heymon’s material. Castellani et al. (2011) provided the latest overview comparing Recent species with fossil material. Poore (2012) recently provided a nomenclatural revision of the Recent Pentastomida.

TAXONOMY Fain (1964) accorded class status for pentastomids. Riley (1986), in the last overview of Pentastomida, maintained the taxon as a class, under the belief that they were to be included in Phylum Crustacea. On the other hand, Osche (1963) argued for arthropod affinities of Pentastomida and placed them at phylum level. In this regard he was followed by Nicoli (1963) and Self (1969). The same status is accorded by many former editions of textbooks on invertebrate zoology (Russel-Hunter, 1979; Barnes, 1987). With the discovery of an extended Palaeozoic record of stem-group pentastomids since the Cambrian (last reviewed in Castellani et al., 2011), we have strong additional, circumstantial evidence (palaeontological, morphological, as well as on the minimum age of the group) to support phylum status for this clade, which now indeed seems to have evolved independently from the Arthropoda. On the other hand, Sanders & Lee (2010) have provided newly estimated molecular-clock data for pentastomid origins ranging from

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Fig. 45B.1. Some representative male copulatory spinules in species of the pentastomid genus Raillietiella. A, Raillietiella affinis; B, Raillietiella maculatus; C, Raillietiella mabuiae; D, Raillietiella orientalis; E, Raillietiella furcocercum; F, Raillietiella crotalis. [Adapted from Ali et al., 1985.]

490 to 520 Myr ago, consistent with the age of Cambrian fossils of Pentastomida. Herein, and on the basis of the phylogenetic system proposed in Christoffersen & De Assis (2013), we establish the class level for the extant, crown-group Eupentastomida. The identification of pentastome parasites is based on relatively few morphological characteristics (Riley, 1986). Because males tend to be comparatively short-lived, taxonomy and mature infections mostly refer to observations on females (Rego, 1984; Riley, 1986). Only in raillietiellids do males become important in specific diagnoses (Ali et al., 1985). In this group, the male copulatory spicule (fig. 45B.1) is considered to be of taxonomic value (Gretillat & Brygoo, 1959; Ali et al., 1982a, b, c, 1984a, b). Criteria used for classification are anatomical, pertaining to mouth and hook position and morphology, glands, and male and female genitalia, among many others (Riley, 1969; Paré, 2008). These characters are subject to high levels of intraspecific variation, which has often been referred to as one of the hallmarks of pentastome morphology (Riley, 1986; Riley & Huchzermeyer, 1995). For example, hooks increase in size and may change in shape at each moult (Fain, 1964), while body size is possibly influenced by the host (Giglioli, 1927) and the number of annuli can show pronounced intraspecific variation (Ali et al., 1982b, 1984b). Self & McMurry (1948) showed that not only can different hosts influence the size of specimens of Porocephalus, but size is also related to age. Vargas V. (1970) conducted a detailed analysis of the morphology of the eggs and nymphal stages of two species of Porocephalus and concluded that neither the statistical, nor the morphological analyses of these data can be used to separate these forms satisfactorily. Nevertheless, the combination of various characters presumably provides a reliable means for determining taxonomic status (Junker, 2002). It has been proposed that, to facilitate valid descriptions of new species of pentastomes, taxonomic work may benefit from including both morphological measurements, including quantitative measurements of body size and hook bluntness, and molecular sequence data (Kelehear et al., 2011). Mätz-Rensing et al. (2012) demonstrated that molecular diagnostic methods are necessary tools to determine the exact species involved in cases of visceral pentastomiasis.

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CLASSIFICATION OF THE PENTASTOMIDA A phylogenetic system of Pentastomida was proposed by Christoffersen & De Assis (2013). It should be noted that only two previous phylogenetic proposals were known for the relationships within Pentastomida: (1) (Cephalobaena (Raillietiella (Reighardia (Leiperia (Sambonia (Sebekia (Alofia + Selfia)))) (Waddycephalus + Kiricephalus + Gigliolella (Parasambonia + Porocephalus) + (Armillifer + Cubirea))) (cf. Almeida & Christoffersen, 1999); and (Leiperia (Sambonia (Diesingia (Selfia + Alofia))) (Agema (Sebekia + Pelonia))))) (cf. Junker, 2002). These proposals were combined and further developed in Christoffersen & De Assis (2013) (see item Current classification, below).

Phylogenetic position Fossils differ from Recent forms in having trunk somites with appendages located in front of the genital pores (Walossek & Müller, 1994). Cephalobaena is the sister group of all remaining recent pentastomids, having a rostrum in the first larval stage (Von Haffner, 1971). Leiperia occupies a different niche, the tracheae of crocodiles, and has a unique life cycle, including an obligatory phase in the circulatory system (Riley & Huchzermeyer, 1996; Junker et al., 2000). We have herein indicated a new, unnamed family-group taxon for Leiperia. This new subfamily has been formally named and diagnosed in a recent monograph for the present synthesis (Christoffersen & De Assis, 2013). A RE PENTASTOMIDS ICHTHYOSTRACAN MAXILLOPODS (B RANCHIOPODA + P ENTASTOMIDA )? Wingstrand (1972) first proposed a Branchiura-Pentastomida relationship, based on the unique sharing of a set of ultrastructural sperm features of pentastomids with fish lice (Crustacea). This idea seems to make sense for understanding the transition of marine to terrestrial pentastomids, at least at first sight, because Cambrian pentastomes necessarily must have parasitized aquatic hosts such as fish, thus paralleling the parasitic habits of fish lice. Mysteriously, however, no such hosts for pentastomes have been documented to date. If the ancestors of pentastomids were Argulus-like arthropods, infesting the gills and perhaps the lungs of crossopterygians as adults, they could easily be imagined to have evolved into specialized parasites of the lungs, while their hosts developed into terrestrial animals. The rarity of adult pentastomids in the small remnants of the amphibian group surviving today is certainly no strong argument against such a possibility (Wingstrand, 1972). Currently, a consensus has developed for placing pentastomids within Crustacea, as the sister group of Branchiura (Crustacea, Oligostraca, Ichthyostraca). The grounds for this is the striking similarities in the ultrastructure of spermatozoa (Wingstrand, 1972; Riley et al., 1978; Grygier, 1983; Storch, 1984; Storch & Jamieson, 1992; Jamieson & Storch, 2000). Both Branchiura and Pentastomida possess a bilateral spermatozoan with a completely reduced flagellum (Møller, 2009).

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Storch & Jamieson (1992) presented a hierarchichal structure for the comparative data on sperm ultrastructure, an impressive nine apomorphies for Branchiura + Pentastomida, another four for Cirripedia as a sister to the previous clade, two for Mystacocarida as the next out-group, and one more for Ascothoracida as the most basal clade of the former taxon Maxillopoda. To this ultrastructural evidence, an impressive corpus of molecular data has been added, based on nucleotide and amino-acid sequences. This additional support comes from aminoacid sequences from mitochondrial genes (Lavrov et al., 2004), from 18S rRNA-gene sequences (Abele et al., 1989; Spears & Abele, 1998; Zrzavý, 2001), and more recently from 18S plus half of the 28S rRNA gene (Giribet et al., 2005), nearly complete 28S plus 18S rRNA genes (Mallat & Giribet, 2006), from 16S rDNA, cytochrome c oxidase subunit I (COI) and the nuclear ribosomal gene 18S rDNA (Koenemann et al., 2010), as well as from nuclear protein-coding sequences (Regier et al., 2010). The complete sequence of the mitochondrial DNA (mtDNA) of the pentastomid Armillifer armillatus and complete or nearly complete mtDNA sequences of various Crustacea, i.e., Remipedia (Speleonectes tulumensis), Cephalocarida (Hutchinsoniella macracantha), Cirripedia (Pollicipes polymerus), and Branchiura (Argulus americanus) are taken to indicate unambiguously that Pentastomida are a sister group to Branchiura within a monophylum Ichthyostraca (Lavrov et al., 2004). The maximum likelihood tree calculated from the combined 28S + 18S rRNA genes corroborated that the pentastomid Raillietiella groups with the branchiuran crustacean Argulus (Mallat & Giribet, 2006). The name Ichthyostraca was first suggested for this clade by Zrzavý (2001). Summarizing, the evidence for pentastomids being Ichthyostraca remains rather specific: (1) spermatological data (Wingstrand, 1972; Riley et al., 1978; Storch & Jamieson, 1992); (2) molecular cladograms (DNA sequence data: Abele et al., 1989, 1992; but see Spears & Abele, 1998; Regier et al., 2010); (3) mitochondrial gene order (Lavrov et al., 2004); 18S and 28S rRNA data (Giribet et al., 2005); (4) and other molecular data (K. J. Peterson & Eernisse, 2001; Regier et al., 2010). The amazing discovery of fossils from the Cambrian (Walossek & Müller, 1994), however, implies that if pentastomids are related to branchiurans, both their morphology and their modes of development have differed markedly at least since the Middle Cambrian, for more than 500 Myr. It would be interesting if pentastomids could be derived from fish lice, but at present Pentastomida appear to represent a much older taxon (at least Middle Cambrian). The lower limit for the origin of the branchiurans would be the Devonian, 400 Myr ago, during the diversification of their fish hosts (Romer, 1996). Or else they have an undiscovered ghost-lineage extending much further back in time than currently known. Branchiura (argulids), a specialized group of crustaceans, must belong to a lineage that originated much later than the pentastomids (Cave et al., 1998), whence it seems an historical impossibility that Branchiura would be the ancestral group of Pentastomida. Branchiurans have articulated appendages on the head (antennae), biramous appendages on the body, and the adults are ectoparasites of fishes. Even highly modified copepod and cirripede parasites have nauplius larvae, segmented head appendages, and biramous

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body appendages, albeit not as adults. Thus pentastomids could be interpreted as having lost segmented and biramous appendages, such as in adult cirripede and copepod parasites. But if pentastomids were ichthyostracans, they would represent the only terrestrial invasion within crustaceans. Consequently, the concurrence in nucleotide sequences of ribosomal RNA should be re-examined and tested with other species of pentastomids (Tchesunov, 2002). Both these lines of evidence (ultrastructural sperm data and molecular data) have been questioned by other studies (Walossek & Müller, 1994; Tchesunov, 2002). Specialized holomorphological data, such as sperm ultrastructure, ultrastructure in general, and sequence data in particular, when taken alone and out of context with holomorphology in general, may provide misleading signals for phylogenetic inference, simply because the availability of such data is more restricted, limited to few taxa, being thus less representative of the variability and generality of the data in the groups under analysis. Furthermore, sequences of 18S rRNA may not be reliable for discerning cladogenetic events that occurred as far back as the Cambrian (Philippe et al., 1994). Riley (1986) reviewed the spermatological evidence of Wingstrand (1972) and concluded that these similarities may be expected as a result of convergence. Very long and narrow spermathecal ducts could result in the independent evolution of filiform sperm in Branchiura and Pentastomida (Riley, 1986). Spermatozoa of Arthropoda underwent an extraordinary variety of specializations, with apparent convergences and parallel developments (Cave et al., 1998). The ultrastructural similarities of sperm between Pentastomida and Branchiura could also be due to plesiomorphies (we need more comparative data on ecdysozoan spermatology to decide this issue). So what seems to unite pentastomes with branchiurans may be fishy convergences or plesiomorphies in sperm and sequence data. Such convergent adaptations and plesiomorphic similarities would not indicate shared ancestry of branchiurans and pentastomes. The analysis of mtDNA of the pentastomid Armillifer armillatus (cf. Lavrov et al., 2004) revealed three derived gene arrangements informative for the phylogenetic position of pentastomids. These rearrangements suggest, unambiguously according to those authors, that Pentastomida are not an early proarthropod lineage, but should be placed inside the assemblage Pancrustacea (their Tetraconata) (Lavrov et al., 2004). In addition, the maximum likelihood and distance analyses based on amino acid sequences of mitochondrial protein-coding genes support a close relationship between the pentastomid Armillifer armillatus and the branchiuran Argulus americanus (cf. Lavrov et al., 2004). We disagree: What are three not perfectly-aligned nucleotide similarities among thousands of similar nucleotides? Even the most recent mitochondrial genome comparisons (Yan et al., 2012) continue to indicate a close affinity of Branchiura and Pentastomida. In that work, the mtDNA arrangement of Armillifer armillatus is compared to that of several other maxillopods. What strikes us as remarkable is that overall similarity is still used in phylogenetic arguments with such impunity in an era of Hennigian character relativity. Which are the decisive apomorphic similarities among so many conserved plesiomorphic molecular sequences in these and similar molecular approaches? Of course,

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if pentastomids are not maxillopodans, the pentastomid convergences in ultrastructural sperm characters remain in need of a more conclusive explanation. On the other hand, if Pentastomida and Branchiura are closely related, they would have diverged since their origin in the Cambrian. Pentastomids would have lost nearly all characters of maxillopods and crustaceans, as well as the majority of arthropod features. This seems unlikely, however, because these supposed losses must have happened before the end of the Cambrian, to judge from the fossils. The present consensus considering Pentastomida to be maxillopod crustaceans pushes their documented fossil origin way back into the Cambrian. Sanders & Lee (2010) have obtained a molecular phylogeny with a PentastomidaBranchiura grouping, in which this clade is the sister-group of Tetraconata, whereas all other crustaceans form a monophyletic group that is sister to the hexapods. This scheme is congruent with the estimated molecular dates for pentastomid origins, ranging from 490 to 520 Myr ago, thus being consistent with the age of Cambrian pentastomid fossils. The proposal of Sanders & Lee (2010) is interesting, because it attempts to reconcile two opposing views currently available on pentastomid relationships: maxillopodan relationships versus a basal arthropodan position. While most morphological characters suggest that branchiurans are typical crustaceans such as copepods and cirripedes, pentastomids lack typical euarthropodan characters such as cuticular proteins, and have consequently been interpreted as basal arthropods (Karappaswamy, 1977; Böckeler, 1984a; Maas & Waloszek, 2001; Tchesunov, 2002; Waloszek et al., 2006; Almeida et al., 2008). Sanders & Lee (2010) accept the sperm ultrastructure and the molecular evidence that join Pentastomida and Branchiura into the taxon Ichthyostraca as robust evidence, but suggest that this group is more distantly related to the other crustaceans than previously indicated (Lavrov et al., 2004; Møller et al., 2008). Ichthyostraca thus becomes placed more basally in their phylogeny, as the sister group to Tetraconata (Hexapoda and the remaining crustaceans). They interpret the small Cambrian pentastomids as adults with a direct life cycle in small fish-like vertebrates and suggest that complex life cycles and large adults only developed when air-breathing tetrapods appeared in the Upper Devonian (∼365 Myr ago). Direct development is actually known in living pentastomids (Haugerud, 1989) and a simplified life cycle is consistent with the relative basal position of the Cambrian fossils along the pentastomid stem (Waloszek et al., 2006). Branchiurans and pentastomids are supposed to differ from most other crustaceans and all insects in one striking character: oocytes develop on the outer surface of the ovary, extending into the haemocoel (Ikuta & Makioka, 1999; Giribet et al., 2005). We may add that branchiurans and pentastomids differ from many crustaceans in one negative character, the lack of a naupliar phase in their development. Although no fossils of Branchiura are known, the earliest crustacean fossils are 480 Myr old (X. D. Zhang et al., 2007; Harvey & Butterfield, 2008). Sanders & Lee (2010) have thus elegantly reconciled life cycle, fossil record, and conflicting phylogenetic signals, showing that pentastomids can be simultaneously related to branchiurans, and also have a deep fossil record. However, their molecular phylogeny still differs from known morphological cladistics in indicating Onychophora as the sister group of Myriapoda plus Pycnogonida + Chelicerata, instead of placing myriapods at the base of Tetraconata.

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A RE P ENTASTOMIDA MANDIBULATE CRUSTACEANS ? Pentastomids have been considered a class of Mandibulata (Beaver et al., 1984). A crustacean relationship of pentastomids was endorsed, from somatic and other evidence, by Riley et al. (1978). Thus, several textbooks considered pentastomids as crustaceans (Ruppert & Barnes, 1994; Brusca & Brusca, 2003). However, Pentastomida and crustaceans are sharply disparate in characters concerning morphology, embryology, life cycles, and geological history. The placement of Pentastomida in the system of Crustacea implies a significant inflation of the taxonomic diagnosis of the latter group; for this reason alone, the move appears suspect. How many other predominantly marine invertebrate taxa can claim to have representatives living in the respiratory passages of crocodilians, reindeer, and lions (Martin & Davis, 2001), not to mention humans? Pentastomes would be the only crustaceans to parasitize the airways of terrestrial vertebrates (Abele et al., 1989). Furthermore, what happened to the non-ultrastructural morphological evidence for the crustacean nature of pentastomids? Or, considering that Crustacea are no longer believed to represent a monophyletic group (Moura & Christoffersen, 1996; Regier et al., 2010; Wägele & Kück, 2014), where are the supposed mandibulate synapomorphies of pentastomes: nauplius-larvae, compound eyes, sensory antennae, mandibles, maxillae, maxillipeds, biramous limbs? No clues whatsoever. Pentastomes appear to be rather simple and worm-like in overall appearance, not what one would expect from very highly evolved mandibulate crustaceans. Furthermore, no signs of any crustacean larval features have yet been detected during embryogenesis (Böckeler, 1982a, b, 1984a-d; Waloszek et al., 2006). It may be argued, of course, that the absence of a free-swimming larva in pentastomids is a necessary adaptation to endoparasitism. But then, as a counter argument, one would ask, why do even more profoundly modified crustacean parasites such as some cirripedes, copepods, and isopods, retain a typically crustacean free-swimming larva? Summarizing, some important differences have been used previously to argue against pentastomids representing Crustacea: (1) There is no free-living crustacean larva, as is the case even in highly modified crustacean parasites (although branchiurans do not have nauplii or metanauplii in their development, they do not hatch with the final number of somites, as pentastomids do); (2) biramous limbs and body appendages are absent; (3) compound eyes, one or two pairs of sensory antennae, and mouth appendages (mandibles, maxillules, and maxillae in the cephalic tagma) are also absent in adults; (4) the body is not sclerotized; features such as tergites, dorsal sclerotization, and a head shield, are all absent; (5) metamorphosis is absent; instead of a gradual increase in body segments as seen in crustaceans, the primary larva of pentastomids hatches with the final number of body segments. A RE PENTASTOMIDS EUARTHROPODS ? As an alternative for a mandibulate relationship, some authors have tried to link pentastomes with myriapods (see Haugerud, 1989), or mites (H. W. Brown & Neva, 1983).

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Osche (1963) concluded from their embryology that pentastomids are tracheate arthropods with probable myriapod affinities. Nørrevang (1972) recognized chelicerate or chilopod relationships from the structure of the ovary, and Storch & Böckeler (1979) saw arthropod affinities in the ultrastructure of the cephalic sensilla. Leuckart (1860) adduced important anatomical and embryological evidence to support their arthropod nature. Land (1888) then questioned these arthropod affinities, but Ihle (1899), by contrast, considered them a special class of Tracheata. Sambon (1922) again considered them as greatly modified descendants of the Acarina, adding as further evidence the anterior position of the female genital openings in recent species (the fossils now indicate that two appendage-bearing trunk somites lying anteriorly to the genital openings, were lost in Recent species), as well as the six-legged larvae of Raillietiella and Reighardia. Infective, third stage nymphs of Armillifer armillatus are supposed to look pretty much like insect larvae (Lavarde & Fornes, 1999). The following evidence has formerly been used in favour of pentastomids being Euarthropoda: (1) a complex brain, innervating the head appendages (Osche, 1963); (2) the dorsal organ places them near Myriapoda, according to Osche (1963). However, an embryonic dorsal organ is now known to occur in Crustacea, Pentastomida, insects, tardigrades, onychophorans, and chelicerates (Martin & Laverack, 1992), which is congruent with pentastomids belonging to the onychophoran-ecdysozoan lineage. Here is an illustration of the usual limits of inferences from ultrastructure: a character considered as evidence for Pentastomida + Myriapoda now indicates that pentastomids are ecdysozoans. But neither the Cambrian fossils nor the Recent forms of Pentastomida present morphological, ontogenetic, or anatomical evidence for their inclusion as any specific group of Euarthropoda (Walossek & Müller, 1994; Maas & Waloszek, 2001; Waloszek et al., 2006; Castellani et al., 2011). Pentastomids are oligomeric. Therefore, pentastomid larvae are fundamentally different from those of Euarthropoda, the larvae of which are primitively ‘head’ larvae (e.g., Trilobita, Pantopoda, stem-group Crustacea; ‘partial-head’ nauplii are restricted to their crown-group, according to Walossek & Müller, 1990, 1993). Pentastomid head limbs are uniramous and divided into three-jointed podomeres that arise from a socket provided by the body. Pentastomids also hatch with their final number of body segments. Segment addition does not occur during size increase, neither in fossils nor in extant forms (Castellani et al., 2011). Euarthropods have teloblastic growth (a budding zone in front of the telson that splits off somites progressively during growth). Pentastomids have no hypostome or labrum, and the mouth has a frontoventral position, with no head shield as in arthropods. Oligomery, segment constancy, pseudo-metamerism of the trunk end, and β-chitin, are not typical of Euarthropoda (Walossek & Müller, 1994). A RE PENTASTOMIDS PROTOARTHROPODS ? The true phylogenetic position of the Pentastomida has long remained unresolved (Junker, 2002), but lately consensus on their arthropod nature seems to have been reached

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(Walossek & Müller, 1994). Severe reductions in organ systems and appendages as an adaptation to a strictly parasitic life style are supposed to have conspired to obscure their systematic affinities (Self, 1969; Bosch, 1987). There is some evidence for Pentastomida to be considered basal Arthropoda (Sambon, 1922; Self, 1969; Riley et al., 1978; Riley, 1986; Haugerud, 1989): (1) sperm stored in spermathecae (Self, 1969; Riley, 1983, 1986; Storch, 1993); (2) striated muscles (Dujardin, 1845), not present in Onychophora or Tardigrada (Nicoli, 1963); (3) muscles attached to the cuticle; (4) sensory cilia; (5) dorsal position of gonads and spermathecae; (6) paired appendages; (7) presence of several membranes in the egg shell, resistant to desiccation (Esslinger, 1962a); (8) nine nymphal stages in Linguatula serrata (cf. Leuckart, 1860); (9) presence of a dorsal organ (absent in Annelida). The fossils described by Walossek & Müller (1994) and Walossek et al. (1994) were considered to represent larvae (Cave et al., 1998). Yet, these larvae do not look like recent pentastomid larvae. The discovery of the late Cambrian pentastomid fossils shed some light on the phylogenetic origin of the Pentastomida and suggested protoarthropod affinities (Walossek & Müller, 1994). However, miraculous fossil discoveries also have a disconcerting effect. While providing quantum leaps in our previous understanding, they produce quantum increases in our unanswered questions. The present picture of fossils seems dauntingly incomplete and enigmatic. Juvenile stages of Recent pentastomids live encysted in granulomatoma within vertebrate tissues and do not look very much like the described Cambrian juveniles. Pentastomids have been assumed to be the latest offshoot of the proto-arthropods, because they possess segmented limbs with pivoted joints between the articles (Maas & Waloszek, 2001). But even a basal arthropod position of pentastomids may be questioned. They have an anamorphic rather than a metamorphic development, would have lost a freeswimming larva, and do not have a comparable head tagma. Recent Pentastomida hatch with no more than two limb-bearing head somites and three trunk somites. There are two more anterior (progoneal) trunk somites in fossils. Karuppaswamy (1977) suggested that the pentastomid Raillietiella gowrii has β-chitin, like annelids have but that does not occur in arthropods, which have α-chitin. Pentastomids may thus not have an important arthropod apomorphy, but, as with many ultrastructural characters, more detailed knowledge is needed on the universality of this character within the group. The following evidence is in favour of pentastomids lying ouside the Arthropoda: (1) reduced number of metameres; (2) appendages reduced; (3) modified buccal appendages absent (Nicoli, 1963); (4) no free-living arthropod-like larvae. The unusual morphology of pentastomids has confounded attempts to find their relations within the animal kingdom (Jenner, 2004) and cladistic analyses using morphology fail to place pentastomids in arthropods (Giribet et al., 2005). P ENTASTOMIDS ARE ECDYSOZOANS Cuénot (1949) associated Pentastomida with Tardigrada and Onychophora, considering them to form a transition between annelids and arthropods. Pentastomids have been related

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Fig. 45B.2. Phylogenetic proposal for relationships between Tardigrada and Myzopharingea (Pentastomida + Nemathelminthes). [Adapted from Almeida et al., 2008.]

to the Tardigrada and Onychophora (Graff, 1877; Cuénot, 1949; Vandel, 1949; Weber, 1949) or derived from annelids or pro-articulates independently, or with some affinity with tardigrades (Kästner, 1955; Beklemishew, 1958; Von Haffner, 1971). More recently, Almeida et al. (2008a) have considered pentastomids to form a clade (Pentastomida (Facivermes + Nemathelminthes)). This clade and its sister group, the Tardigrada, were named Myzopharyngea (fig. 45B.2). Instead of considering Pentastomida as proto-arthropods, Almeida et al. (2008a) suggested that Pentastomida represent a transitional ecdysozoan group lying between Arthropoda and Nemathelminthes. The following evidence indicates that Pentastomida are Ecdysozoa: (1) haemocoel present (also referred to as a pseudocoel or myxocoel); (2) a chitinous cuticle (β-chitin) (Karuppaswamy, 1977); (3) cuticularization of the hooks of the penetrating apparatus; (4) anterior and posterior digestive tract chitinized (also in Tardigrada); (5) ecdysis, probably controlled by hormones; (6) lack of free cilia. According to our present knowledge, all we can say with certainty is that Pentastomida share ecdysozoan synapomorphies: a chitinous cuticle, moulting, a haemocoel, and the lack of free cilia. They apparently are not crustaceans, because their limbs are not composed of a proximal basipod and a distal endopod and exopod which seems to characterize most crustaceans. They do not look like euarthropods, because they do not bear segmented antennae on the head. Pentastomes do not display simplified morphology due to parasitism. They depict primary ecdysozoan characters suitable for parasitism already present in the Cambrian. The Cambrian fossil larvae have two appendage-bearing trunk somites not found in Recent Pentastomida. The presence of these anterior two portions of the trunk indicates that the pentastomids are not progoneate as occurs in some myriapods, i.e., the classes Diplopoda and Pauropoda (whereas Chilopoda and Symphyla are, of course, opisthogoneate) (cf. Osche, 1963), but the gonopore is located near the head in Recent forms because of the absence of the anterior portions of the trunk. The head appendages are three-segmented in both recent and fossil forms (considering the distal hooks as composing the third segment), with pivotal joints and arthrodial membranes between the limb’s articles (Maas & Waloszek, 2001). Fossil juvenile Pentastomida represent a stage of organization prior to those of recent pentastomes. The diversity of juveniles in the Cambrian suggests that the evolution

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of pentastomes began earlier than the late Cambrian. Their morphology illustrates an advanced adaptation to a parasitic way of life, such as for example in the gill chambers of fish (Junker, 2002). Conodonts were usually present in residues containing Palaeozoic pentastomes, as noted by Walossek & Müller (1994). These authors suggest they may alternatively have been parasitic in the pallial cavity or inside the valves of animals like some arthropods, brachiopods, or molluscs (Walossek & Müller, 1994). Since species of amphibians can act as final or as intermediate hosts for some of the Raillietiellidae (Ali et al., 1985), it is possible that the Carboniferous amphibian stock from which reptiles arose passed on their pentastomid parasites to the newly evolving amniotes (Haugerud, 1989). The pentastomid progenitor was conceivably a parasite of fish, which subsequently became adapted to an endoparasitic existence in aquatic reptiles, with the life cycle being established through predation (Riley et al., 1978). The more primitive cephalobaenids contain 8-11 ganglia and nerve pairs (Riley, 1986; Storch, 1993). Development is through a series of larval stages, with no metamorphosis.

MORPHOLOGY AND FUNCTION Body tagmata and appendages Pentastomids may be elongated, flattened, or cylindrical. The adults range from 1 mm to 15 cm in length. Fully mature females are larger than males (Abadi et al., 1996). The body of pentastomids consists of two tagmata, a short cephalothorax or head region, and an elongated, vermiform, trunk region (named abdomen by those researchers contending an arthropod or crustacean affinity of pentastomids). The two divisions have usually no clear line of demarcation, but they may be separated by a distinct neck (Hett, 1924) (fig. 45B.3). However, separation of the body into definite regions as in insects does not occur. In fact, there is little resemblance to arthropods, even though researchers were struck with a superficial resemblance to the larvae of mites (Mapp et al., 1976). Adults of all pentastome species are easily distinguished from any other parasite, because they bear two pairs of hollow, retractile hooks on either side of the mouth (Paré, 2008) (fig. 45B.4). The sucking mouth is supported by a chitinous oral frame (Junker, 2002) (fig. 45B.5) opening antero-ventrally in the midline, beside the two pairs of appendages that are each equipped with a terminal hook ventrally. These occur in most cases more anteriorly and laterally, often arranged in a crescent around the front of the head and with the mouth opening located in the centre. The limbs of extant pentastomids can be withdrawn in most species, by which the head seems to have five openings, giving the name of the group (Pentastomida = “five-mouths”) (Catellani et al., 2011) (fig. 45B.6). Adult pentastomids use their hooks to anchor themselves into the host’s tissues (Riley, 1986). In some genera, the cephalothorax becomes embedded in the mucosa of the host (Paré, 2008). Adults have no other external appendages (Mapp et al., 1976), but the external head morphology includes two pairs of sensory papillae frontally.

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Fig. 45B.3. Anterior view of Cubirea annulata. [Adapted from Kästner, 1968.]

The trunk may be finely annulated, as in most living species, worm-shaped, or dorso-ventrally flattened (leading to the alternative group name Linguatulida, or tongue worms) (Catellani et al., 2011). The trunk of extant pentastomids does not exhibit any signs of external division. Only the last trunk area, the non-somitic caudal end elongates extensively and becomes more conical and multi-annulated in advanced stages and adults (Esslinger, 1962a; Sachs et al., 1973; Riley & Self, 1979; Böckeler, 1984a; Riley et al., 1985; Winch & Riley, 1986a). The distinct external annulation gives an annelid-like appearance, but it is not matched by an internal segmentation. The very high number of annuli forming the trunk of Reighardia sternae is considered to represent secondary multiplications of true body segments (Osche, 1963; Legendre, 1967), an adaptation to parasitism (Heymons, 1926a; Von Haffner, 1926a). A similar elongation of the trunk is found in parasitic mites (Trombidiformes: Demodicidae and Tetrapodili: Eryhophyidae) (Legendre, 1967). The rings vary in number throughout the group, but are more or less constant for each species (Hett, 1924). The terminal or subterminal anus, absent only in Reighardia (cf. Böckeler, 1984a), is sometimes flanked by a pair of terminal papillae (Von Haffner, 1977; Riley, 1986; Storch, 1993) (fig. 45B.7). In extant taxa, they have been interpreted as sensory structures, as in Reighardia sternae (cf. Storch & Böckeler, 1982), or as a migrating apparatus for anchoring or crawling, as in Subtriquetra subtriquetra (cf. Winch & Riley, 1986b).

Body wall, body cavity, and locomotion The thin cuticle is chitinous (fig. 45B.8), untanned, and is soft enough to allow for peristaltic locomotion, similar to that of maggots (Riley & Banaja, 1975). Thus, it is the pressure of the haemolymph within the body that provides a hydrostatic skeleton for

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support and locomotion (Riley, 1986), rather than there being a rigid exoskeleton on which muscles can support flexor and extensor motions of appendages, as in arthropods. Von Haffner (1972) noted that the infective larvae of Neolinguatula nuttalli executed a fast and efficient crawling similar to that of leeches (fig. 45B.9). Esslinger (1962b) remarked that for Porocephalus crotali the extension of the appendages is performed by simple turgescence, comparing the anatomical structure with that of the head in Tardigrada. However, because the body wall is thin and elastic, the shape of the pentastomid body may be markedly affected by fixation. Riley (1986) concluded that an expanded head, previously considered the prime diagnostic character of the genus Kiricephalus (Fain, 1961; Riley & Self, 1979), rather constitutes a permanent property of alcohol-fixed material only. The external envelope of Pentastomida is richly ornamented. According to Doucet (1965), the cuticular covering is divided into two parts, a thin exocuticle and a thicker endocuticle. In the four species studied, Porocephalus subuliferum, Raillietiella boulengeri, Sebekia minor, and Armillifer armillatus, glandular cells of uncertain function open to the surface (Doucet, 1965; Legendre, 1967). The pentastome cuticle is similar to that of arthropods, although simpler (Trainer et al., 1975). While Annelida, Coelenterata, Mollusca, and Brachiopoda contain the β form of chitin in their cuticles (Rudall, 1955), α-chitin is the only form present in all arthropods (Dennell, 1960). As the occurrence of β-chitin was detected in Raillietiella gowrii, it was suggested that Pentastomida could be considered an independent phylum (Karuppaswamy, 1977). Perhaps β-chitin is plesiomorphic in relation to α-chitin, and thus this character, if confirmed to occur in all pentastomids, would corroborate the exclusion of Pentastomida from Arthropoda. The internal organs are suspended in haemolymph (Parré, 2008). The body cavity can thus be classified as a haemocoel. The adult has no coelomic pouches, nor are the muscle fibres associated into muscle blocks (Mill & Riley, 1972).

Fig. 45B.4. Mouth hooks in Pentastomida. A, Hook of male Cephalobaena tetrapoda [adapted from Rego, 1983]; B, the double-hook of an infective larva in a U-shaped fulcrum, and, C, the singlehook of a 5th -stage larva of Raillietiella gehyrae [adapted from Ali & Riley, 1983]; D, anterior hook in an adult female of Raillietiella amphiboluri [adapted from Mahon, 1954]; E, anterior hook in Reighardia sternae [adapted from Riley, 1973a]; F, anterior hook in immature Hispania vulturis [adapted from Martínez et al., 2004]; G, hook and fulcrum of Sebekia oxycephalum [adapted from Rego, 1984]; H, anterior, and, I, posterior hook of adult female, as well as, J, anterior, and, K, posterior hook of larva of Sebekia mississippiensis [adapted from Motta, 1964]; L, a sharply curved outer hook of Diesingia megastomum [adapted from Self & Rego, 1985]; M, anterior, and, N, posterior hook in Porocephalus clavatus [adapted from Fain & Mortelmans, 1960]; O, posterior hook and fulcrum of Alofia platycephalum [adapted from Self & Rego, 1985]; P, hook of adult Diesingia kachugensis, showing shaft and double hook [adapted from Shipley, 1910]; Q, hook in infective larva of Subtriquetra rileyi [adapted from Junker et al., 1998]; R, inner, and, S, outer hook in larva of Linguatula multiannulata [adapted from Von Haffner, 1973]; T, lateral hook of nymph VI of Porocephalus crotali [adapted from Esslinger, 1962a]. [Legends: b, base of mouth hook; cf, cuticular fold or auxiliary hook; f, fulcrum; h, external, clawlike portion of mouth hook.]

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Fig. 45B.5. Buccal frame in Pentastomida. A, In male of Cephalobaena tetrapoda [adapted from Rego, 1983]; B, in Raillietiella venteli [adapted from Motta, 1965]; C, in adult male of Reighardia sternae [adapted from Riley, 1973b]; D, in adult male Sebekia oxycephalum [adapted from Self & Rego, 1985]; E, in infective larva of Subtriquetra rileyi [adapted from Junker et al., 1998]; F, in nymph VI of Porocephalus crotali [adapted from Esslinger, 1962b]. [Legends: mo, mouth; mr, mouth ring; op, oral papilla; p, pharynx.]

Pentastomids have cross-striated muscles arranged in two layers, circular and longitudinal (Doucet, 1965; Mill & Riley, 1972; Storch, 1993). Dujardin (1845) was the first to notice the striated nature of pentastomid body wall muscles. Later Von Haffner (1924a) established that all pentastomid muscles are cross-striated. Summarizing, the body wall musculature is composed of two layers, longitudinal and circular, with obliquely oriented strands at intervals along the length of the body (Mill & Riley, 1972). Cross-striated muscles also appear in arthropods, whilst the musculature of annelids is obliquely striated (Knapp & Mill, 1971; Mill & Knapp, 1971). Also the attachment of muscle cells onto the integument is similar to that of Arthropoda (Banaja & Riley, 1974). On the other hand, the arrangement into two layers is typical of annelids. Muscle insertions are not associated with apodemes or apophyses in the cuticle, as they are in insects (Trainer et al., 1975).

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Fig. 45B.6. Anterior region of Cephalobaena tetrapoda. [Adapted from Kästner, 1968.]

Fig. 45B.7. Posterior end of body in Pentastomida. A, Of female Raillietiella furcocercum, showing postanal etensions [adapted from Rego, 1984]; B, in Sambonia clavata [adapted from Fain & Mortelmans, 1960]; C, in Linguatula serrata [adapted from Sambon, 1922]; D, in Elenia australis [adapted from Heymons, 1932]; E, in female Waddycephalus longicauda (arrows indicate postvaginal annuli 1-9); and, F, in female Waddycephalus superbus (arrows indicate post-vaginal annuli 1-4) [adapted from Riley & Self, 1981b]. [Legends: g, gonopore; i, intestine; v, vagina.]

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Fig. 45B.8. Schematic cross-section of body in Pentastomida. A, Raillietiella, and B, Reighardia [adapted from Von Haffner, 1967]; C, Kiricephalus coarctatus [adapted from Von Haffner, 1926a]. [Legends: bg, body glands; cm, circular muscles; dlm, dorsal longitudinal muscles; go, gonads; i, intestine; lsp, lateral sinus papillae; n1, n2, nerves; nc, nerve cord; ov, ovary; tr, transversal muscles; ut, uterus; vlm, ventral longitudinal muscles.]

Fig. 45B.9. Locomotion in Pentastomida. A-E, Stages in the peristaltic locomotion of Linguatula multiannulata. [Adapted from Von Haffner et al., 1969.]

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Moulting and growth In extant species the number of moults is variable according to species and even according to sex. About ten instars may occur in pentastomids (Self, 1969). Nine have been described in Raillietiella gehyrae (cf. Ali & Riley, 1983) and 12 in Linguatula serrata (cf. Leuckart, 1860). There might also be at least 12 moults in the complete life cycle of Raillietiella (Ali et al., 1982b), two or three more than in Porocephalus (Riley, 1981). Porocephalus crotali, as in Argulus, requires six moults to reach the infective stage (Esslinger, 1960, 1962a) and at least three more occur before the adult stage is attained (Ali & Riley, 1983). Differences in the number of moults may even occur within the same species, between male and female (Buckle et al., 1997). It seems that the moults show an asynchronous development; the moulting event does not occur in the same period for all semaphoronts of the same species, and neither do all features grow in parallel (Castellani et al., 2011). Basically, the size of any of the morphological structures found in a specimen is not considered sufficient evidence for discriminating among instars. However, a few features, such as the mouth structure, the cephalic appendages, or the number of pseudoannuli on the trunk, are considered the most reliable stage-discriminating features (e.g., Fain, 1964; Riley, 1981; Ali et al., 1981, 1982a, 1984a, b; Winch & Riley, 1986a), especially when authors are comparing species that are morphologically closely related (Castellani et al., 2011).

Sensory systems The sensory apparatus is reduced in pentastomids; eyes are absent. All pentastomids (larvae and adults) are well supplied with several structures, mainly located on the head, possibly representing sense organs (‘dorsal lobes’, ‘apical’, ‘terminal’ or ‘frontal’ papillae; e.g., Heymons, 1927, 1935; Osche, 1959, 1963; Von Haffner & Rack, 1965; Von Haffner, 1971; Wingstrand, 1972; Böckeler, 1982a, 1984b; Ali & Riley, 1983; Walossek & Müller, 1994). Their small size is part of an adaptation to a specialized endoparasitism in the respiratory tracts of vertebrates (Ali & Riley, 1985) (fig. 45B.10). According to Von Haffner & Rack (1965), the rich sensory papillae in Reighardia sternae favour the displacement of individuals in the aerial lumina of the hosts. Embryological investigations indicate that the early embryo of Reighardia carries four pairs of limb buds, each associated with ganglia and coelomic pouches (Osche, 1963; Doucet, 1965; Böckeler, 1984b). The first two limbs are later reduced to sense organs in the late larvae and adults. When the larvae hatch, they contain seven pairs of appendages corresponding to as many somites (Riley, 1986). These observations indicate that at least two pairs of sensory head papillae correspond to reduced appendages. We may note here that apparently similar sensory head papillae occur in adult tardigrades and some gastrotrichs and nematodes. Pending future comparative and ontogenetic studies, homology hypotheses involving these vestigial arthropod-like sensory structures may indicate phylogenetic relationships within the ecdysozoan clade.

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Fig. 45B.10. Sensory organs of the head in Pentastomida. Schematic representation of the left-hand side of the ventral cephalothorax of a female raillietiellid, showing the distribution of sensilla into four fields (1-4). The anterior frontal papilla (afp) carries three small (2-4) sensilla and one large sensillum; the posterior frontal papilla (pfp) carries a row of five sensilla. Field 4 covers three pairs of peribuccal sensilla (= secondary papillae) disposed as a broad arc across the front of the mouth. The mouth (mo) is flanked laterally by field 3, which carries four sensilla, aggregated as two pairs. The position of the extra sensilla in the male is indicated by an arrow [adapted from Ali & Riley, 1985]. [Legends: dp, dorsal papilla; fp, frontal papillae; pbp, peribuccal papillae.]

Papillae have traditionally been divided into two groups (Stiles, 1891b; Spencer, 1893; Ali & Riley, 1985). The so-called frontal papillae (= primary papillae) are a pair of conspicuous elevations usually located on the antero-ventral margin of the cephalothorax between the inner hooks. Peribuccal sensilla (= secondary papillae), which total about seven pairs, are distributed more generally over the cephalothorax (Hett, 1924). Hett (1924), after examining a number of porocephalids, discovered that there was some variation in the distribution of cephalic sensory papillae between particular genera. Some details of the anatomy of the sense organs of porocephalids, and their innervations, appear from the studies of Von Haffner (1926a, 1971), Doucet (1965), Von Haffner et al. (1969), and Hollis (1979a). Von Haffner et al. (1969), in particular, were able to discern small sensory cones (sensilla?) in the region of the frontal papillae of various species of Linguatula (Ali & Riley, 1985). Later, Von Haffner (1926b) described a chain of papillae extending down the lateral lines of the porocephalid Kiricephalus coarctatus; a similar situation occurs in Porocephalus crotali (cf. Hollis, 1979b) and in species of Armillifer (Riley & Self, 1981a). Ali et al. (1982b) were able to show that Raillietiella hebitihamata possesses chains of lateral papillae set between the abdominal annuli (= trunki annuli). The presence of minute annular pores, referred to as stigmata in the earliest descriptions (Shipley, 1898; Hett, 1924), appear to be a common feature in pentastomids, although their distribution may vary in each developmental stage and in different species (Banaja, 1983). In immature stages, the pores are regularly distributed in rows, but as the adult form is reached, their arrangement is obscured (Hett, 1924). The latter author found several rows in each trunk annulus in most sebekiid and porocephalid pentastomes, but only one row in Raillietiella and Linguatula. However, these pores are absent in Cephalobaena tetrapoda (cf. Von Haffner &

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Rack, 1971). Previous light microscopic studies have shown these pores to be openings of certain epidermal glands, which presumably function in excretion, respiration, nymphal cyst wall formation, secretion, or osmoregulation (Leuckart, 1860; Spencer, 1893; Shipley, 1898; Hett, 1924; Von Haffner, 1924b, 1971; Doucet, 1965; Cuénot, 1968; Riley, 1973a). Banaja et al. (1977) suggested that the “plugged” pores in Reighardia sternae, Porocephalus crotali, and Armillifer moniliformis belong to “chloride cells” that regulate the hydromineral balance of the pentastomid haemolymph (Banaja, 1983). Sensory cells associated with the lateral line system in the porocephalid Neolinguatula nuttalli may respond to very different stimuli, because, according to Von Haffner (1971), the necks of the cells terminate in a porous plate set in the cuticle. Clearly these cells may fulfil an osmoor chemosensory function (Ali & Riley, 1985). All sensilla appear to be of the mechanosensitive type and some of those positioned on the frontal papillae may have a tactile function, which enables the parasite to move and orientate within the confined spaces of a lung. The large dorsal papilla of raillietiellids may also be important in orientation (Ali & Riley, 1985). Both the sensory papillae and tracts of the ventral cephalothorax carry small spiky receptors that show a close correspondence, in virtually every detail under the scanning and the transmission electron microscope, to the sensilla of arthropods (Storch, 1979, 1984; Storch & Böckeler, 1979, 1982; Ali & Riley, 1985). In the old order Cephalobaenida, the papillae are less easy to observe (Hett, 1924), and most of the so-called secondary papillae seem not to be represented (Ali & Riley, 1985). Doucet (1965) demonstrated nervous connections to lateral papillae in Raillietiella boulengeri. In the genera Cephalobaena and Raillietiella there are only two pairs of large sensory papillae on the cephalothorax. A pair of elongate, backward-projecting, fingerlike papillae occurs on the dorsal surface at about the level of the anterior hooks. The other pair is located on the ventral surface of the cephalothorax, on either side, but in front of the mouth. Some confusion and inconsistency persists over the nomenclature of these papillae. The pair on the dorsal cephalothorax, not surprisingly, is called ‘dorsal papillae’ by Heymons (1926b) and Fain (1961). They are referred to as antenniform papillae by Hett (1924b), and ‘frontal papillae’ by Von Haffner (1971) and Von Haffner & Rack (1971). Those on the ventral surface, in front of the mouth, are variously termed ‘frontal papillae’ (Heymons, 1926b; Fain, 1961), ‘dorso-lateral papillae’ (Doucet, 1965), or ‘apical papillae’ (Von Haffner, 1971; Von Haffner & Rack, 1971). Doucet (1965) showed that each frontal papilla of Raillietiella boulengeri was in fact divided into two distinct regions, a broad, cone-like elevation carrying four small spiky sensilla and a smaller elevation nearer to the mouth, supporting two comparatively large spikes. Such a pattern may also exist in Cephalobaena tetrapoda (cf. Heymons, 1935). But the scanning electron microscope (SEM) studies of Storch & Böckeler (1979) showed, that many more small spiky sensilla were distributed around the mouth of Reighardia sternae, in addition to those on the frontal papillae. These authors divided the various types of sensilla into four fields (numbered 1-4). The account of Ali & Riley (1985) follows the notation of Heymons and Fain, and therefore papillae will here be called dorsal (the dorsally located, finger-like papillae) and frontal (the ventral pair situated on the anterior margin of the cephalothorax) (fig. 45B.10).

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The SEM studies by Ali & Riley (1985) of the frontal papillae (fields 1 and 2) and peribuccal cuticle (fields 3 and 4) of four species of raillietiellids belonging to three different taxa (see Ali et al., 1985), pursued two objectives: to ascertain the potentially diagnostic value of the distribution of these sensilla since, in many cases, species are notoriously difficult to identify specifically (Ali et al., 1981, 1982a, 1984b) and secondly, to compare the pattern within the genus Raillietiella to that described by Storch & Böckeler (1979, 1982) in a representative of the genus Reighardia. Ali & Riley (1985) concluded that sensory sensilla cannot be used in specific diagnoses. In Raillietiella, the dorsal papillae, although almost certainly fulfilling some sort of sensory function, appear bereft of obvious external features. Likewise, the podial and parapodial lobes that occur on the hooks carry a number of low-profile bumps (which again are probably sensory) but sensilla are absent. Thus, sensilla are limited to the extreme ventral tip of the cephalothorax (Ali & Riley, 1985). Hence, we can distinguish primary lobe-like papillae without sensilla from secondary peribuccal sensilla without lobe-like projections. Storch & Böckeler (1979) and Storch (1979, 1984) observed that the typical, arthropod mechanosensitive sensilla, where each receptor is surrounded by an inner sheath-cell enclosing a fluid-filled space containing a sensory cilium, appear more or less unmodified on the cephalothorax of Reighardia. Surprisingly, the adoption of an endoparasitic mode of life does not seem to have produced a concomitant reduction in the number of cuticular sense organs (Ali & Riley, 1985). Dorsal papillae and the anterior part of the frontal papillae (field 1) receive nerve fibres from the upper region of the supra-oesophageal ganglion, whereas the posterior frontal papilla (field 2) is innervated from the mid-region of the same ganglion (Doucet, 1965). There can be little doubt that at least some of the sensilla around the mouth (fields 3 and 4) are important in the location of suitable feeding sites in the lung (Ali & Riley, 1985).

Nervous system The anatomy of the nervous system of Cephalobaenidae and Porocephalidae is based on the studies of Doucet (1965) (fig. 45B.11). The nervous system is very similar in both families; a supraoesophageal portion may be interpreted as forming the brain and a suboesophageal nervous mass is ganglionated and arthropod-like. However, the central nervous system of pentastomids still represents a vexing problem. The major ganglia and nerve tracks appear to arise from a suboesophageal position. The actual circumoesophageal rind does not seem to connect the dorsal and ventral main ganglia, although the ring appears as well thickened with tracks. Thus different hypotheses could be generated to explain which conditions are primitive and which are derived. These specializations are no doubt a reflection of the anterior location of the mouth and the elaboration of the anchoring function of the hooks. At this time, then, it cannot be entirely discounted that these hooks are homologous to maxillules and maxillae. In Reighardia, three ganglia fuse to form the suboesophageal ganglion, while one remains solitary as the supraoesophageal ganglion, and ganglia 5-7 fuse to form another

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Fig. 45B.11. Anterior nervous system in Pentastomida. A, Cerebral ganglia of Raillietiella boulengeri [adapted from Legendre, 1967]; B, schematic representation of central nervous system in Reighardia sternae [adapted from Böckeler, 1984b]. [Legends: cpc, circumpharyngeal commissure; fn1, dorsolateral sensory nerve; fn2, dorsal parabuccal sensory nerve; fn3, parabuccal ventral nerve of inner anterior crochet; g1-3, first to third pair of ganglia; len, lateral oesophageal nerves reuniting into a supra-oesophageal ganglion; ln1-3, lateral nerves innervating parietal muscles and lateral sensory organs; n1-2, first and second nerves of the middle intestine; nap, nerve of apical papilla; nfp, nerve of frontal papilla; nh1, nerve to hook 1; nh2, nerve to hook 2; un2-3, unpaired nerves innervating middle intestine.]

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complex mass (Böckeler, 1984b). The cerebral mass of Raillietiella boulengeri is formed by two ganglia innervating the sensory organs and the anterior muscles of the head, the second ganglia innervating especially the buccal region and the sensory papillae near the first pair of hooks; also from the second cerebral ganglia originates the anterior pair of nerves (along the stomodaeal part of the anterior intestine) and the anterior median unpaired nerve running along the median intestine. These nerves form a sympathetic stomodaeal nervous system of Pentastomida, the second cerebral ganglion apparently representing the tritocerebrum. The third pair of ganglia is suboesophageal, innervating the first pair of hooks; the fourth pair of ganglia innervates the second hooks; the ganglia of the fifth, sixth, and seventh pairs innervate, respectively, the various portions of the genital organs; the eighth pair gives rise to the abdominal nerve chords that extend along the trunk. However, this disposition may present variations and the anterior ganglia (cerebroid) may function together, and even fuse, with the following ganglia, not forming a supraoesophageal part distinct from the suboesophageal portion, as apparently happens in Reighardia sternae (cf. Osche, 1963; Von Haffner & Rack, 1965; Legendre, 1967). In the Porocephalida there is a single compact suboesophageal ganglion (Storch, 1993). The neuro-anatomical data provided by Böckeler (1984b) in particular appear to leave very little possibility for interpreting the nervous system as secondarily modified or simplified from a state as developed in the in-group eucrustaceans (Waloszek et al., 2006).

Digestive system, food, and feeding The digestive tract in Pentastomida is straight and tubular, and it ends in a posterior rectum (or cloaca in most porocephalids). The mouth is cylindrical, sustained by a chitinous buccal ring; the anus is terminal or subterminal, but lacking in Reighardia sternae (cf. Thomas & Böckeler, 1992b; Storch, 1993). The pharynx forms the anterior part of the digestive tube, and is delimited by two chitinous plates (a ventral and a dorsal plate) with powerful muscular bands inserting on the chitinous buccal frame, that make the dorsal plate move, thus functioning as a true pharyngeal pump that sucks the food (fig. 45B.12). The innervation of these muscles is provided for by nervous ramifications originating from the posterior suboesophageal ganglia; these nervous formations may be referred to the stomatogastric nervous system (= anterior unpaired sympathetic) (Doucet, 1965; Legendre, 1967). A cylindrical oesophagus, strongly chitinized, extends from the pharynx to the non-chitinized middle intestine; however, an eminently chitinized conical trunk bulges into the lumen of the middle intestine; this valve apparently prevents reflux of the digestive matter back into the pharynx (Doucet, 1965; Legendre, 1967). The middle intestine is lined with an epithelium of high cells. Anatomically, the external tunic is bordered by internal circular muscles overlapped by external longitudinal fibres (revealed to be true microvillosities under the electron microscope). A pyloric valve leads to a relatively short posterior intestine, which ends in the anus. The entire course of this intestine (posterior digestive tract) is chitinized. There are glands attached to the digestive tube; anteriorly, voluminous glands project into the buccal cavity, and visceral glands project into the middle intestine (Legendre, 1967). Glands similar to the chloragogen

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Fig. 45B.12. Anterior digestive tract and feeding in Pentastomida. A, Schematic representation of anterior digestive tract in Reighardia sternae; B-D, schematic representation of stomodaeal pump mechanism during the feeding process [adapted from Thomas & Böckeler, 1992b]. [Legends: am, anterior pharyngeal muscles; hg, head glands; mg, midgut; t, tongue; tm, transversal muscle.]

glands of Clitellata (Annelida) are also associated with the digestive tract (Doucet, 1965; Self, 1969). One must keep in mind, however, that these glycogen storage-rich areas of the digestive tract may simply represent a functional analogy with the storage cells of in the intestine of annelids (Thomas et al., 1999a). Adults and larvae are haematophagous parasites that feed on the blood from ruptured capillaries of their host via a sucking mouth (Doucet, 1965; Riley, 1973b, 1986), with the exception of species of Linguatula, which feed on blood cells, tissue fluids, and nasal secretions (Olson & Cosgrove, 1982; Storch, 1993; Paré, 2008). Pentastomids depend for feeding on the blood of their hosts but, unlike arthropods, they are devoid of modified piercing, biting, or sucking extremities. Therefore, they depend on a sucking mechanism provided by two rigid plates in the pharynx and several bundles of muscles that are inserted dorsally (Thomas & Böckeler, 1992a, b). Digestion takes place extracellularly in Raillietiella (Thomas et al., 1999a, b), because large quantities of haematin form in the gut lumen (Rao & Jennings, 1959; Riley, 1972a). Yet, some intracellular digestion occurs as well, since iron accumulates in certain gastrodermal cells that are then shed periodically into the intestinal lumen (Riley, 1986).

Reproductive system, reproduction, and chromosome number Pentastomes are dioecious and sexually dimorphic (Junker, 2002) (figs. 45B.13-14); fertilization is internal (Riley, 1986). As in most parasites, the body structure of pentastomids is designed for a truly massive production of eggs. Most of the body mass is represented by the trunk, which becomes enlarged due to a gradual increase of the dorsal gonads and, in females, of the uterus. Female egg production may exceed two thousand

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Fig. 45B.13. Reproductive organs in Pentastomida. Schematic representation of body plan in: A, male, and, B, female, of a cephalobaenid [adapted from Riley, 1983]; C, diagrammatic representation of female reproductive system in a porocephalid [adapted from Riley, 1986]. [Legends: an, anus; br, brain; di, dilatator; eb, ejaculatory bulb; gp, genital pore; i, intestine; li, ligament; mo, mouth; o, ovary; ov, oviduct; s, spermatheca; sc, sperm cells; sp, spermatocytes; sr, seminal receptacle; sv, seminal vesicle; te, testis; u, uterus; vd, vas deferens; vnc, ventral nerve cord.]

eggs per day. Fecundity may be influenced by several factors, such as the immunological response of the host and the quantity of pentastomids present in each parasitic infestation (Riley, 1983, 1986, 1988, 1992a; Storch, 1993; Almeida & Christoffersen, 2002). Females are relatively larger than males but, as a rule, they occur in smaller numbers in a parasitic infestation (Riley, 1986; Almeida & Christoffersen, 2002). A single copulation is present in the life cycle (fig. 45B.13). Females are monogamous, whereas males can copulate with more than one female (Riley, 1983). Females copulate precociously, before the full development of the uterus. Sperm becomes stored in the spermathecae (Self, 1969; Riley, 1983, 1986; Storch, 1993; Almeida & Christoffersen, 2002). Males die soon after copulation in many species of pentastomids. The copulatory period is considered critical for both sexes (Riley, 1986). An absence of males may retard the development of females and an absence of females may prolong the longevity of males (Almeida & Christoffersen, 2002). That copulation happens only once in the lifetime of a female, when both sexes have attained a similar length, represents an unusual aspect of pentastomid reproduction (Storch et al., 1990). Sperm is stored in the female’s spermathecae for up to an estimated 19 years, according to Riley (1983).

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Fig. 45B.14. Copulation in Pentastomida. A, In Armillifer mazzai, illustrating the way in which the tip of the trunk of the female fits into a groove on the ventral side of the male [adapted from Riley, 1992]; B, in Armillifer armillatus [adapted from Sambon, 1922].

In Armillifer, copulation occurs when the paired penis threads travel along the vagina/uterus to at least the level of the anterior spermathecae. Thus, the male genitalia are appropriately modified to conduct sperm cells directy into the spermathecae. The spermathecae probably function to isolate the sperm completely from external influences. Stored sperms remain metabolically inactive and quiescent (Riley, 1986). The genital organs of Pentastomida are believed to be initially paired, but they fuse secondarily. They are located dorsally along the entire length of the trunk cavity. The genital pore of the male, which is anterior in position, is flanked by one of the pairs of peribuccal sensilla or secondary papillae (Hett, 1924) (fig. 45B.10). The anterior position of the gonopore in cephalobaenids is most likely nothing more than a retention of its original position between trunk somites and the non-somitic ‘caudal end’, when the two trunk somites were lost in Recent forms (Walossek & Müller, 1994). The male genital system of Cephalobaena tetrapoda comprises the unpaired posterior testis, anteriorly a single seminal vesicle, and the paired connecting tubes, ejaculatory bulbs, vasa deferentia, and a dilator (fig. 45B.15). Details of the male organs and of the intromittent organ of Raillietiella amphiboluri were provided by Mahon (1954). In the Porocephalida, males normally have an unpaired testis and paired (or a Y-shaped) seminal vesicle(s) leading into the vasa deferentia. At the junction of seminal vesicles and vasa deferentia, ejaculatory ducts open into the system. The cirri are extremely long, coiled tubes that are located within a spacious cirrus sac. Further details of their structure and function are provided by Storch et al. (1990). Sperm development takes place in the unpaired testis. Through a helical opening the male gametes are released into the unpaired seminal vesicle, where they are kept until copulation. They are then released through paired and very thin connecting tubes into the

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Fig. 45B.15. Genital system of the male in Pentastomida. A, Schematic representation of the male genital system of Cephalobaena tetrapoda [adapted from Mahon, 1954; Böckeler & Storch, 1990]; B, ventral view of male organs in Raillietiella amphiboluri [adapted from Böckeler, 1990]; C, semidiagrammatic representation of the male reproductive system in Reighardia sternae [adapted from Riley, 1973a; Böckeler & Storch, 1990]; D, schematic representation of copulation apparatus in the male of Linguatula serrata [adapted from Riley, 1973a]; E, schematic representation of the male genital system of Porocephalus crotali [adapted from Storch et al., 1990]. [Legends: ca, copulations apparatus; ci, cirrus; co, copulatory organ; cs, cirrus sac; ct, connecting tube; di, dilatator; dr, dilatator rod; drs, dilatator rod sac; eb, ejaculatory bulb; ed, ejaculatory duct; es, ejaculatory sac; g, gland; gp, genital pore; i, intestine; n, ventral nerve cord; pgd, paired genital ducts; s, spicule; sv, seminal vesicle; t, testis; ugd, unpaired genital ducts; vd, vas deferens; vs, vesicula seminalis.]

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ejaculatory bulbs, which — because of their extensive, cross-striated musculature — must be considered to provide the driving force during ejaculation. The ejaculatory bulbs release the sperm cells via the vasa deferentia, which merge with a complicated dilator. After merging, the vasa deferentia lose their epithelium and become cuticular tubes. The dilator is an ectodermal invagination that is lined by cuticle. The dilator probably serves to guide the cirrus into the genital tract. Furthermore, the male genital atrium can be extended, thus building a male copulatory organ and enabling the cuticular tubes to penetrate the female openings (Böckeler & Storch, 1990). In Porocephalida, males have paired seminal vesicles with connecting tubes that lead from their anterior end. The ejaculatory bulbs may be much more elongated than in Cephalobaena tetrapoda. The distal parts of the vasa deferentia (cirri) are coiled tubes that terminate in a thin, sclerotized top; they are normally located in a spacious cirrus sac (Böckeler & Storch, 1990). Spermatogenesis occurs in closed cysts that conduct filamentous spermatozoa of 200 μm long (Armillifer armillatus), having distinct caudal and cephalic extremeties (Doucet, 1965; Legendre, 1967). The mature spermatozoa are distinctly filiform, a necessary attribute facilitating the passage of sperms along the narrow, elongate penis and through an even narrower spermathecal duct (Riley, 1983). The unpaired testis of Raillietiella spp. is a thin-walled sac lying mostly in the posterior half of the trunk, and is connected to the dorsal body wall by a median mesentery. Its epithelium consists of two types of cells, predominantly phagocytic vegetative cells, whose role is to recycle debris suspended in the vesicular lumen, and germinal cells (primary spermatogonia); these latter cells correspond to the “nutritive” and “germinative” cells of Von Haffner (1924b) (Wingstrand, 1972). As in most parasites, the female reproductive system is quite complex and composed of several parts (fig. 45B.16). In most species the ovary is simple but in some it may be divided anteriorly or posteriorly (Heymons, 1922; Fain, 1961; Nørrevang, 1972), indicating that it was originially a paired organ (Nørrevang, 1983). Ovaries are peculiar inasmuch as mature oocytes are located on the outside of the ovary where they are bathed directly in haemolymph (Nørrevang, 1972, 1983; Böckeler, 1984b; Walldorf & Riehl, 1985). Oocytes migrate to this position via the ovarial lumen, into which they are liberated from germinal epithelia; they are finally supported by a stalk cell and separated from the haemocoel by a thin basal lamina. A cover of microvilli enables oocytes to absorb some nutrients from the haemolymph but the source of yolk appears to be different in different stages of the oogenesis (Nørrevang, 1983). In Reighardia, an accessory genital gland may be partially responsible for yolk production (Böckeler, 1984b). The bulk of the haemocoel of mature females is occupied by the uterus, which contains eggs in various stages of development (Riley, 1986). In the pentastomids paired spermathecae are found at the junction of the oviduct and the distal uterus, and, because the uterus expands enormously during development, they become progressively more remote from the vagina (Riley, 1986). This contrasts with many arthropods that possess a seminal receptacle or spermatheca near the vagina (Chapman, 1971).

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Fig. 45B.16. Female reproductive system in Pentastomida. A, In Diesingia megastomum [adapted from Fonseca & Ruiz, 1956]; B, dissected female of Armillifer grandis in ventral view [adapted from Hett, 1915]. [Legends: cov, cut end of left oviduct; i, intestine; ov, oviduct; rov, right oviduct; rs, receptaculum seminis; sp, spermatheca; ut, uterus.]

During insemination, sperm must be placed directly within the spermathecae from the tips of the paired penes of the male. This transfer occurs only in the early development of females, before the uterus has developed (Sambon, 1922). Thus, females display a precocious sexual development with their once-in-a-lifetime event of insemination (Riley, 1981, 1983; Ali & Riley, 1983). Spermathecae combine two functions: they store sperm and, after an interval of many years, they provide for the continuous fertilization of oocytes (Riley, 1986). Oogenesis produces “oogonia” of 70 μm in diameter, covered by a membrane of 2 μm; it is in this form that the female gametes enter the oviduct and accomplish the first

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maturation division; the expulsion of the secondary polar globules only occurs with the penetration of the spermatozoa (Doucet, 1965; Legendre, 1967). With the exception of Reighardia (Banaja et al., 1976), ovulation and egg deposition in pentastomids are continuous processes (e.g., Riley, 1981; Ali & Riley, 1983; Winch & Riley, 1985), although Nørrevang (1972, 1983) provided some evidence that in Raillietiella hemidactyli oocytes are not produced beyond a given time in the life of the female. Essentially, the vagina in raillietiellids consists of two functionally distinct regions, a chitinous cylinder next to the uterus, which is surrounded by an epidermal layer and by longitudinal and circular muscle systems — this performs the sieving of egg size — and a wider anterior region lined by epidermis, which temporarily stores eggs before release. The cylinder, which is substantially narrower than an egg, is filled by a thick amorphous matrix pierced by an exceedingly narrow lumen. This matrix clearly acts as a physical barrier to the exit of eggs, but at the same time it must be easily deformable so that, when mature eggs of the appropriate dimensions lodge in the uterus end of the system (triggering stretch receptors?), muscle contraction can force eggs through by peristalsis (Riley, 1986). The following numbers of chromosomes have been reported in species of pentastomids: Raillietiella boulengeri, 2N = 8; Sebekia minor, 2N = 14; Armillifer armillatus, 2N = 20; and Porocephalus subuliferum, 2N = 24 (Doucet, 1965; Legendre, 1967).

DEVELOPMENT AND LIFE HISTORIES Development is very variable among species, and ranges from indirect, with several successive nymphal (or larval) stages, to direct development. When the larvae hatch, they contain seven somites (Riley, 1986).The embryonic phase (Böckeler, 1984b) ends with a pre-hatchling still within the eggshell, the so-called primary larva or nymph. This late embryo consists of a head with the mouth region and two pairs of hook-like appendages, and the hind body, which is shorter than the head. The hatching larva, about 250 μm long, may be rather mobile and resembles the pre-hatchling in having a swollen head region and two pairs of limbs and a trunk part. New features of it are the frontal papillae and another frontal structure in the form of a chitinous rod to penetrate the host’s gut wall; this apparently occurs in the hatchlings of all living taxa. The conically tapering larval trunk may be of different length and ends in a pair of caudal papillae. These may be hump-shaped or spine-like and aid as sensory structures (Storch & Böckeler, 1982) and, in the case of Subtriquetra subtriquetra, as locomotory structures (Castellani et al., 2011). After having penetrated the gut wall of their host, the larvae migrate through the body cavity. They moult several times during this phase, which may last up to several weeks. During their movements, the larvae change morphologically, mainly reducing the penetrating apparatus and elongating their trunk enormously. The infective larvae attain maturity in the respiratory tract of the definitive host (Buckle et al., 1997; Castellani et al., 2011).

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The hatching larva of Reighardia sternae does not correspond to the first stage larva of other pentastomids, but more likely represents a stage similar to the infective larva, which is the fourth stage in Raillietiella (Thomas et al., 1999c). The early embryo of Reighardia carries four pairs of limb buds, each associated with ganglia and coelomic pouches (Osche, 1963; Doucet, 1965; Böckeler, 1984b). The first two limbs later reduce to sense organs in the late larvae and adults.

Embryonic development The embryonic development of Pentastomida (fig. 45B.17) is accomplished inside several embryonic envelopes. Formation of the egg membranes in Reighardia and raillietiellids begins when the oocyte is a mere 7-15 μm in diameter (Riley, 1986). Osche (1963) distinguishes two membranes in Reighardia sternae: an external membrane produced by the organ of the embryo (role still enigmatic) and an internal membrane corresponding to the blastodermic cuticle; in this species the chorion (of ovular origin) is soon rejected and it does not adhere to the embryonic membranes; this is not the case in young embryos of Raillietiella boulengeri and of Armillifer armillatus observed by Doucet (1965) a little before eclosion, because this author cites four membranes: the outer chorion, a mucous substance corresponding to the external envelope of Osche, the initial blastodermic cuticle and the new embryonic cuticle; at eclosion, the mucous substance provokes the rupture of the chorion, while the larva sheds the old blastodermic cuticle. The egg of Porocephalus crotali, studied by Esslinger (1962a), also has two membranes, the inner of which is stratified into three zones; for that author, the dorsal organ of the embryo, following the opinion of several classical authors, is a strictly glandular structure. Osche (1963) demonstrated that the dorsal organ elaborates the outer membrane of the embryo of Reighardia sternae, which is confirmed by Doucet (1965) for Raillietiella boulengeri and

Fig. 45B.17. The embryo of Pentastomida. A, lateral view, and B, schematic representation of sagittal section through an embryo of Reighardia sternae [adapted from Osche, 1963]. [Legends: a, archicerebrum; ac, antennular coelom; bc, blastodermic cuticle; cc, cephalic curvature; co, collar; cp, caudal papilla; dc, deutocerebral ganglion; do, dorsal organ; ep, epidermis; fa, first antenna; gp, germinal primordial; md, mandible; mi, middle intestine; mx, maxillae; pc, pore collar; pmc, premandibular coelom; pmm, postmaxillar mesoderm; po, pore of dorsal organ; pr, proctodaeum; sa, second aantennae; scdo, secretory cells of dorsal organ; st, stomodaeum.]

CLASS EUPENTASTOMIDA

39

Armillifer armillatus. In these latter species there is a secretion of a mucus that is rich in acid mucopolysaccharides, leading to the hypothesis that the dorsal organ has a different function at the beginning vs. towards the end of embryonic life. It is becoming clear that Reighardia has two egg layers, cephalobaenids and raillietiellids have three distinct egg layers, whereas porocephalids have four (Riley, 1986). The innermost, a chitinous epidermal secretion of the embryo itself, is termed a blastoderm cuticle (Osche, 1963; Böckeler, 1984b), and is overlain by a spongy mucous layer secreted through a pore in the eggshell by a complex of cells in the mid-dorsal region of the embryo that collectively constitute the dorsal organ (Osche, 1963). In the uterus, the mucous layer is delimited by a very thin layer that Riley (1983) termed a chorion. By contrast, the outermost layer of the raillietiellid egg is a definitive shell (Heymons, 1926c; Doucet, 1965; Esslinger, 1968), which in Raillietiella gigliolii is thick and brittle (Winch & Riley, 1985): the mucous layer is still present but is now sandwiched between the two eggshells and swells only when the outer eggshell is ruptured (Riley, 1986). These three components are still present in porocephalids and in the same order, but external to the whole assemblage is another layer (Heymons, 1935; Esslinger, 1962c), which swells to form an obvious hyaline capsule in water. This is clearly not homologous with the dorsal organ secretion, and because it lies outside the outer eggshell it must derive from a secretion from the female’s reproductive tract (Riley, 1986). The egg envelopes of Subtriquetra subtriquetra have become secondarily reduced to a single, thin, flexible membrane (Vargas V., 1975), an obvious adaptation to an aquatic, free-living existence, but the presence of a dorsal organ may indicate the involvement of a mucous layer (Vargas V., 1975). The embryo of Reighardia sternae has an antennal and three appendicular projections. The walking appendages are divided into a coxa and a telopod, similar to the situation in arthropods. The epidermis of embryos is unistratified and the central nervous system is derived from the ectoderm. A protocerebrum is absent (associated with the absence of vision), the brain being formed by the deutocerebrum and tritocerebrum. The mesoderm forms five true metameres, one preoral and four postoral (which are considered homologous to the Ant1, Ant2, Md, and Mx of crustaceans by some, plus “post-maxillae” without appendages) (Osche, 1959, 1963). Doucet (1965) confirms these mesodermic formations in Raillietiella boulengeri and Armillifer armillatus, and further complements the information on embryonic segmentation: equal divisions produce a sterroblastula with a virtual blastocoel. Segmentation is of the spiral type. Cleavage in Raillietiella boulengeri, although initially equal, becomes spiral by the eighth blastomere stage (Doucet, 1965), as in annelids. Blastodermic cells are formed by delamination. The blastula carries a dorsal organ. The endodermic cells organize late in the archenteron. The primary coelom does not persist in adult Pentastomida, in which the adult general cavity corresponds to a mixocoel (Legendre, 1967). Böckeler (1984b) concluded that originally pentastomids might have had three trunk somites, followed by a non-metameric caudal end carrying the anus. Later stages do not develop additional ganglionated structures, which implies that early pentastomid larvae already possess the final (= adult) number of trunk segments (Castellani et al., 2011).

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The so-called dorsal organ of pentastomids is an embryonic gland, and thus most suitably called an embryonic gland. According to Stendler-Seidel et al. (1997), it is not homologous to the dorsal organ of adult arthropods. It remains to be demonstrated if the embryonic dorsal organ that appears in crustaceans (including pentastomids) and many other arthropods, are or are not homologous structures (Martin & Laverack, 1992). This possible homology is one of the arguments sustaining that pentastomids are closely related to branchiuran crustaceans. However, it appears that in this case a transitory embryonic pentastomid character is being compared to an adult arthropod structure, and obviously the validity of such a comparison must as yet remain uncertain. The eggs are typically large (100 to 200 μm), with a thin, external shell surrounding an ovoid, mite-like primary larva (Bowman, 1995). There may be quite a lot of empty space between the larva and the shell. Hooklets at the anterior end of the larva, and either budding or short, stumpy limbs are often identified in mature eggs with the aid of a microscope (Paré, 2008). Egg hatching is infective to the next host in the life cycle, which necessarily acquires it as a contaminant in food or water, with the exception of Subtriquetra (Riley, 1986). The eggs of Subtriquetra hatch internally in the nasal passages of captive caimans (Winch & Riley, 1986a). Eggs of Porocephalus crotali hatch in the duodenum of rodents (Penn, 1942; Esslinger, 1962c) and those of Kiricephalus coarctatus hatch in the upper intestine of amphibian tadpoles (Guidry & Dronen, 1980); in both species hatching occurs within 30 minutes (Riley, 1986). The hatching of Raillietiella eggs has been observed in the crop and intestine of insects that are intermediate hosts (Ali & Riley, 1983; Winch & Riley, 1985); Raillietiella gigliolii nymphs develop in the larva of the scarabaeid Coelosis biloba (cf. Riley, 1986). Eggs remain viable for long periods in water (Penn, 1942; Keegan, 1943a; Esslinger, 1962a) and are tolerant to acids and preservatives (Salazar, 1965), but show variable responses to drying (Keegan, 1943a; Esslinger, 1962a). All eggs contain fully developed primary larvae at the time they are shed by the female into the host’s respiratory tract, and they are immediately infective to the next host (Riley, 1986).

Larval development The primary larvae resemble mites. In addition, the larvae possess a circular, ventral mouth and two pairs of hooks in the anterior end (Abadi et al., 1996) (fig. 45B.18). It is assumed that, after hatching, the primary larvae mechanically penetrate the gut using the penetration apparatus combined with an offset breast-stroke action of the hooked limbs (Self, 1969; Guidry & Dronen, 1980). Sites of penetration are visible as haemorrhagic spots on the wall of the intestine (Esslinger, 1962b, c). Both Fain (1961) and Esslinger (1962a) described gland cells with ducts opening onto the penetration apparatus of porocephalid primary larvae, and it is possible that histolytic secretion also assists passage through tissues (Riley, 1986). Extant larvae hatch with a mouth and an anus. During development the mouth area undergoes several transformations (for example extension

CLASS EUPENTASTOMIDA

41

Fig. 45B.18. Development in Pentastomida. A, Mature egg; B, larva in ventral view; C, first nymphal stage (nymph I); D, nymph II; E, nymph III; F, nymph IV; G, nymph V (stigmata not shown); H, nymph VI (infective stage); A-H, all of Porocephalus crotali [adapted from Esslinger, 1962a, b]; I, primary larva of Porocephalus subuliferum [adapted from Von Haffner, 1973]. [Legends: ac, anterior neutrophilic granular cell; bd, sclerotized leg bud; ce, leg with claws extended; cw, leg with claws fully withdrawn; do, dorsal organ; dt, duct associated with penetration apparatus; ec, eosinophilic granular cell; es, oesophagus; fu, fulcrum; fg, foregut; fl, fluid-filled space; ga, circumoesophageal ganglion; gt, sacklike gut; hg, hindgut; ic, inner shell complex; lf, lateral fork of penetration apparatus; lh, lateral mouth hook; lv, larva; mg, midgut; mgo, male genital opening; mh, medial mouth hook; mo, mouth; mr, mouth ring; om, outer shell membrane; pa, papilla; pc, posterior neutrophilic granular cell; ph, paired hooks; sp, median spear of penetration apparatus; st, stigma (on dorsal surface); tl, tail; ts, terminal segment.]

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M. L. CHRISTOFFERSEN & J. E. DE ASSIS

of the oral region or translocation of the mouth; Von Haffner, 1973) and the V- or ringshaped chitinous structures surrounding the mouth opening become increasingly more sclerotized in more advanced stages (Castellani et al., 2011). The podia of the primary larvae transform into the hooks of the secondary larvae and persist to the adult stage (Legendre, 1967). The cephalic hooks increase significantly in size during development, and some species develop a secondary hook that is lost in adults (Castellani et al., 2011). Böckeler (1984b) demonstrated that the larvae of Reighardia sternae hatch with four head and three trunk metameres, and that two more body segments are added during postembryonic development. Hence, larvae and adults possess the same number of body segments, which may be extrapolated for Pentastomida in general (Walossek & Müller, 1994). Only the caudal region elongates extensively during development and becomes more or less regularly annulated in Pentastomida (pseudo-metamerism, according to Böckeler, 1984a). The secondary larva of Reighardia sternae has distinct cuticular ornamentation (Von Haffner & Rack, 1965; Legendre, 1967). The primary larva is separated from the infective stage by between six and eight moults in Linguatula (Leuckart, 1860), Porocephalus (Stiles, 1891a, c; Esslinger, 1962b), and Sebekia (Winch & Riley, 1986b) in vertebrate intermediate hosts (Riley, 1986). Intermediate instars lack hooks and early instars are devoid of external segmentation. Hooks are retained by some of the instars in species of Sambonia (Fain & Mortelmans, 1960), and by all instars of Reighardia and Subtriquetra, which are at all times freely mobile (Banaja et al., 1975; Winch & Riley, 1986a). Larvae show active site selection; Linguatula prefers bronchial and mesenteric lymph nodes (Sachs et al., 1973); Armillifer armillatus in man invades the liver, intestine and mesenteries (Hopps et al., 1971); Porocephalus crotali in mice and rats favours fatty tissue around the reproductive organs and intestines (Riley, 1986); Sebekia nymphs occur freely in the body cavity among the viscera (Winch & Riley, 1986b); and Subtriquetra invades the swim-bladder of its fish host (Vargas V., 1975; Winch & Riley, 1986a). Raillietiella species in invertebrate hosts are located on the surface of the viscera or in the fat body, and require only two moults to become infective (Ali & Riley, 1983; Winch & Riley, 1985), but at least three moults are necessary when vertebrate intermediate hosts are involved (Fain, 1961, 1964; Ali et al., 1982b). Infective larvae carry single or double rows of uniform penetration spines, which immediately distinguish them from primary larvae (Fain, 1961, 1964; Ali & Riley, 1983; Winch & Riley, 1985). With few exceptions larvae are encysted in intermediate hosts within the last moulted cuticle inside a capsule of host origin, although primary larvae may migrate for some time before becoming quiescent around the time of the first moult (Esslinger, 1962b; Self et al., 1972). From the third-stage larvae to the adult form, pentastomes are transparent, having a cylindrical or flattened vermiform body. Two distinct body regions, the cephalothorax and the trunk, have been described. The latter exhibits bracelet-like, oblique rings (Abadi et al., 1996). This pseudoannulation is due to a metameric arrangement of the striated muscle and chitinous cuticle, which gives the pentastomid a screw-like appearance (Sambon, 1910).

CLASS EUPENTASTOMIDA

43

During ontogeny, larvae of some extant species lose the pair of terminal papillae after penetrating the gut of their hosts, and yet others, as in certain porocephalids, retain them for migrating through the body of their host (Castellani et al., 2011). The sensilla present on the caudal lobes of Reighardia sternae second-stage larvae may be important in orientation (Storch & Böckeler, 1982). Sexual features, such as the female vagina-uterus complex or the male ejaculatory duct, start to develop in the early phase of ontogeny, such as in Sebekia oxycephalum (cf. Leuckart, 1860; Stiles, 1891a; Winch & Riley, 1986a). At the time of the infective stages, copulation becomes possible, at least for females (Riley, 1983). Reighardia sternae represents the only known pentastomid that has shifted its larval phase from an intermediate host into the egg, hatching at a stage that is directly infective to the definitive host. Hence, this species is actually monoxenous. Other pentastomids are only facultatively monoxenous, but Reighardia sternae has passed its corresponding “intermediate host” larval time before infecting its host; therefore, its monoxeny is obligatory. Thus, the hatching larva of Reighardia sternae does not correspond to the firststage larva of the other pentastomids (and therefore should no longer be termed a firststage larva) but more likely represents a stage similar to the infective larva. Because of its monoxenous development in an endothermic host, Reighardia sternae could conquer even polar and subpolar regions (Thomas et al., 1999c), whereas Raillietiella cannot even colonize temperate regions due to its ectothermic hosts (Riley et al., 1988). The death of the intermediate host appears to be the cue for encystment. In the body cavity of snake hosts killed by drowning, Self & Kuntz (1967) observed that the infective nymphs of Kiricephalus pattoni emerged through rents in the scales, nares, etc. Riley & Self (1980) killed mice harbouring infective nymphs of Porocephalus crotali and found nymphs erupting through the epidermis 24-48 h later. In both cases nymphal behaviour was directed towards liberation into the stomach and thence to the body cavity of the snake, their definitive host; the lung was penetrated from this site within a few days (Esslinger, 1962b; Riley, 1981). Infective larval raillietiellids, pipetted into the stomachs of geckos, invaded the lungs (again via the body cavity) in as little as 4 h (Ali & Riley, 1983). Nymphal Linguatula serrata could be recovered from the nasopharynx of dogs in as little as 2-3 h after infection; these nymphs did not traverse tissues but migrated directly up the oesophagus from the stomach (Hobmaier & Hobmaier, 1940). In the conspicuously sexually dimorphic genus Leiperia, adult females are embedded in the bronchus of their crocodilian host, whereas developing stages are located in the bloodstream around the heart (Rodhain & Vuylsteke, 1932).

Life cycles Pentastomes are wormlike metameric animals uniquely adapted to an obligate endoparasitic lifestyle in the respiratory tract of terrestrial vertebrates (Paré, 2008) (figs. 45B.19-21). The Pentastomida constitute a highly aberrant group of parasites. All known species are parasitic in both adult and immature stages. Most of them are heteroxenous (with diverse hosts) and have a complicated life-cycle involving two successive hosts. In

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M. L. CHRISTOFFERSEN & J. E. DE ASSIS

Fig. 45B.19. Life cycle of Raillietiella sp. [Adapted from Fredes & Raffo, 2005.]

the most evolved genera, such as Armillifer and Linguatula, the definitive host is a carnivorous animal, either a large snake or other carnivore, and the intermediate host is a mammal (Fain, 1975). Host specificity is quite marked in most pentastomid species (Riley, 1986). By contrast, a few species, particularly some large raillietiellids, can each infect 12-14 species of snakes belonging to three of four families (Ali et al., 1982b, 1985), although there are grounds for believing that these cases may involve more than a single species of pentastomid (Ali et al., 1984b; Riley, 1986). Development to the adult occurs through a series of larval instars, each separated by a moult, but there is no true metamorphosis. An intermediate host is one in which the primary larva develops to the infective stage, whereas in the definitive hosts parasites must be capable of attaining sexual maturity. Ideally, only when all stages, from infective larva to egg-laying female, are found in a particular host species, can that species be considered a definitive host (Fain, 1964; Ali et al., 1982a). The larval forms are usually found free

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Fig. 45B.20. Life cycle of Porocephalus crotali. [Adapted from Mehlhorn & Waldorf, 1988.]

in the body cavity or encapsulated in or on the walls of the alimentary canal, the liver, spleen, mesentery, or abdominal muscles, of smaller animals on which the definitive host preys. In fact, they lie in a position not far removed from the alimentary tract from which they have presumably migrated (Shipley, 1898). While Pentastomida are a moderately homogeneous taxon as regards morphology, such uniformity is not reflected in their life-cycle strategies (Riley, 1993). The life cycles of pentastomids usually involve at least one intermediate host, although direct life cycles have been recorded (Banaja et al., 1975; Riley, 1986). Most cycles are thus classified as indirect, a few as direct. Many life cycles are diheteroxenous, that is, they have a primary and a secondary host. Intermediate hosts may be invertebrate (raillietiellids only) or vertebrate (most pentastomids), aquatic or terrestrial (Banaja et al., 1975; Olson & Cosgrove, 1982; Böckeler, 1984b; Haugerud, 1988; Riley, 1993). Indirect cycles include several intermediate hosts (insects, fish, amphibians, reptiles, and mammals) (Sambon, 1922; Hett, 1924; Heymons, 1935; Nicoli, 1963; Nicoli & Nicoli, 1966; Rego, 1984; Riley, 1986; Almeida & Christoffersen, 2002). Completion of the life cycle involves aquatic intermediate hosts for nymphs of some genera. For example, freshwater fish and turtles

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Fig. 45B.21. Life cycle of Armillifer agkistrodontis. A, Adult specimens reside mainly in the bronchi and lungs of final snake hosts; B, the development of larvae into adults in final snake hosts lasts about 10 months; C, larvae parasitize the liver, spleen, and mesenteric system of their intermediate hosts, e.g., rats and mice; D, mature eggs hatch in the small intestine and invade venules before reaching the liver, spleen, and mesenteric system over the portal system; the development from eggs into infective larvae lasts about four months; E, females release hundreds of thousands of eggs into the intestinal and respiratory systems of their snake final host; when eggs are excreted they can reach bodies of water and infect intermediate hosts; F, the consumption of the raw gallbladder and blood of a snake, as well as drinking contaminated water, are the main sources of human infection; G, the development from eggs into infectious larvae lasts about four months in humans; larvae can not develop into adults in humans, since humans are not permissive as intermediate hosts; H, larvae mainly parasitize the human liver, spleen, and mesenteric system. [Adapted from Chen et al., 2010.]

for some species of Leiperia, Sebekia and probably Diesingia; insects for species of Raillietiella; amphibians and reptiles for species of Kiricephalus; crocodilians and turtles for species of Leiperia; and snakes for species of Leiperia, Kiricephalus, Porocephalus, and Raillietiella (Olson & Cosgrove, 1982). In most indirect life cycles, eggs must gain access to the alimentary tract of a suitable intermediate host where appropriate stimuli can initiate hatching. Released primary larvae penetrate the stomach or intestinal wall, encyst in or on the viscera, and grow to an infective stage; a total of 6 and 10 moults occur during this ontogenesis, respectively, in the porocephalids Porocephalus crotali (cf. Esslinger, 1962a-c) and Linguatula serrata (cf. Leuckart, 1860), whereas only three moults are necessary in Raillietiella (cf. Bosch, 1986; Mehlhorn et al., 1988). Adult parasites that inhabit the respiratory tract of tetrapod definitive hosts release their eggs into the lungs and nasopharynx, and gain access to the oesophagus. Eggs, normally

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deposited in the faeces, are immediately infective and contain distinctive primary larvae that are specialized for tissue migration (Self, 1969). Once ingested by the intermediate host, the primary larva hatches and penetrates the gut wall with its small, double hooks, and a variety of penetration spines and stylets on the dorsal cephalothorax, which enable it to penetrate and traverse tissues, a process that may be entirely mechanical (Riley, 1986). The larva then migrates, sometimes extensively, across the trunk/coelom, to finally encyst, often in visceral tissue, where it undergoes several moults to become an infective nymph. Nymphs then excyst in the digestive tract and migrate to the lungs, where they mature into young adults. Males traverse throughout the lung tissue and fertilize females early during the infection. Fertilization occurs only once, because the gravid state anatomically precludes fertilization (Riley, 1986). The copulatory spicules of males are distinctive, and their morphology is one key criterion used for identification of raillietiellids to the species level. Because males usually do not live long, mature pentastome infections in definitive hosts may well be all female (Riley, 1986). With a few exceptions, patent females lay massive numbers of ova (up to several millions) consistently throughout their reproductive lives (Paré, 2008). Under natural conditions, the eggs remain viable for months and can withstand low temperatures, but not, apparently, desiccation (Keegan, 1943b). The life cycle thus involves oral, nasal, or faecal passage of embryonated eggs, which are usually ingested from the environment by intermediate hosts, in which several larval stages are passed with moulting and growth in cysts or migratory locations. Ingestion of the intermediate host by an appropriate predatory final or definitive host with the release of the wormlike nymph and its migration to the lung, usually complete the cycle (Olson & Cosgrove, 1982). The vast majority of species that use vertebrate intermediate hosts release comparatively large numbers of eggs into the environment. Females lay ova that are coughed up, sneezed out, or ingested and passed on with faeces (Paré, 2008). These are subsequently acquired as contaminants of food and water. Infection under these circumstances is purely fortuitous. In most cases, the larvae appear to encyst in or on the viscera of intermediate hosts but there are some exceptions: e.g., Kiricephalus larvae remain free in the body cavity of their second intermediate hosts, snakes, and Subtriquetra subtriquetra nymphs remain non-encapsulated in fish. The possible influence of such free larvae on host vulnerability (i.e., its liability to predation) is at present unknown. There are, however, many examples from helminths where parasites without intermediate hosts are able to alter host behaviour, thereby facilitating transmission (Riley, 1993). Reptiles represent important hosts for pentastomids (Self, 1969; Riley, 1986; Almeida & Christoffersen, 2002). Previously it was estimated that circa 90% of pentastomids have reptiles as their hosts (Baer, 1952). The present recounting of hosts/parasites gives significantly different numbers (see table I). Less than 50% of the hosts are reptiles, although more than one-third of the species found in reptiles are adults, while most of the pentastomids found in non-reptiles are juveniles. It must be kept in mind, however, that few pentastomid life cycles are actually known. According to Bosh (1987), the life cycles of only about 10% of the known pentastomid species have been established experimentally. The life cycles of a large number of other representatives (and indeed entire genera) remain

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M. L. CHRISTOFFERSEN & J. E. DE ASSIS

TABLE I Summary of host/parasite relationships (based on detailed data presented in Christoffersen & De Assis, 2013) Class

Species

Percentages

Insecta Pisces

4 89

2%

304

48%

19

3%

Mammalia

194

32%

Total

628

100%

Reptilia Aves

Remarks Only young stages of Raillietiella Only young stages, mostly Leiperia, also Sebekia and Subtriquetra Mostly young stages, only 2 species of Raillietiella as adults More than 1/3 as adults; sometimes both adults and young in same species Young and adult stages (autoinfection), mostly of Reighardia Mostly young stages

to be elucidated (Self, 1969). Most reptilian host associations have been registered in the Southern Hemisphere (Gondwana). Pentastomid parasitations of chelonians and crocodilians by Sebekiidae and Subtriquetridae appear to have preceded the snake infestation by porocephalids (Junker, 2002). The family Sebekiidae was created by Sambon (1922) to accommodate the crocodilian pentastomes Sebekia, Alofia, and Leiperia. The more recently described Agema, Pelonia, Selfia, as well as Sambonia, are also included in Sebekiidae (Junker, 2002). Sebekia is the genus with the widest host spectrum, including hosts from both crocodilian subfamilies, and the broadest geographical range, and has reached the highest species diversity within the Sebekiidae. It is assumed that representatives of the genus Sebekia and Leiperia evolved as early as 80 Myr ago, while Alofia, Selfia, and Diesingia seem to have emerged more recently from a common ancestor. The genus Agema, endemic to the African continent, presumably evolved after its host had diverged from the remaining crocodilian stock (Junker, 2002). The majority of the six genera comprising the family Sebekiidae occurs exclusively in crocodilians (Junker & Boomker, 2002). Dukes et al. (1971) speculated that a single species of the genus Sebekia may also reach maturity in piscivorous turtles. Until now, only the South American genus Diesingia has been known to be exclusive to a chelonian definitive host (Sambon, 1922; Heymons, 1941; Overstreet et al., 1985; Riley, 1994). It would appear that Diesingia megastomum is currently the only pentastome of which mature specimens have been recovered from chelonian hosts in Brazil (Diesing, 1836; Heymons, 1941; Fonseca & Ruiz, 1956; Self & Rego, 1985). Pelonia africana was found in two South African terrapins (Junker & Boomker, 2002). All sebekiids, as far as known, develop to an infective stage in fish intermediate hosts (Riley, 1986). Since Diesingia megastomum infects at least two species of piscivorous turtles (Fonseca & Ruiz, 1956), it is reasonable to speculate that fishes serve as intermediate

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hosts (Riley, 1986). Sebekia mississippiensis utilizes an alligator (Alligator mississippiensis) as a definitive host and several species of fish as intermediate hosts (Overstreet et al., 1985; Boyce et al., 1987). Adult pentastomes in the lungs of alligators deposit eggs containing larvae, which are passed on with the faeces. Following ingestion by an appropriate piscine host the larvae hatch and undergo several moults (Boyce et al., 1987). The case of fish as intermediate hosts of sebekiids was used as evidence for the conquest of terrestrial hosts from aquatic origins (Osche, 1959). Riley et al. (1978) have postulated that the pentastomid progenitor was originally a parasite of fish, which subsequently became adapted to an endoparasitic existence in aquatic reptiles through predation (Olson & Cosgrove, 1982). Currently, a second family of crocodile pentastomes is known, the Subtriquetridae. The monotypic genus Subtriquetra has three species (Junker et al., 1998a). Subtriquetra subtriquetra is the only pentastomid known to have a free-living stage in the life cycle. In this species, eggs hatch in the water and the first larvae are infective for fish (Vargas V., 1974, 1975). Two species of Raillietiella (Raillietiella frenatus and Raillietiella gehyrae) occur in insects as larvae, but specimens become adult almost exclusively in amniotes, and only very occasionally in amphibians (Raillietiella bufonis) (Stunkard & Gandal, 1968). Juveniles are common in amniotes, usually parasitizing a different host than the adult stage. Lavoipierre & Lavoipierre (1966) reported the presence of larval pentastomids in the haemocoel of cockroaches in Singapore. They summarized that these arthropods are the intermediate hosts for a species of Raillietiella that infects the common house-gecko in this area (Fain, 1975). Larvae are also common in fish and amphibians, which usually function as intermediate hosts (Heymons, 1935; Riley, 1986). Only two species of amphibians (Bufo lemur and Bufo melanostictus) have been indicated to be final specific hosts for Raillietiella indica, Raillietiella bufonis, and Raillietiella rileyi (cf. Gedoelst, 1921; Ali et al., 1982a; Krishnasamy et al., 1995). Fish and insects function as intermediate hosts only (see table I). Kiricephalus uses snakes as definitive hosts, and two vertebrate intermediate hosts are essential in the life cycles of the two best known species, Kiricephalus pattoni from SouthEast Asia, including the Philippines, and Kiricephalus coarctatus, from the Americas. Both of these infect an impressive number of snakes, lizards, and amphibians as intermediate hosts (Riley, 1986). Eggs are known to be infective for amphibians (Salazar, 1965; Keegan et al., 1969; Guidry & Dronen, 1980; Riley & Self, 1980) and lizards (Yamamoto et al., 1978), but snakes, including snake intermediate hosts, are resistant to infection with eggs (Keegan, 1943a). Nymphs recovered from amphibians and snakes assort into distinct, non-overlapping size categories, indicating that these vertebrates are first and second intermediate hosts, respectively (Riley & Self, 1980). Those in amphibians are encysted (Riley & Self, 1980), and those in snake intermediate hosts are generally occurring freely in the body cavity (Self & Kuntz, 1967), whereas adults and preadults occur exclusively in the lungs of the ophiophagous definitive host (Riley, 1986).

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Krishnasamy & Self (1981) found a nymphal Kiricephalus tortus in the orbit of a cat shark (“Meniscyllium indicum”), which was assumed to have eaten the snake definitive host (Boiga irregularis). This hypothesis was supported by the presence of other snake pentastomids (Raillietiella sp.) in the shark’s gut (Riley, 1986). Several species have now been found in birds: Reighardia sternae in gulls and terns and Reighardia lomviae in guillemots; both live in the host’s airsacs and have a direct life cycle (Riley, 1972b; Banaja et al., 1975; Dyck, 1975; Hoberg, 1987). Raillietiella trachea is the first record of a pentastomid from a fully terrestrial bird (Riley et al., 2003). Another species, Hispania vulturis, was described from the the non-coastal black vulture (Martínez et al., 2004). There are also two reports of Cubirea from birds. Adults of Cubirea annulata were reported from a crane (Anthropoides virgo), probably as a consequence of the bird having eaten an infective snake (Riley, 1986). Another author reported the species from a water hen, Porphyrio sp. (Heymons, 1940). The conquest of homeotherms occurred in the Northern Hemisphere (Laurasia), first in Aves, by Reighardiidae, and then in Mammalia, independently, by Linguatulidae. Only a few species may have a direct life cycle in a single host (Riley, 1983; Abele et al., 1989). In taxa such as in Reighardia and Raillietiella gehyrae, autoinfection is known or believed to occur. Direct cycles without intermediate hosts have been well corroborated for Reighardia sternae, whose eggs contaminate the regurgitated food used to feed the brood of herring gulls (Banaja et al., 1975, 1976; Riley et al., 2003). Reighardia has two species that infect marine birds, viz., guillemots and puffins (Alcidae: respectively, genera Uria and Fratercula) (Threlfall, 1971; Riley, 1972b; Dyck, 1975; Böckeler, 1984b). Reighardia sternae lives exclusively in the lungs of Laridae (Von Haffner & Rack, 1965; Banaja et al., 1975; Böckeler, 1984b). Primary larvae occur in the stomach and intestine of young sea-gulls (Larus argentatus) and produce secondary larvae by moulting. These are not provided with a rostrum or piercing hooks. Only later larvae regain these hooks, can subsequently penetrate the circulatory system, and reach the thoracic aerial sacs of the host, where the adult Reighardia sternae are found (Von Haffner & Rack, 1965). Eggs containing the primary larvae are literally spit-out by a contaminated female, and end up reaching a new definitive host via the alimentary tract as contaminants of food and water. After hatching inside the intestine, the larvae penetrate its wall. In the body cavity they mate paedomorphically (at a length of 10 mm) and the males die. Females moult several times while migrating via different air sacs to the clavicular air sac. There egg production and embryogenesis take place (Böckeler, 1984b). From here the females migrate through lung and tracheae into the throat, from which they will be disgorged (Castellani et al., 2011). As a rule, adult Linguatulidae are found in the nasal cavities and spaces communicating with them as well as in the lungs of the Carnivora, snakes, crocodiles, and flesh-eating animals in general (Shipley, 1898). Linguatula has also been discovered in ruminants, i.e., the caribou (Chapin, 1926; Murie, 1935) and the reindeer (Voblikova, 1961; Skjenneberg, 1965; Skjenneberg & Slagsvold, 1968; Christensson et al., 1974; Rehbinder & Nordkvist, 1982). Specimens from reindeer were previously misidentified as Linguatula serrata (cf. Riley, 1986), but are now known as Linguatula arctica (cf. Riley, 1993). Linguatula arctica

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thus represents another species with supposedly direct development, whose host is a herbivore (Riley et al., 1987). Tranmission must be either direct or involves an unknown herbage-dwelling invertebrate intermediate host, which could be accidentally ingested when reindeer feed (Riley, 1986). Direct development has also been observed for Sambonia clavata. This species lives in the respiratory tract of the Komodo dragon (or Komodo monitor), Varanus komodoensis (cf. Fain & Mortelmans, 1960). All intermediate forms between the embryo and the adults, including five successive larval stages, were found in the pulmonary tissues of that giant lizard (Fain, 1975). The above examples thus exhibit an alternative mode of life, also called a monoxenous life cycle. They all develop from the primary larva to the adult within the same host (Castellani et al., 2011). Clearly, in the case of direct life cycles, eggs are infective to definitive hosts and it is now known that some of these are sustained by autoinfection (Deakins, 1973; Banaja et al., 1976; Böckeler, 1984b; Riley, 1993).

PENTASTOMID INFESTATIONS OF ANIMAL GROUPS, PATHOLOGY, AND DISEASES Pentastomiasis (a clinical perspective) Pentastomiasis is an unusual parasitic zoonosis caused by members of the phylum Pentastomida (Abadi et al., 1996). Eggs hatch upon reaching the digestive tracts of various intermediate hosts. The young larvae are liberated by digestive juice action, penetrate the intestinal wall, and come to lie under the peritoneum where they undergo several moults to become nymphs. For the life cycle to be completed, it is necessary for the snake or other definitive host to eat the animal containing the encysted nymphs. The nymphs are released into the intestine of the definitive host; from here, by penetrating through the mucosa, they enter the mesenteric venules and migrate to the lungs, where they become adults (Mapp et al., 1976). We propose to classify the cases of pentastomiasis into two types: T YPE 1 — V ISCERAL PENTASTOMIASIS ( CAUSED BY LARVAE ) Larvae or nymphs produce granulations in viscera of intermediate hosts. In intermediate hosts such as rodents and amphibians, experimental nymphal pentastomid infection of Porocephalus crotali has been proven to cause mechanical tissue damage and haemorrhage following migration (Boyce & Kazacos, 1991). Visceral pentastomiasis is a common disease in many tetrapods, mainly reptiles, but can also affect man. T YPE 2 — R ESPIRATORY PENTASTOMIASIS ( CAUSED BY ADULTS ) Adults live in the respiratory tracts of the definitive host. For example, Linguatula serrata is a cosmopolitan parasite whose intermediate hosts are cattle, goats, sheep,

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and other ruminants. The adult form is found in the nasal airways, frontal sinuses, and tympanic cavity mostly of canines and felines, and it produces haemorrhages and breathing difficulties (Bowman, 1995; Alcala-Canto et al., 2007). This is the only species known to infect the respiratory tracts of man as adults.

Pentastomes and pentastomiasis in man The most common infective stages of the pentastomids in man include the primary and third-stage larva. Humans become infected by ingestion of eggs contained in respiratory secretions, blood, saliva, or faeces of the definitive hosts. The primary larvae penetrate the gastrointestinal tract of the intermediate host, migrating and encysting in various host tissues. The third-stage larvae can also encyst and migrate. Exclusive involvement of the heart has also been reported previously. The severity of human visceral pentastomiasis may vary, although this stage is usually asymptomatic. Humans are usually highly tolerant to pentastomid infections (Abadi et al., 1996). Pentastomids in humans may assail the respiratory tracts, liver, pancreas, intestine, and lymphatic vessels, mainly in the form of encysted nymphs (Self et al., 1975; Riley, 1986). Although most visceral infections produce few or no symptoms, severe infestation has caused intestinal obstruction, pneumoanitis, meningitis, pericarditis, nephritis, peritonitis, obstructive jaundice, and even death (Mapp et al., 1976). Pentastomiasis is usually an incidental finding in an autopsy, a radiological examination, or during a surgical intervention (Abadi et al., 1996). Thus only some parasites pose a risk to man, who can act as intermediate host (Adeoye & Ogunbanwo, 2007). Man is only rarely infected by adult pentastomids. Some severe medical cases involve Linguatula serrata. This is the only species that infects man as adults, causing respiratory pentastomiasis. Linguatula serrata is a cosmopolitan parasite, whose intermediate hosts are humans and other mammals, but more often involve herbivores such as cattle, goats, sheep, and other ruminants that have ingested the parasite’s eggs contained in their feed of contaminated plants (Alcala-Canto et al., 2007). Nymphal parasitism, on the contrary, is not rare in man (Fain, 1975). In Africa, the larva most commonly parasitic in man is that of Armillifer armillatus (the adult form of which is parasitic in the lungs of pythons and big vipers) and the cysts are usually located in the abdominal viscera, particularly the liver and omentum, but sometimes in the lung and other organs (Alcock, 1923). Another eleven species (nine identified to species level) have been recorded as producing visceral pentastomiasis in man by action of their larval stages (Baird et al., 1988; Mairena et al., 1989; Junker, 2002). Armillifer moniliformis, occurring as adults in African and Asian pythons, has been reported in man by Herzog & Hare (1907), Waldow (1908, 1910), Sambon (1909), Faust (1927), Fain (1975), C. P. Qiu et al. (2004), Tappe & Büttner (2009), and Latif et al. (2011). Armillifer grandis is another parasite of the lungs of African pythons and vipers, having been reported as nymphs in the lungs of man by Fain (1961, 1975), Fain & Salvo (1966), Ette et al. (2003), M. H. Qiu & Jiang (2007), and Tappe & Büttner (2009), and includes a case of lethal pentastomiasis (Cagnard et al., 1979). A disease report case of visceral

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pentastomiasis in China and Taiwan was reported for Armillifer agkistrodontis (cf. Q. Y. Zhang et al., 1996), the life cycle of which includes snakes as adult hosts and mice, rats, and primates as intermediate hosts (Chen et al., 2010; Mätz-Rensing et al., 2012). Raillietiella affinis occurs in Africa, and the aetiology of human porocephalosis by first larvae was discussed by Awachie (1974). Ingestion of live lizards for therapeutic reasons by humans in southeast Asia was linked to subsequent subcutaneous pentastomid infection called “creeping disease” and was tentatively attributed to Raillietiella hemidactyli (cf. Dollfus & Canet, 1954; Drabick, 1987). Man can be infected with Raillietiella sp., by having their hands contaminated from the faeces or saliva of the reptile, and then accidentally ingesting the eggs (Nash, 2005). This pentastome may cause localized inflammation and intestinal infection in humans. Handling faecal contaminated water, dishes, and other equipment may also result in accidental transmission. Usually, there are no clinical signs; however, some people may develop localized inflammation. The larvae can encyst in various tissues, causing abdominal pain, vomiting, constipation, diarrhoea, and a tender trunk (Adeoye & Ogunbanwo, 2007). In isolated cases, septicaemia may occur (Nash, 2005). Porocephalus subuliferum, which as an adult is a parasite of certain African snakes, has been reported in man by Sambon (1922). Porocephalus taiwana, described from Taiwan on the basis of the morphology of the nymphs, causes ‘porocephalosis taiwana’ in humans. Excystation of the nymphs was hypothesized to explain their presence in the faeces, although there were no adult specimens to examine (M. H. Qiu et al., 2005). Porocephalus crotali, a parasite of rattlesnakes in America, has been doubtfully attributed as causing visceral pentastomiasis in man (Sambon, 1922). Leiperia cincinnalis lives as an adult in the lungs of African crocodiles. The nymphs have been found in the connective tissue enveloping the intestine, or in the muscles of various fishes. A nymph of this species was found in the faeces of a European woman in Zaire (Fain, 1960, 1961). This patient had probably become infected by eating fish harbouring this larva. This case of parasitism was considered, therefore, to be purely accidental (Fain, 1975). The last species reported for humans is Sebekia sp. A nymph of this species was recovered from a dermatitic laesion in a Costa Rican woman (Mairena et al., 1989).

ECOLOGY Pentastomids, in common with other parasites, are regulators of host populations. Pentastomids are often recovered from zoo autopsies, so that from a conservation point of view, it should be important to determine how pentastomids affect and regulate rare and endangered host species (Riley, 1986). To employ hosts as vehicles for pentastomids in long-term ecological studies is a particularly esoteric branch of parasitological research, with relatively few adherents, in particular when one considers that most zoologists, and many parasitologists, have never seen a pentastomid (Riley, 1986). This dim perspective may explain why amniote

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palaeobiologists have apparently never specifically searched for, and thus not yet actually found, fossil pentastomids. Of course, their soft bodies and progressive evolution away from aquatic hosts make the prospects of actually finding such fossils rather fortuitous. The effects of parasites in auks was reviewed by Muzaffar & Jones (2004). Even though two species of pentastomids are involved in the biology of auks, and episodes of mass mortality of seabirds are periodically recorded, few of those episodes have been exclusively linked to parasitic infestations. Brown et al. (1995) demonstrated experimentally for Pacific geckos that unisexual lizards arise through hybridization of two sexual species and should be highly resistant to parasitism, because they are maximally heterozygous, resulting in hybrid vigour. Marcogliese (2004) cited that natural illnesses caused by parasites may impose energetic demands, alter behaviours, affect morphology and appearance of the hosts, cause their deaths, and even their complete extinctions. However, despite the significant parasitic loads encountered in many reptiles, including several pentastomid species in tropical northeastern Brazil (Lopes & Almeida, 2006), data on how they may affect the population structure of their hosts, their trophic interactions, and their biodiversity, are still largely undocumented. Pentastomids may also represent a health problem for man in certain regions of the world, particularly Africa, the Middle East, South-East Asia (Riley, 1986), and Latin America, particularly in poverty-stricken communities living in arid regions (Almeida & Christoffersen, 2002).

PHYSIOLOGY, BIOCHEMISTRY, AND IMMUNOLOGY Since pentastomids lack an excretory system, it may be surmised that nitrogen diffuses across the cuticle to be eliminated by the host (Riley, 1986). Osche (1963) signaled a cutaneous type of excretion in old adult females of Reighardia sternae: true excretory concretions are found below the cuticle and at the level of the hypodermic conjunctive tissue. Remarkably, these concretions are not found in young adult females (Doucet, 1965; Legendre, 1967). Intestinal spherocrystals are regarded as a kind of storage excretion such as present in many other arthropods (Thomas & Böckeler, 1994). Also, since there is no circulatory system; the peristalsis of the body wall simply agitates coelomic fluid, so the body fluid may be important in the transport of respiratory gases. Some species (for example, of Waddycephalus, Elenia, and Subtriquetra) are bright red in life because of haemoglobin in the haemocoel, and it is likely that dietary haemoglobin is broken down and resynthesized before being secreted into the haemocoel, a process known from nematodes (Riley, 1973c). Haemocyanin can occur in the haemocoel of large Raillietiella’s (Riley, 1986). The deep, occluded pores in larval Linguatula serrata may regulate the hydromineral balance of the pentastomid’s haemolymph (Banaja, 1983). Banaja et al. (1977) present evidence to suggest that pentastomids osmoregulate hypoosmotically. They maintain a blood concentration that is lower than that of their hosts and,

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because they feed on host blood and lymph, which are relatively rich in electrolytes, it was postulated that the tegumental chloride cells secrete excess ions to maintain the water balance (Riley, 1986). The demonstration of intense phosphatase activity in the apices of these cells underscores their role in active transport (Riley, 1973a; Nadakal & Mohandas, 1975; Banaja et al., 1977; Hollis, 1979a). Pentastomids, in common with many endoparasitic helminths, must adapt to several quite dissimilar environments for the successful completion of their life cycle. Typically, eggs must withstand environmental fluctuations, the primary larva must survive the gut conditions of an intermediate host, migrate, and subsequently evade the host’s defensive strategies, and infective stages must survive excystment in the gut of the definitive hosts, adapt to an essentially aerobic environment in the respiratory tract of a vertebrate, and overcome yet another immune response of a host (Riley, 1986). Porocephalus crotali possesses the genetic capacity to respond differently to different environments: large differences in the specific activity and isoenzyme composition of lactate dehydrogenase were found in eggs, infective nymphs, and adults (Rodrick, 1974, 1976). Glycogen, the principal storage product of pentastomids (Doucet, 1965) is sequestered mainly within striated muscles and the gastrodermis. The moderate cytochrome oxidase activity in epidermal glands and intestinal cells of Kiricephalus pattoni suggests that this species is capable of some form of oxidative metabolism (Nadakal & Mohandas, 1975). All pentastomids are equipped with elaborate glands that discharge a lamellate secretion onto the cuticle (Riley et al., 1979). The postulated function of this membranous surfactant is to protect the parasite’s surface from the the host’s immune response (Riley, 1986). The formation of granulomata in host tissues represents the best evidence for cell-mediated immunity in helminth-infected animals (Olgive & Jones, 1973). Adults of Porocephalus crotali mature in the lungs of rattlesnakes, whereas larval stages are found in the tissues of rodent intermediate hosts. Previous studies (Riley & Henderson, 1999; Buckle et al., 2002) suggest that the survival of Porocephalus crotali, in both hosts, is higly dependent on the continuous secretory activity of frontal glands that flank the intestine, and subparietal cells that are suspended beneath the cuticle. Both glands have ducts directing secretions onto the cuticle (Buckle et al., 2002). Moulting nymphs become the focus of intense granulomatous responses that are directed primarily at the underside of ecdysed cuticles (Riley & Henderson, 1999; Buckle et al., 2002). Electron microscopy reveals that the cuticle of each instar is protected by predominantly membranous secretion. Pre-adult and adult worms within the snake’s lung deploy a similar protective mechanism (Riley & Henderson, 1999; Buckle et al., 2002). However, histological and microscopic studies reveal that every individual secretory lobule within the frontal glands contains cells that secrete either membranes, or proteins, and the same is true for the subparietal cell system (Doucet, 1965; Riley, 1973a; Ambrose & Riley, 1988a, b). Thus, the available evidence suggests that both classes of molecules may be involved in immunomodulation (Riley, 1992b; Buckle et al., 2002). It could be that proteins enable post-ecdysial expansion and immune evasion. The proteinases degrade haemoglobin and fibrinogen as well as structural proteins such as collagen and fibronectin, suggesting roles in bloodmeal digestion and tissue penetration. Immunoglobulin digestion

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was not demonstrated. Porocephalus crotali releases a complex mixture of proteins, some of which appear to be stage-specific, and a number of these proteins show proteolytic activity with an optimum at alkaline pH values. Evidence from degradation studies indicates that these metallo-proteinases may have histolytic and anti-coagulant functions in vivo, suggesting a role in tissue migration and disruption, as well as in the acquisition of nutrients by extracorporeal digestion (Buckle et al., 2002). The immune competence of the host profoundly influences the parasite’s growth (Riley, 1986). This may explain why Reighardia sternae does not infect adult gulls (Riley, 1972a; Banaja et al., 1975). The combination of surface-active secretion, coupled with a physical surface barrier during periods of peak inflammation, enables pentastomids to survive the host’s immune response fully intact (Riley, 1986). While lipids that functioned as storage products were found in the intestine of Reighardia, glycogen accumulation was observed in Raillietiella and Cephalobaena (Thomas & Böckeler, 1992a, b). The so-called ‘salivary’ glands are also present in the digestive tract, but these are associated with the pores above the internal hooks, probably having an anti-coagulant function, rather than being connected to the digestive system. Completing known endocrine functions, there are epidermal glands that may be responsible for the secretion of a layer of mucopolysaccharides at each ecdysis (Riley, 1986, 1988, 1992; Storch, 1993).

BIOGEOGRAPHY Pentastomids predominate in the tropics and subtropics (Self, 1969; Rego, 1984; Almeida & Christoffersen, 2002), but also occur in temperate regions and can be found in relatively cold countries such as Norway, where Linguatula arctica parasitizes the reindeer Rangifer tarandus (cf. Riley et al., 1987). Despite being considered to be rare by some authors (Shipley, 1909), Eupentastomida are conspicuous parasites of reptiles and mammals. Pentastomids are all around us, really everywhere (Almeida & Christoffersen, 2002). Eupentastomida predominate today in the tropics and subtropics of Gondwana (Self, 1969; Rego, 1984). Taxa of Gondwanan distribution are Cephalobaenidae, Raillietiellidae, and Porocephalidae. Raillietiella, for example, cannot even colonize temperate regions, due to its ectothermic hosts (Riley et al., 1988). This could indicate that Gondwana represents a possible origin of the recent species of Pentastomida, with subsequent dispersals to North America by Reighardiidae and Linguatulidae (Rego, 1984). Reighardia sternae has conquered polar and subpolar regions in the Holarctic region (Nicoli & Nicoli, 1966), because of its monoxenous development in endothermic bird hosts, while Linguatula serrata, with a life cycle mostly restricted to mammals, has become cosmopolitan. On the other hand, the Holarctic location of the Cambrian fossils may indicate a Pangaeic origin for the group. Pangaea began to split during the Jurassic period (180130 Myr ago) into northern Laurasia and southern Gondwana. South America is estimated

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to have separated from Antarctica about 60 Myr ago, and Australia split from Antarctica about 50 Myr ago (Junker, 2002). Within the clade Sebekiidae, the high diversity and wide host spectrum of Sebekia suggests that this genus had already emerged in crocodilians before their split into two families 80 Myr ago and possibly before the South American and African crocodiles started diverging 100 Myr ago. Leiperia also has an equally early origin, despite its, apparently, only slight subsequent morphological development. Alofia is restricted to South American and African crocodilians, suggesting that it emerged more recently. Selfia and Agema are exclusive of Australia and Africa, respectively, indicating their more recent ages (Junker, 2002).

SYSTEMATICS: CURRENT CLASSIFICATION (for diagnoses of taxa, refer to Christoffersen & De Assis, 2013) Phylum PENTASTOMIDA Huxley, 1869 (8 fossil species, 141 Recent species and subspecies) Pan-Pentastomida [stem-group fossil pentastomids + crown-group Recent pentastomids] Stem-group pentastomids (4 Palaeozoic fossil genera, 8 fossil species) Class E UPENTASTOMIDA Waloszek, Repetski & Maas, 2006 [crown-group Recent pentastomids] (141 spp.-sspp.) Order Cephalobaenida Heymons, 1935 (2 spp.) Family Cephalobaenidae Heymons, 1922 (2 gen., 2 spp.) Order Raillietiellida Almeida & Christoffersen, 1999 (44 spp.-sspp.) Family Raillietiellidae Sambon, 1922 (2 gen., 44 spp.-sspp.) Order Reighardiida Almeida & Christoffersen, 1999 (3 spp.) Family Reighardiidae Heymons & Vitzhum, 1936 (2 gen., 3 spp.) Order Porocephalida Heymons, 1935 (92 spp.-sspp.) Superfamily Linguatuloidea Haldeman, 1851 (10 spp.-sspp.) Family Linguatulidae Leuckart, 1860a (2 gen., 6 spp.-sspp.) Family Subtriquetridae Fain, 1961 (1 gen., 4 spp.) Superfamily Porocephaloidea Sambon, 1922 (82 spp.-sspp.) Family Sebekiidae Sambon, 1922 (38 spp.) Subfamily Leiperiinae Christoffersen & De Assis (2013) (1 gen., 3 spp.) Subfamily Samboninae Heymons, 1935 (1 gen., 5 spp.) Subfamily Diesingiinae Heymons, 1935 (3 gen., 13 spp.) Subfamily Sebekiinae Sambon, 1922 (3 gen., 17 spp.) Family Porocephalidae Sambon, 1922 (44 spp.-sspp.) Subfamily Armilliferinae Kishida, 1928 (2 gen., 13 spp.-sspp.) Subfamily Porocephalinae Sambon, 1922 (6 gen., 31 spp.)

CONCLUSIONS We need further evidence from their life cycles, phylogeny, biogeography, palaeontology, and parasitology, if we are ever to resolve the enigma represented by Pentastomida. Molecular biology and total evidence cladistics have not provided the holy grail towards solving the phylogenetic relationships of the Pentastomida. When molecules and morphology clash, are we to consider secondary loss of morphological characters (Jenner,

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2004), secondary change of molecular characters, or plesiomorphy of either morphology or molecules? There is no ultimate Pandora’s box for automatically solving metazoan phylogeny. Both sperm and molecular data do not guarantee final historical truths. Both molecular phylogeny and total evidence cladistics unfortunately also group by overall similarity, which may or may not reflect true synapomorphy. Computer methods are not being successful in consistently distinguishing, a posteriori, apomorphies from plesiomorphies and convergencies, simply because plesiomorphies at any level of analysis are almost ubiquitous relative to apomorphies (Nunes & Christoffersen, 2009). Pentastomids are not arthropods, nor do they share convincing synapomorphies with any of the arthropod subgroups with which they have been historically correlated (arachnids: mites; crustaceans: branchiurans; myriapods). However, they are unquestionably ecdysozoans, passing through a series of moults until they reach the adult stage. Several enigmas remain unsolved to date: (1) Why was only Linguatula serrata successful in, as an adult, parasitizing human lungs? (2) Are the known fossils of Pentastomida juvenile forms, or do they reflect something akin to an ancestral adult state? (3) What were the Palaeozoic hosts of Pentastomida, or did these animals have some other life style, without the complex digenetic cycles as in current pentastomes? (4) Are the original Pentastomida Pangaeic in distribution? (5) Did the radiation of recent pentastomids coevolve with the tetrapods in the conquest of land? In order to satisfactorily solve these questions, more scientists, i.e., especially biologists, veterinarians, and physicians, should be able to effectively recognize, observe, and report (infections of) Pentastomida. For that purpose, they should first of all upgrade their knowledge of the group to a workable level. This goes in particular for carcinologists, who work on a taxon with which pentastomids have been associated quite prominently during the past decades.

ACKNOWLEDGEMENTS This paper was supported with a productivity grant to M.L.C. and a Ph.D. and further post-doctoral scholarships to J.E.A. A PPENDIX Checklist of species of Recent Pentastomida cited in this review Alofia platycephalum (Lohrmann, 1889) Armillifer agkistrodontis Self & Kuntz, 1966 Armillifer armillatus (Wyman, 1845) Armillifer grandis (Hett, 1915) Armillifer mazzai (Sambon, 1922) Armillifer moniliformis (Diesing, 1836) Cephalobaena tetrapoda Heymons, 1922 Cubirea annulata (W. Baird, 1853) Diesingia kachugensis (Shipley, 1910) Diesingia megastomum (Diesing, 1836)

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Elenia australis Heymons, 1932 Hispania vulturis J. Martínez, Criado-Fornelio, Lanzarot, Fernández-García, Rodrigues-Caabeiro & Merino, 2004 Kiricephalus coarctatus (Diesing, 1850) Kiricephalus pattoni (Stephens, 1908) Kiricephalus tortus (Shipley, 1898) Leiperia cincinnalis (Sambon [in Vaney & Sambon], 1910) Linguatula arctica Riley, Haugerud & Nilssen, 1987 Linguatula multiannulata Von Haffner, Sachs & Rack, 1967 Linguatula serrata Frölich, 1789 Neolinguatula nuttalli (Sambon, 1922) Pelonia africana Junker & Boomker, 2002 Porocephalus clavatus (Wyman, 1845) Porocephalus crotali (Von Humboldt, 1808) Porocephalus subuliferum (Leuckart, 1860) Porocephalus taiwana M. H. Qiu, Ma Fan & Lu, 2005 Raillietiella affinis Bovien, 1927 Raillietiella amphiboluri Mahon, 1954 Raillietiella boulengeri (Vaney & Sambon, 1910) Raillietiella bufonis Ali, Riley & Self, 1982 Raillietiella chamaeleonis Gretillat & Brygoo, 1959 Raillietiella furcocercum (Diesing, 1836) Raillietiella gehyrae Bovien, 1927 Raillietiella gigliolii Hett, 1924 Raillietiella gowrii Rajalu & Rajendran, 1970 Raillietiella hebitihamata Self & Kuntz, 1960 Raillietiella hemidactyli Hett, 1934 Raillietiella indica Gedoelst, 1921 Raillietiella mabuiae Heymons, 1922 Raillietiella maculatus Rao & Hiregandar, 1959 Raillietiella mottae Almeida, Freire & Lopes, 2008 Raillietiella orientalis (Hett, 1915) Raillietiella rileyi Krishnasamy, Jeffery, Inder, Singh & Oothuman, 1995 Raillietiella trachea Riley, Oaks & Gilbert, 2003 Raillietiella venteli (Motta, 1965) Reighardia lomviae Dyck, 1975 Reighardia sternae Diesing, 1864 Sambonia clavata (Lohrmann, 1889) Sebekia minor Giglioli [in Sambon], 1922 Sebekia mississippiensis Overstreet, Self & Vilet, 1985 Sebekia oxycephalum (Diesing, 1836) Subtriquetra rileyi Junker, Boomker & Booyse, 1998 Subtriquetra subtriquetra (Diesing, 1836) Waddycephalus komodoensis Riley & Self, 1981 Waddycephalus longicauda Riley & Self, 1981 Waddycephalus punctulatus Riley & Self, 1981 Waddycephalus superbus Riley & Self, 1981

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Authorities and dates of non-pentastomid species names C RUSTACEA Argulus americanus Wilson, 1902 (Branchiura) Hutchinsoniella macracantha Sanders, 1955 (Cephalocarida) Pollicipes polymerus Sowerby, 1833 (Cirripedia: Thoracica) Speleonectes tulumensis Yager, 1987 (Remipedia) [currently as: Xibalbanus tulumensis] N ON -C RUSTACEA Alligator mississippiensis (Daudin, 1802) (Reptilia: Crocodilia: Alligatoridae) Anthropoides virgo (L., 1758) (Aves: Gruidae) Boiga irregularis (Merrem, 1802) (Reptilia: Squamata: Serpentes: Colubridae) Bufo lemur (Cope, 1869) (Amphibia: Anura: Bufonidae) [currently as: Peltophryne lemur] Bufo melanostictus Schneider, 1799 (Amphibia: Anura: Bufonidae) [currently as: Duttaphrynus melanostictus] [N.B.: Both the names melanosticus auct. and melanosticum auct. involve misspellings of the species name.] Coelosis biloba (L., 1767) (Hexapoda: Coleoptera: Scarabaeidae) Larus argentatus Pontoppidan, 1763 (Aves: Laridae) Meniscyllium indicum (Gmelin, 1789) (Pisces: Chondrichthyes: Hemiscyliidae) [currently as: Chiloscyllium indicum] [N.B.: The name Meniscillum auct. involves at least a misspelling of an unretrievable generic name; yet, it may well be that also Meniscyllium involves a misspelling, perhaps of the registered name Hemiscyllium.] Rangifer tarandus (L., 1758) (Mammalia: Artiodactyla: Cervidae) Varanus komodoensis Ouwens, 1912 (Reptilia: Squamata: Lacertilia: Varanidae)

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— —, 1994. A revision of the genus Alofia Giglioli, 1992 and a description of a new monotypic genus, Selfia: two genera of pentastomid parasites (Porocephalida: Sebekidae) inhabiting the bronchioles of the marine crocodile Crocodylus porosus and other crocodilians. — Syst. Parasit., 29: 23-41. R ILEY, J. & A. A. BANAJA, 1975. Some ultrastructural observations on the integument of a pentastomid. — Tiss. Cell, 7: 33-50. R ILEY, J., A. A. BANAJA & J. L. JAMES, 1978. The phylogenetic relationships of the Pentastomida: the case for their inclusion within the Crustacea. — Int. J. Parasit., 8: 245-254. R ILEY, J., R. E. H AUGERUD & A. C. N ILSSEN, 1987. A new species of pentastomid from the nasal passages of the reindeer (Rangifer tarandus) in northern Norway, with speculation about its life-cycle. — J. Nat. Hist., Lond., 21: 707-716. R ILEY, J. & R. J. H ENDERSON, 1999. Pentastomids and the tetrapod lung. — Parasitology, (Suppl.) 119: 89-105. R ILEY, J. & F. W. H UCHZERMEYER, 1995. Pentastomid parasites of the family Sebekidae Fain, 1961 in West Africa[n] dwarf crocodiles Osteolaemus tetraspis Cope, 1851 from the Congo, with a description of Alofia parva n. sp. — Onderst. J. Vet. Res., 62: 151-162. — — & — —, 1996. A reassessment of the pentastomid genus Leiperia Sambon, 1922, with a description of a new species from both the IndoPacific crocodile Crocodylus porosus and Johston’s crocodile C. johnstoni in Australia. — Syst. Parasit., 34: 53-66. R ILEY, J., J. L. JAMES & A. A. BANAJA, 1979. The possible role of the frontal and sub-parietal gland systems of the pentastomid Reighardia sternae (Diesing, 1864) in the evasion of the host immune response. — Parasitology, 78: 53-66. R ILEY, J., C. T. M C A LLISTER & P. S. F REED , 1988. Raillietiella teagueselfi n. sp. (Pentastomida: Cephalobaenida) from the Mediterranean gecko, Hemidactylus turcicus (Sauria: Gekkonidae), in Texas. — J. Parasit., 74: 481-486. R ILEY, J., J. L. OAKS & M. G ILBERT, 2003. Raillietiella trachea n. sp., a pentastomid from the trachea of an oriental white-backed vulture Gyps bengalensis taken in Pakistan, with speculation about its life-cycle. — Syst. Parasit., 56: 155-161. R ILEY, J. & J. T. S ELF, 1979. On the systematics of the pentastomid genus Porocephalus (Humboldt, 1811), with descriptions of new species. — Syst. Parasit., 1: 25-42. — — & — —, 1980. On the systematics and life cycle of the pentastomid genus Kiricephalus (Sambon, 1922), with descriptions of three new species. — Syst. Parasit., 1: 127-140. — — & — —, 1981a. Some observations on the taxonomy and systematics of the pentastomid genus Armillifer (Sambon, 1922) in south east Asian and Australian snakes. — Syst. Parasit., 2: 171-179. R ILEY, J., D. M. S PRATT & P. J. A. P RESIDENTE, 1985. Pentastomids (Arthropoda) parasitic in Australian reptiles and mammals. — Austr. J. Zool., 33: 39-53. R ILEY, J. & L. S. WALTERS , 1980. Porocephalus dominicana n. sp. from the Dominican boa (Constrictor constrictor nebulosus). — Syst. Parasit., 1: 123-126. RODHAIN , J. & C. V UYLSTEKE, 1932. Contribution à l’étude des porocéphales des crocodiles africains. — Rév. Zool. Bot. Afr., 23: 1-11. RODRICK , G. E., 1974. The ontogenetic study of lactate dehydrogenase in Porocephalus crotali (Pentastomida). — Proc. 3rd Int. Congr. Parasit., Munich, 2: 1022. — —, 1976. An ontogenetic study of lactate-dehydrogenase in Porocephalus crotali (Pentastomida). — Comp. Biochem. Phys., (B, Bioch. Mol. Biol.) 53: 325-328. ROMER , A. S., 1996. The vertebrate body: shorter version. — Pp. 1-627. (AbeBooks Inc., Saunders, Philadelphia, PA.) RUDALL , K. M., 1955. The distribution of collagen and chitin. — Symp. Exp. Biol., 9: 49-71. RUDOLPHI , C. A., 1809. Histoire naturelle des entozoaires. — Vol. 2 (1): 1- 457, pl. 12. (Rücker, Berlin.)

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— —, 1891c. Bau und Entwicklungeschichte von Pentastomum proboscidium Rud. und P. subcylindricum Dies. — Z. Wiss. Zool., 52: 85-157, pls. 7-8. S TORCH , V., 1979. Contributions of comparative ultrastructural research to problems of invertebrate evoluton. — Amer. Zool., 19: 637-645. — —, 1984. Pentastomida. — In: J. B EREITER -H AHN , A. G. M ATOLTSY & K. S. R ICHARDS (eds.), Biology of the integument, 1, Invertebrata, pp. 709-713. (Springer-Verlag, Berlin.) — —, 1993. Pentastomida. — In: F. W. H ARRISON & M. E. R ICE (eds.), Microscopic anatomy of invertebrates, 12, Onychophora, Chilopoda, and lesser Protostomata, pp. 115-142. (Wiley-Liss, New York.) S TORCH , V. & W. B ÖCKELER , 1979. Electron microscopic observations on the sensilla of the pentastomid Reighardia sternae (Diesing, 1864). — Z. Parasit.-kund., 60: 77-86. — — & — —, 1982. Zur Ultrastruktur der Terminalanhänge larvaler Reighardia sternae (Pentastomida). — Z. Parasit.-kund., 68: 103-107. S TORCH , V., W. B ÖCKELER & J. R ILEY, 1990. Microscopic anatomy and ultrastructure of the male genital system in Porocephalus crotali and P. stilesi (Pentastomida: Porocephalida). — Parasit. Res., 76: 610-618. S TORCH , V. & B. G. M. JAMIESON, 1992. Further spermatological evidence for including the Pentastomida (tongue worms) in the Crustacea. — Int. J. Parasit., 22: 95-108. S TUNKARD , H. W. & C. P. G ANDAL, 1968. The pentastomes Waddycephalus terestiusculus (Baird, 1862) Sambon, 1922 and Parasambonia bridgesi n. gen., n. sp., from the lungs of the Australian snake Pseudechis porphyriacus. — Zoologica, N.Y., 53: 49-56. TAPPE , D. & D. W. B ÜTTNER, 2009. Diagnosis of human visceral pentastomiasis. — PLoS, (Negl. Trop. Dis.) 3: 1-7. T CHESUNOV, A. V., 2002. [A case of tongueworms (Pentastomida): a peculiar problem in context of the modern phylogenetics]. — Zh. Obsh. Biol., 63: 209-226. [In Russian.] T HOMAS , G. & W. B ÖCKELER , 1992a. Light and electron microscopical investigations of the midgut epithelium of different Cephalobaenida (Pentastomida) during digestion. — Parasit. Res., 78: 587-593. — — & — —, 1992b. Light and electron microscopical investigations on the feeding mechanism of Reighardia sternae (Pentastomida; Cephalobaenida). — Zool. Jahrb., (Anat.) 122: 1-12. — — & — —, 1994. Investigation of the intestinal spherocrystals of different Cephalobaenida (Pentastomida). — Parasit. Res., 80: 420-425. T HOMAS , G., S. S TENDER -S EIDEL & W. B ÖCKELER , 1999a. Investigation of different ontogenetic stages of Raillietiella sp. (Pentastomida: Cephalobaenida): excretory functions of the midgut. — Parasit. Res., 85: 274-279. — —, — — & — —, 1999b. Investigation of different ontogenetic stages of Raillietiella sp. (Pentastomida: Cephalobaenida): the midgut in nutrition and digestion. — Parasit. Res., 85: 312-319. — —, — — & — —, 1999c. Considerations about the ontogenesis of Reighardia sternae in comparison with Raillietiella sp. (Pentastomida: Cephalobaenida). — Parasit. Res., 85: 280283. T HRELFALL , W., 1971. Helminth parasites of alcids in the northwestern North Atlantic. — Can. J. Zool., 49: 461-466. T RAINER , J. E., J R ., J. T. S ELF & K. M. R ICHTER , 1975. Ultrastructure of Porocephalus crotali (Pentastomida) cuticle with phylogenetic implications. — J. Parasit., 61: 753-758. VANDEL , M., 1949. Embranchement des Arthropodes. Généralités. — In: P.-P. G RASSÉ (ed.), Traité de Zoologie, 6: 79-158. (Masson, Paris.) VARGAS V., M., 1970. A contribution to the morphology of the egg and nymphal stages of Porocephalus stilesi Sambon, 1910 and Porocephalus clavatus (Wyman, 1847) Sambon, 1910 (Pentastomida). — Rev. Biol. Trop., 17: 27-89.

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— —, 1974. The biology and taxonomy of Sebekia and Subtriquetra. — Proc. 3rd Int. Congr. Parasit., Munich, 2: 1021. — —, 1975. Descripcion del huevecillo, larva y ninfa de Subtriquetra subtriquetra Sambon, 1922 (Pentastomida), y algunas observaciones sobre su ciclo de vida. — Rev. Biol. Trop., 23: 67-75. VOBLIKOVA , N. V., 1961. [Cases of parasitism of adult Pentastomida in the reindeer.] — Zool. Zh., 40: 129-130. [In Russian.] WÄGELE , J. W. & P. K ÜCK , 2014. Arthropod phylogeny and the origin of the Tracheata (= Atelocerata) from Remipedia-like ancestors. — In: J. W. WÄGELE & T. BARTOLOMAEUS (eds.), Deep metazoan phylogeny: the backbone of the tree of life. New insights from analyses of molecules, morphology, and theory of data analysis, pp. 285-341. (de Gruyter, Berlin). [With 750 pp. in total.] WALDOW, H., 1908. Porocephalus moniliformis Dies. bei Kameruner. — Arch. Schiffs TropenHyg., 12: 321-324. — —, 1910. Porocephalus moniliformis Diesing, 1836 bei einem Kamerun-Neger. — Arch. Schiffs Tropen-Hyg., 14: 101, 506. WALLDORF, V. & R. R IEHL , 1985. Oogenesis in the pentastomid Raillietiella aegypti (Cephalobaenida). 1. Previtellogenic and vitellogenic stages. — Z. Parasit.-kund., 71: 113-124. WALOSSEK , D. & K. J. M ÜLLER , 1990. Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus. — Lethaia, 23: 409427. — — & — —, 1993. Die Wirbeltierparasiten Pentastomida lebten im Altpalaeozoikum im Meer. — Verh. Deutsch. Zool. Ges., 86: 148. — — & — —, 1994. Pentastomid parasites from the Lower Palaeozoic of Sweden. — Trans. Roy. Soc. Edinb., (Earth Sci.) 85: 1-37. WALOSSEK , D., J. E. R EPETSKI & K. J. M ÜLLER , 1994. An exceptionally preserved parasitic arthropod, Heymonsicambria taylori n. sp. (Arthropoda incertae sedis: Pentastomida), from Cambrian-Ordovician boundary beds of Newfoundland, Canada. — Can. J. Earth Sci., 31: 1664-1671. WALOSZEK , D., J. E. R EPETSKI & A. M AAS, 2006. A new Late Cambrian pentastomid and a review of the relationships of this parasitic group. — Trans. Roy. Soc. Edinb., (Earth Sci.) 96: 163-176. DOI:10.1017/S026359330000/280 W EBER , H., 1949. Grundriss der Insektenkunde. — (Gustav Fischer, Jena.) W INCH , J. M. & J. R ILEY, 1985. Experimental studies on the life-cycle of Raillietiella gigliolii (Pentastomida: Cephalobaenida) in the South American worm-lizard Amphisbaena alba: a unique interaction involving two insects. — Parasitology, 91: 471-481. — — & — —, 1986a. Studies on the behavior, and development in fish, of Subtriquetra subtriquetra — a uniquely free-living pentastomid larva from a crocodilian. — Parasitology, 93: 81-98. — — & — —, 1986b. Morphogenesis of larval development of Sebekia oxycephala (Pentastomida) from a South-American crocodilian (Caiman sclerops) in experimentally infected fish. — Z. Parasit.-kund., 72: 251-264. W INGSTRAND , K. G., 1972. Comparative spermatology of a pentastomid, Raillietiella hemidactyla, and a branchiuran crustacean, Argulus foliaceus, with a discussion of pentastomid relationships. — Kong. Dansk. Vidensk. Selsk., Biol. Skr., 19: 1-72, pls. 1-23. YAMAMOTO , H., S. T OSHIOKA , S. M ISHIMA , M. KOBAYASHI & N. O GURA , 1978. [A study of the pentastomids in Japan, with a key to the orders and genera]. — The Snake, 10: 143-150. [In Japanese.] YAN , J., J.-L. Z HOU , H.-Y. S UN & K. Z HOU, 2012. Nearly complete mitochondrial genome of Polyascus gregaria and the phylogenetic relationships among maxillopodans. — Mol. Biol. Rep., 39: 7413-7419. Z HANG , Q. Y., B. WANG , M. H UANG & T. T. C HENG, 1996. [Armillifer agkistrodontis disease: report of a case]. — Zhonghua Nei Ke Za Zhi [Chin. J. Int. Med.], 35: 747-749. [In Chinese.]

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Z HANG , X., D. S IVETER , D. WALOSZEK & A. M AAS, 2007. An epipodite-bearing crown-group crustacean from the Lower Cambrian. — Nature, Lond., 449: 595-598. Z RZAVÝ, J., 2001. The interrelationships of metazoan parasites: a review of phylum- and higher-level hypotheses from recent morphological and molecular phylogenetic analyses. — Fol. Parasit., Ceske Budejovice, 48: 81-103. http://faculty.uml.edu/rochberg/hochberglab/ courses/parasite/PDF%20papers/parasitology%20papers/interrelationships%20of%metazoan %20parasites.pdf

CHAPTER 53

ORDERS BOCHUSACEA, MICTACEA AND SPELAEOGRIPHACEA1 ) BY

GARY C. B. POORE

Contents. – Introduction and definition – Bochusacea Gu¸tu & Iliffe, 1998 – Mictacea Bowman, Garner, Hessler, Iliffe & Sanders, 1985 – Spelaeogriphacea Gordon, 1957. External morphology. Internal morphology. Reproduction and development. Ecology and conservation status – Ecology – Conservation status. Phylogeny and biogeography – Phylogeny – Biogeography. Systematics. Bibliography.

INTRODUCTION AND DEFINITION The description in 1957 by Isabella Gordon of an unusual, rather featureless new crustacean from a freshwater pool in a cave on Table Mountain in South Africa was the first in a series of discoveries of similar species occupying a variety of deep-sea, freshwater cavernicolous, and anchialine marine environments. While only eleven extant and three fossil species are now involved, their relationships are unclear and for the time being they are included in three orders of Peracarida that may or may not be related: Bochusacea, Mictacea, and Spelaeogriphacea.

1 ) To comply with current views on the taxonomy of these three groups of Peracarida, the original, French chapter on Spelaeogriphacea by G. A. Boxshall and that on Mictacea by R. R. Hessler have been combined for the present series, with the addition of a third taxon at order level that was proposed in the meantime, Bochusacea, under the authorship of G. C. B. Poore. This also means that what had earlier been planned as chapters 53 (Spelaeogriphacea) and 55 (Mictacea), is now united in a single chapter, no. 53. As we shall not change existing chapter nos. in this stage of the series, a chapter with no. 55 will accordingly be omitted from the numerical sequence. Originally conceived October 2014; latest additions January 2015.

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DIAGNOSES Bochusacea Gu¸tu & Iliffe, 1998 Cervical groove absent. Dorsal fold absent. Ocular lobe absent. Antennule, inner ramus rarely more than 6 articles, outer ramus with fewer than 10 articles. Antenna peduncle article 3 about third as long as article 4 (or more). Mandibular spine row and lacinia mobilis long, incisor and molar widely-spaced; palp with distal setae on article 3 only. Labium with acute apices, each bearing long seta; mesial faces bearing tooth plus 2 denticulate setae. Maxillule coxal endite with 4-5 spiniform setae; basal endite with distolateral row of denticulate setae (longer and distinct from distal spiniform setae), without lateral pappose setae (usually pair of facial long pappose setae instead). Maxilla basal endites longer than wide; endopod present as long external seta at base of outer lobe. Maxilliped basal endite with setae variously structured; epipod absent; palp article 5 aligned with article 4. Pereopods [= pereiopods] 1-7 with row of long setae on all articles; unguis long, setiform. Pereopod 1 enclosing mouthparts, ischium-merus articulation angled anteriorly; basis more elongate than that of pereopod 2; exopod present or absent. Pereopods 2-3 exopods of at least 3-4 articles. Pereopod 4 exopod of female of 2 or more articles. Pereopods 6 and 7 exopod present. Oostegites on pereopods 2-6, with marginal setae. Pleopods 1-5 reduced in females, biramous with linear rami in males. Uropodal endopod of 1 annulated article, exopod of 2 articles.

Mictacea Bowman, Garner, Hessler, Iliffe & Sanders, 1985 Cervical groove absent. Dorsal fold absent. Ocular lobe present. Antennule, inner ramus with 4 articles, outer ramus with 8 articles. Antenna peduncle article 3 about third as long as article 4 (or more). Mandibular spine row and lacinia mobilis long, incisor and molar widely-spaced; palp with lateral setae on articles 2 and 3. Labium with apices rounded, without long seta; mesial faces smooth. Maxillule coxal endite with 2 apical pappose setae; basal endite without distolateral row of denticulate setae or teeth, without lateral pappose setae (usually pair of facial long pappose setae instead). Maxilla basal endites longer than wide; endopod absent. Maxilliped basal endite with setae variously structured; epipod absent; palp article 5 aligned with article 4. Pereopods 1-7 with few short setae on articles; unguis short, curved. Pereopod 1 ambulatory or not enclosing mouthparts, ischium-merus articulation linear; exopod present. Pereopods 2-3 exopods of 2 articles. Pereopod 4 exopod of female of 2 articles. Pereopods 6 and 7 exopod absent. Oostegites on pereopods 1-5, without marginal setae. Pleopods 1-5 reduced except pleopod 2 in male which is elongate, 2-articulate. Uropodal endopod and exopod both of 2 articles.

Spelaeogriphacea Gordon, 1957 Cervical groove present (at least in part). Dorsal fold present. Ocular lobe present. Antennule, rami multiarticulate (more than 20 articles). Antenna peduncle article 3 very

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much shorter than article 4. Mandibular spine row and lacinia mobilis short and compact, incisor and molar closely-set; palp with lateral setae on articles 2 and 3. Labium with apices rounded, without long seta; mesial faces smooth. Maxillule coxal endite with 2-4 pappose setae; basal endite without distolateral row of denticulate setae or teeth, with single distolateral or facial pappose seta. Maxilla basal endites about a wide as long; endopod absent. Maxilliped basal endite with c. 8 short distomesial robust setae, lateral simple setae; epipod present; palp article 5 at right angles to article 4. Pereopods 1-7 with few short setae on articles; unguis short, curved. Pereopod 1 ambulatory or not enclosing mouthparts, ischium-merus articulation linear; exopod present. Pereopods 2-3 exopods of 2 articles. Pereopod 4 exopod of female of 1 article. Pereopod 6 exopod present, usually present on pereopod 7. Oostegites on pereopods 1-5, without marginal setae. Pleopods 1-5 well developed, biramous; exopods of 1 article; pleopod 2 modified in males. Uropodal endopod of 1 article, exopod of 2 articles.

EXTERNAL MORPHOLOGY G ENERAL HABITUS All members of the three orders are thin, elongate crustaceans of similar dimensions from head to tail. While there is some differentiation of a cephalothorax, the pereon [= pereion] and pleon can be only slightly distinguished. Adult Bochusacea have been reported from 1.4 to 5.7 mm long, 6 to 8 times as long as wide; in the only species where both males and females are known, Montucaris distincta, females are 1.5 times as long as males. Mictocaris halope, the only member of Mictacea, reaches 3.5 mm in length. Extant Spelaeogriphacea range from 3.5 to 7.5 mm, about 5 times as long as wide; in Mangkurtu kutjarra males and females are the same size while in Potiicoara brasiliensis females are 1.8 times as long as males. The cephalothorax comprises the cephalic somites and the fused first thoracic somite. It extends posteriorly as a dorsal fold [cf. “carapace” in other groups] only in Spelaeogriphacea and anteriorly more or less as a short rostrum in some species. The cephalothorax extends ventrolaterally as lappets to cover the bases of the mouthparts, with a longitudinal articulation in Bochusacea and Mictacea (Jaume et al., 2006, fig. 3) but not in Spelaeogriphacea. Spelaeogriphacea have paired partial lateral cervical grooves. The pereon comprises seven similar pereonites and the pleon six pleonites [or: pleomeres] plus a telson (fig. 53.1A-G). Pereonite 6 and the telson are distinguished by a suture dorsally but not ventrally (Jaume et al., 2013). All segments lack lateral plates. The telson (fig. 53.3H, I) is flat, posteriorly rounded, with the anus opening at the base of the telson in Mictocaris halope but terminally in Spelaeogriphacea and Bochusacea (Knopf et al., 2006). A PPENDAGES All species are blind but the Mictacea and Spelaeogriphacea have mobile, flat ocular lobes without visual elements. Bochusacea lack such lobes.

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Fig. 53.1. A, Hirsutia bathyalis, adult female; B, Mictocaris halope, adult female; C-D, Mangkurtu mityula, adult male; E-G, Spinogriphus ibericus, photograph of fossil and authors’ interpretations. [A, after Sanders et al., 1985; B, after Bowman & Iliffe, 1985; C, D, after Poore & Humphreys, 1998; E-G, after Jaume et al., 2013, supplied by D. Jaume, reproduced with permission from The Palaeontological Association.]

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Fig. 53.2. A, Mangkurtu mityula, mandible; B, Mangkurtu mityula, labium; C, Hirsutia bathyalis, labium; D, Mangkurtu mityula, maxillule; E, Mangkurtu mityula, maxilla; F, Montucaris distincta, maxilla; G, Thetispelecaris kumejimensis, maxilliped; H, Mangkurtu mityula, maxilliped. [A, B, D, E, H, after Poore & Humphreys, 1998; C, after Sanders et al., 1985; F, after Jaume et al., 2006, reproduced with permission from John Wiley and Sons; G, after Shimomura et al., 2012, reproduced with permission from Magnolia Press, Auckland.]

The antennules are biramous beyond a 3-articulate peduncle. The rami have 20 or more articles in Spelaeogriphacea (fig. 53.1C-G) but 10 or fewer in the other orders (fig. 53.1A-B). The peduncle of the antennae is 4- or 5-articulate with a scaphocerite (exopod) on the second article (fig. 53.1A-G); the remaining articles plus an annulated terminal article contribute to a flagellum often almost as long as the body (Boxshall & Jaume, 2013). The mandibles (fig. 53.2A) are well developed and obliquely forwardly directed; except in Spelaeogriphacea the molar and incisor are more widely spaced than in typical peracaridans. The molar is prominent, cylindrical, and with a strongly ornamented apex. The incisor is a thin multi-toothed narrow blade. The lacinia mobilis, present on the left mandible only, ends in 3-5 denticles. The spine row comprises thin spines. The mandibular palp comprises three articles (except in Spelaeogriphus lepidops with one article).

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The labium (paragnaths) comprises a pair of setiferous lobes separated by a deep angle in Spelaeogriphacea and Mictacea (fig. 53.2B) but in Bochusacea the lobes each terminate in an acute projection and have teeth-like structures on the mesial margins (fig. 53.2C). The maxillules (fig. 53.2D) are bilobed, representing coxal and basal endites. The inner coxal lobe is thin and carries a row of complex and varied setae. The outer basal lobe is larger, also has marginal setae, more robust mesially than laterally, but differs between orders. In Mictacea and Spelaeogriphacea a long, robust, pappose seta sits on the distolateral angle but in Bochusacea there is a row of long, denticulate setae along this margin. The maxillae (fig. 53.2E, F) comprise three lobes interpreted as representing a coxal endite and two basal endites. All lobes bear rows of long complex setae along their mesial and distal margins. Notable are the long sigmoid setae with multihooked or pectinate apices. The endopod is represented as a long seta in Bochusacea only. The maxillipeds (fig. 53.2G, H) have an enlarged basal endite, variously setose. Distal setae in Spelaeogriphacea are shorter and simpler than in the other taxa. The distal article of the 5-articulate palp is turned laterally at right angles to the main axis in Spelaeogriphacea but not in the other taxa. An epipod is present only in Spelaeogriphacea; it is cup-like in Spelaeogriphus lepidops, thick and oval in Potiicoara brasiliensis, and minutely digitiform in Mangkurtu spp. (fig. 53.1C). All seven pairs of pereopods (fig. 53.3A-C) are thin, comprising a coxa (probably articulating with the body at least in Bochusacea; Jaume et al., 2006), and six articles; those in Bochusacea are more complexly setose than in Spelaeogriphacea and Mictacea, and terminate in a more elongate unguis. Exopods of 1-4 articles are present on pereopod 1 (except in Hirsutia spp.), pereopods 2-5, pereopod 6 (except in Mictocaris halope), and pereopod 7 (only in Mangkurtu spp., Potiicoara brasiliensis). Exopods typically have setose margins (fig. 53.3A, B) but are gill-like on pereopod 4 and those more posterior in Spelaeogriphacea and Mictocaris halope (fig. 53.3C). Oostegites are present on the coxae of pereopods 2-6 in Bochusacea and on pereopods 1-5 in most Spelaeogriphacea and Mictocaris halope. Only in Bochusacea do the oostegites have marginal long setae while brooding. Paired tubular penes have been reported present on pereonal sternite 7 in Mangkurtu spp. (Poore & Humphreys, 1998, 2003), Potiicoara brasiliensis (cf. PiresVanin, 2012) and Montucaris distincta (cf. Jaume et al., 2006), and are assumed to be similar in all taxa. The five pairs of pleopods differ markedly between taxa. In females of Bochusacea, the pleopods are reduced to simple lobes or single articles (fig. 53.3G) while they are biramous in males; in males, each ramus is a single annulated article except for pleopod 2, which has a 2-articled exopod and inflated endopod. In Spelaeogriphacea, the pleopods have a muscular peduncle and two flattened oval rami, usually with marginal plumose setae in both sexes but the genera differ. In Spelaeogriphus, pleopods 1-4 have similar flattened oval rami of one article in both sexes, while pleopod 5 is reduced to a single article. In males of Mangkurtu and Potiicoara, pleopod 2 is modified (as in Bochusacea); the exopod is 2-articulate and the endopod curved and without marginal setae (fig. 53.3E).

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Fig. 53.3. A, Thetispelecaris yurikago, pereopod 4; B, Mangkurtu mityula, pereopod 2; C, Mangkurtu mityula, pereopod 4; D-E, Mangkurtu mityula, pleopods 1, 2 of male; F, Mictocaris halope, pereopod 2 of male; G, Thetispelecaris yurikago, ventral view of pleon showing pleopods; H, Mictocaris halope, left uropod and telson; I, Thetispelecaris yurikago, left uropod and telson; J, Mangkurtu mityula, left uropod. [A, G, I, after Ohtsuka et al., 2002; B-E, J, after Poore & Humphreys, 1998; F, H, after Bowman & Iliffe, 1985.]

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Males of Mangkurtu spp. (but not in other Spelaeogriphacea) and of Montucaris distincta (but not other Bochusacea) are similar in that the endopods of pleopods 1 and 3-5 bear a laterally-directed proximal projection (fig. 53.3D). In Mictocaris halope, the pleopods are single articles with apical setae except for pleopod 2 of the male, which is elongate and 2-articulate, the basal articles of the pair fused (fig. 53.3F). The uropods (fig. 53.3H-J) have a robust peduncle and have two rami with setose margins. The endopod has one, sometimes annulated, or two articles while the exopod is of two or three articles.

INTERNAL MORPHOLOGY Knowledge of the internal anatomy of these species is slight and concentrated on few species, notably Spelaeogriphus lepidops and Mictocaris halope (cf. Wirkner & Richter, 2007, 2010, 2013; Wirkner, 2009). Excretory and osmoregulatory systems have not been examined. The digestive system of Spelaeogriphus lepidops and Mictocaris halope comprises a short oesophagus leading to a voluminous stomach chamber filling most of the cephalothorax, the two sections separated by three valves. The stomach contains a complex filter apparatus. Posteriorly, a pylorus attaches to the stomach chamber, also containing a filter apparatus. An antechamber of the midgut glands is situated at the transition into the midgut, from which up to four tubular midgut glands emanate. The midgut is a straight tube running through the body and terminating in a short hindgut. The central nervous system in the cephalothorax includes a brain and a suboesophageal ganglion. Both species show some reduction of the protocerebrum correlating with the absence of eyes. The circulatory system is made up of a tubular heart in the thorax. It is equipped with two pairs of incurrent ostia in Spelaeogriphus lepidops (at the posterior borders of pereonites 4 and 6) and one pair in Mictocaris halope (in pereonite 1). The only artery leading off the heart is the anterior aorta, which runs into the cephalothorax. The heart is dilated between the brain and the anterior stomach wall to form a space into which oesophageal dilator muscles are internalized. This myoarterial formation is hypothesized as an accessory pulsatile structure in the anterior cephalothorax.

REPRODUCTION AND DEVELOPMENT All species brood eggs and larvae in a marsupium formed by the oostegites as do typical members of Peracarida, but direct observations are few (Olesen et al., 2014). The female of Thetispelecaris yurikago has paired ovaries in the cephalothorax connecting via paired oviducts to seminal receptacles in pereonites 5 and 6 and paired gonopores opening at the base of pereopod 5 (Ohtsuka et al., 2002). Pires (1987) suggested that females of Potiicoara brasiliensis can attain fully developed oostegites over two instars, while three

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is the case for Montucaris distincta (cf. Jaume et al., 2006). Poore & Humphreys (2003) reported a female of Mangkurtu kutjarra brooding 16 eggs and another with four embryos. Spelaeogriphus lepidops carries up to 12 eggs (Gordon, 1957); Potiicoara brasiliensis carries 7-12 eggs or up to 12 embryos (Pires-Vanin, 2012). Males have tubular penes on the sternum of pereonite 7 and, for the species known, have variously modified pleopods. In Mictocaris halope, the male pleopod 2 is extremely elongate while in Spelaeogriphacea the exopod of pleopod 2 lacks setae. The male of Montucaris distincta might attain a terminal male stage with reduced mouthparts (Jaume et al., 2006). Juveniles of Bochusacea and Mictacea pass through manca stages as do many other peracaridans — it is presumed that Spelaeogriphacea do as well. Manca-I lacks pereopods 7, manca-II has budding pereopods 7, manca-III has a partly formed pereopod 7, and manca-IV has pereopods with exopods smaller than those of an adult male. Thetispelecaris remex passes through at least three of these stages (Gutu & Iliffe, 1998) and Montucaris distincta through all four (Jaume et al., 2006).

ECOLOGY AND CONSERVATION STATUS Ecology All extant members of the three orders are associated with benthic sediments in dark or near dark environments and are active swimmers. Bochusacea are known from two divergent marine habitats. Species of Hirsutia and Montucaris occur in the deep sea, the few known records between 600 and 1500 m depth. Species of Thetispelecaris on the other hand are confined to anchialine or submarine caves. The only species of Mictacea also inhabits anchialine caves. Mictocaris halope swims in open water, typically only in deeper, fully marine waters in those parts of the cave that are relatively more remote from connection with the open sea and therefore where waters tend to have a longer residence time within the cave (Bowman & Iliffe, 1985; Schram, 1986). Fossil Spelaeogriphacea have been reported from near-shore marine sediments or from freshwater river and lake sediments. Extant species are all from fresh water, two in groundwater and two in caves. Shen et al. (1999) hypothesized that Spelaeogriphacea have at some time in their history, between the Carboniferous and the Late Jurassic, certainly by the time of Liaoningogriphus quadripartitus, shifted from marine to freshwater lacustrine habitats. At the same time species invaded cavernicolous and/or groundwater habitats. Spelaeogriphus lepidops is an active swimmer undulating the pleon and flapping the pleopods (Grindley, 1976). R ESPIRATION The paddle-like setose exopods of pereopods 1-3 of Spelaeogriphus lepidops ventilate the cup-shaped maxillipedal epipod under the lateral lobes of the carapace while the exopods of pereopods 4-7, lacking setae, function as gills by pumping water forward

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under the lateral carapace lobes (Grindley & Hessler, 1971). Potiicoara brasiliensis also possesses a substantial maxillipedal epipod, but in Mangkurtu spp. the epipod is minute, while the posterior pereopodal exopods are similarly branchial. In Bochusacea and Mictacea, all pereopodal exopods are linear and setose, smaller on pereopod 1 than posteriorly, so respiration may well be achieved quite differently. The inner surface of the lateral carapace lobes in these taxa is probably the principal respiratory surface (Olesen, 2013; Wirkner & Richter, 2013). F EEDING Feeding has been reported only in Spelaeogriphus lepidops, which chases particles of detritus especially those gathering in sand ripples (Grindley, 1976). Hirsutiids are probable scrapers of small particles with occasional involvement of the first pereopods in gripping and transferring large food items directly to the mandibles. In Hirsutia sandersetalia (cf. Just & Poore, 1988) and Montucaris distincta, the digestive tract was observed to be full of fine-grained, amorphous material from end to end. Terminal males of the latter species have regressed mouthparts and might not feed. The extraordinary degree of ornamentation of hirsutiids suggests that feeding is selective (Jaume et al., 2006).

Conservation status Mictocaris halope occurs in only five caves within an area of 1 km2 in Bermuda, an area subject to adverse environmental pressures resulting from cesspit sewage pollution, rock quarries, and tourism. For these reasons the species qualifies for the Critically Endangered status under International Union for the Conservation of Nature (IUCN) criteria (Iliffe, 2014). The groundwater-dependent ecosystems of the Pilbara in Western Australia have been identified as an international hotspot for stygofaunal species (Boulton et al., 2003; Eberhard et al., 2005). Two of the four spelaeogriphacean species, both in the genus Mangkurtu, are known only from this environment. Subterranean water has been heavily exploited for agriculture in this area, where no significant streams or lakes exist, putting this fauna at risk. According to IUCN criteria the third species, Spelaeogriphus lepidops, should be considered Critically Endangered, its extent of occurrence in South Africa being less than 100 km2 (Sharratt et al., 2000). The fourth species on the other hand, Potiicoara brasiliensis, occurs over a wide area of karst environments in Brazil and possibly beyond.

PHYLOGENY AND BIOGEOGRAPHY Phylogeny Numerous studies have attempted to elucidate peracaridan relationships (Siewing, 1963; Schram, 1981, 1986; Watling, 1981, 1983, 1999; Hessler, 1983; Pires, 1987; Wagner, 1994; Mayrat & de Saint Laurent, 1996; Schram & Hof, 1998; Wheeler, 1998; Wills,

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1998; Richter & Scholtz, 2001) and were reviewed and tested using cladistic methods by Poore (2005). Poore’s (2005) analysis supported two monophyletic taxa, Mictacea as originally proposed by Bowman et al. (1985) to include Mictocarididae and Hirsutiidae, and Spelaeogriphacea (Spelaeogriphidae). This analysis received some support from Wills et al. (2009). The position of fossil Spelaeogriphacea was uncertain in both analyses because of the paucity of characters. Spears et al. (2005) found Spelaeogriphus lepidops to be sister to three species of Amphipoda on the basis of molecular analysis but there is little morphological support for this relationship and Jenner et al. (2009) suspected the molecular result was an artefact resulting from long branch attraction. Gu¸tu (2001) suggested, Wilson (2009) and Jenner et al. (2009) supported, and Jaume et al. (2013) elaborated on similarities between Hirsutiidae and Tanaidacea. Jenner et al. (2009) found molecular and morphological support for Thetispelecaris remex being related to Lophogastrida. Tabacaru & Danielopol (2011) concluded that Spelaeogriphacea are related to a clade containing Tanaidacea and Cumacea, together grouped as Hemicarida by Schram (1981) before Mictocarididae and Hirsutiidae were discovered [although anticipated by him as one of the missing morphotypes in his “matrix of paper animals” (Schram, 1983: 338)]. Tabacaru & Danielopol (2011) also concluded that Mictacea s.s. and Bochusacea are sister taxa. Wilson’s (2009) analysis of a large morphological dataset was unable to resolve the relationships of Mictocaris and Spelaeogriphus to Thermosbaenacea, Cumacea, Tanaidacea, and Isopoda with which they shared a monophyletic clade. The phylogenetic relationships between Hirsutiidae (Bochusacea), Mictocarididae (Mictacea), Spelaeogriphidae (Spelaeogriphacea) and the other orders of Peracarida are far from resolved confidently. As a consequence, the taxonomy adopted here (see below) is interim at best.

Biogeography All four extant spelaeogriphacean species have restricted ranges in fresh water on Gondwanan continental fragments, South Africa, Australia and South America (Poore & Humphreys, 2003). The three so-called spelaeogriphacean fossils are more widely scattered, Carboniferous marine sediment in Canada (Schram, 1974), Jurassic in China (Shen et al., 1998), and Cretaceous lacustrine sediments in Spain (Jaume et al., 2013). From these distributions it can be inferred that the penetration of Spelaeogriphacea into continental waters from shallow marine water on the margins of the Tethys Sea took place prior to the fragmentation of Gondwana (starting c. 140 Mya), and that their current distribution pattern reflects plate tectonic history (Poore & Humphreys, 1998, 2003). Mictocaris halope, restricted to Bermuda, inhabits a mid-ocean volcanic seamount capped with Pleistocene and Recent marine and aeolian sediments (Bowman & Iliffe, 1985). While its marine origin is undoubted, its closest relative is more controversial. Bochusacea include two bathyal species from the Atlantic (Sanders et al., 1985; Jaume et al., 2006), one bathyal species from the South Pacific (Just & Poore, 1988), two anchialine species from islands around the Caribbean Sea (Gu¸tu & Iliffe, 1998; Ohtsuka et al., 2002) and one species from a submarine cave in the northwestern Pacific (Shimomura

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et al., 2012). Such a widespread distribution seems best explained by invasion of deepsea and anchialine environments from shallow water (Ohtsuka et al., 2002), a conclusion supported by research on phylogenetics and distribution of copepods (Boxshall & Jaume, 2000) and ostracods (Iglikowska & Boxshall, 2013).

SYSTEMATICS The arrangement of orders, families and genera followed here depends on that most recently advocated, e.g., by Jaume et al. (2013), and adopted by WoRMS Editorial Board (2014). It differs from earlier views, notably that of Poore (2005), who supported the original concept of Mictacea including Mictocarididae and Hirsutiidae (Bowman et al., 1985). An alternative classification ranks Mictacea and Spelaeogriphacea as suborders with one family each of the order Cosinzeneacea Gu¸tu, 1998, and a second order Bochusacea for Hirsutiidae alone (Gu¸tu & Iliffe, 1998; Gu¸tu, 2001). All species are listed here. The three fossil taxa are included in one family, Acadiocarididae, of Spelaeogriphacea. All are superficially similar to Spelaeogriphacea but lack most limb features, so confidence in placing them in this order rather than either of the other two is low (Poore, 2005). C LASSIFICATION B OCHUSACEA Gu¸tu & Iliffe, 1998. One family with three genera. H IRSUTIIDAE Saunders, Hessler & Garner, 1985 [Diagnosis as for the order, see above] Hirsutia Sanders, Hessler & Garner, 1985: Hirsutia bathyalis Sanders, Hessler & Garner, 1985; Hirsutia sandersetalia Just & Poore, 1988 Montucaris Jaume, Boxshall & Bamber, 2006: Montucaris distincta Jaume, Boxshall & Bamber, 2006 Thetispelecaris Gu¸tu & Iliffe, 1998: Thetispelecaris kumejimensis Shimomura, Fujita & Naruse, 2012; Thetispelecaris remex Gu¸tu & Iliffe, 1998; Thetispelecaris yurikago Ohtsuka, Hanamura & Kase, 2002 M ICTACEA Bowman, Garner, Hessler, Iliffe & Sanders, 1985. Monotypic. M ICTOCARIDIDAE Bowman & Iliffe, 1985 [Diagnosis as for the order, see above] Mictocaris Bowman & Iliffe, 1985: Mictocaris halope Bowman & Iliffe, 1985 S PELAEOGRIPHACEA Gordon, 1957. One family with three monotypic fossil genera and one extant family of three genera; * = fossil. *ACADIOCARIDIDAE Schram, 1974 [Diagnosis: “No optic notch on carapace; thoracopodal endopods well developed; natatory pleopods on the first five pleomeres (M. Miss.)” (Schram, 1974)] *Acadiocaris Brooks, 1962: Acadiocaris novascotica (Copeland, 1957) [Palaeocaris Copeland, 1957] *Liaoningogriphus Shen & Taylor, 1998 in Shen, Taylor & Schram, 1998: Liaoningogriphus quadripartitus Shen & Taylor, 1998 in Shen, Taylor & Schram, 1998 *Spinogriphus Jaume, Pinardo-Moya & Boxshall, 2013: Spinogriphus ibericus Jaume, Pinardo-Moya & Boxshall, 2013

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S PELAEOGRIPHIDAE Gordon, 1957 [Diagnosis as for the order, see above] Mangkurtu Poore & Humphreys, 1998: Mangkurtu kutjarra Poore & Humphreys, 2003; Mangkurtu mityula Poore & Humphreys, 1998 Potiicoara Pires, 1987: Potiicoara brasiliensis Pires, 1987 Spelaeogriphus Gordon, 1957: Spelaeogriphus lepidops Gordon, 1957

ACKNOWLEDGMENTS This chapter builds on two earlier contributions to the Traité de Zoologie, on Mictacea (Hessler, 1999) and Spelaeogriphacea (Boxshall, 1999). I thank Geoff Boxshall for comments on a first draft and Damìa Jaume for supplying figures.

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— — & — —, 2003. Second species of Mangkurtu (Spelaeogriphacea) from north-western Australia. — Records of the Western Australian Museum, 22: 67-74. R ICHTER , S. & G. S CHOLTZ, 2001. Phylogenetic analysis of the Malacostraca (Crustacea). — Journal of Zoological, Systematic and Evolutionary Research, 39: 113-136. S ANDERS , H. L., R. R. H ESSLER & S. P. G ARNER, 1985. Hirsutia bathyalis, a new unusual deep-sea benthic peracaridan crustacean from the tropical Atlantic. — Journal of Crustacean Biology, 5: 30-57. S CHRAM , F. R., 1974. Paleozoic Peracarida of North America. — Fieldiana Geology, 33: 95-124. — —, 1981. On the classification of Eumalacostraca. — Journal of Crustacean Biology, 1: 1-10. — —, 1983. Method and madness in phylogeny. — In: F. R. S CHRAM (ed.), Crustacean phylogeny. Crustacean Issues, 1: 331-350. (A. A. Balkema, Rotterdam.) — —, 1986. Crustacea. — Pp. i-xii, 1-606. (Oxford University Press, New York.) S CHRAM , F. R. & C. H. J. H OF, 1998. Fossils and the interrelationships of major crustacean groups. — In: G. D. E DGECOMBE (ed.), Arthropod fossils and phylogeny, pp. 233-302. (Cambridge University Press, New York.) S HARRATT, N. J., M. D. P ICKER & M. J. S AMWAYS, 2000. The invertebrate fauna of the sandstone caves of the Cape Peninsula (South Africa): patterns of endemism and conservation priorities. — Biodiversity and Conservation, 9: 107-143. S HEN , Y.- B ., F. R. S CHRAM & R. S. TAYLOR, 1999. Liaoningogriphus quadripartitus (Malacostraca: Spelaeogriphacea) from the Jehol biota and notes on its paleoecology. — Palaeoworld, 11: 175-184. S HEN , Y.- B ., R. S. TAYLOR & F. R. S CHRAM, 1998. A new spelaeogriphacean (Crustacea: Peracarida) from the Upper Jurassic of China. — Contributions to Zoology, 68: 19-35. S HIMOMURA , M., Y. F UJITA & T. NARUSE, 2012. First record of the genus Thetispelecaris Gu¸tu & Iliffe, 1998 (Crustacea: Peracarida: Bochusacea) from a submarine cave in the Pacific Ocean. — In: T. NARUSE , T.-Y. C HAN , H. H. TAN , S. T. A HYONG & J. D. R EIMER (eds.), Scientific results of the Marine Biodiversity Expedition — KUMEJIMA 2009. Zootaxa, 3367: 69-78. S IEWING , R., 1963. Studies in malacostracan morphology: results and problems. — In: H. B. W HITTINGTON & W. D. I. ROLFE (eds.), Phylogeny and evolution of Crustacea. Museum of Comparative Zoology, Special Publication, 13: 85-103. S PEARS , T., R. W. D E B RY, L. G. A BELE & K. C HODYLA, 2005. Peracarid monophyly and interordinal phylogeny inferred from nuclear small-subunit ribosomal DNA sequences (Crustacea: Malacostraca: Peracarida). — Proceedings of the Biological Society of Washington, 118: 117157. TABACARU , I. & D. L. DANIELOPOL, 2011. Essai d’analyse critique des principales hypothèses concernant la phylogénie des Malacostracés (Crustacea, Malacostraca). — Travaux de l’Institut Spéléologique, Émile Racovitza, 50: 87-119. WAGNER , H. P., 1994. A monographic review of the Thermosbaenacea (Crustacea: Peracarida). — Zoologische Verhandelingen, Leiden, 291: 1-338. WATLING , L., 1981. An alternative phylogeny of peracarid crustaceans. — Journal of Crustacean Biology, 2: 201-210. — —, 1983. Peracaridan disunity and its bearing on eumalacostracan phylogeny with a redefinition of eumalacostracan superorders. — In: F. R. S CHRAM (ed.), Crustacean Phylogeny. Crustacean Issues, 1: 213-228. (A. A. Balkema, Rotterdam.) — —, 1999. Toward understanding the relationships of the peracaridan orders: the necessity of determining exact homologies. — In: F. R. S CHRAM & J. C. VON VAUPEL K LEIN (eds.), Crustaceans and the biodiversity crisis. Proceedings of the Fourth International Crustacean Congress, Amsterdam, The Netherlands, July 20-24, 1998, 1: 73-89. (Brill, Leiden.) W HEELER , W. C., 1998. Sampling, groundplans, total evidence and the systematics of arthropods. — In: R. A. F ORTEY & R. H. T HOMAS (eds.), Arthropod relationships. The Systematics Association Special Volume Series, 55: 87-96. (Chapman & Hall, London.)

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W ILLS , M. A., 1998. A phylogeny of recent and fossil Crustacea derived from morphological characters. — In: R. A. F ORTEY & R. H. T HOMAS (eds.), Arthropod relationships. The Systematics Association Special Volume Series, 55: 189-210. (Chapman & Hall, London.) W ILLS , M. A., R. A. J ENNER & C. N. D HUBHGHAILL, 2009. Eumalacostracan evolution: conflict between three sources of data. — Arthropod Systematics & Phylogeny, 67: 71-90. W ILSON , G. D. F., 2009. The phylogenetic position of the Isopoda in the Peracarida (Crustacea: Malacostraca). — Arthropod Systematics & Phylogeny, 67: 159-198. W IRKNER , C. S., 2009. The circulatory system in Malacostraca — evaluating character evolution on the basis of differing phylogenetic hypotheses. — Arthropod Systematics & Phylogeny, 67: 57-70. W IRKNER , C. S. & S. R ICHTER, 2007. The circulatory system and its spatial relations to other major organ systems in Spelaeogriphacea and Mictacea (Malacostraca, Crustacea) — a threedimensional analysis. — Zoological Journal of the Linnean Society, London, 149: 629-642. — — & — —, 2010. Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). — Cladistics, 26: 143-167. — — & — —, 2013. Circulatory system and respiration. — In: L. WATLING & M. T HIEL (eds.), The natural history of the Crustacea, 1, Functional morphology and diversity, pp. 376-412. (Oxford University Press, London.) W O RMS E DITORIAL B OARD, 2014. World Register of Marine Species. — Available from http://www.marinespecies.org at VLIZ [accessed 31 August 2014].

CHAPTER 56

ORDER AMPHIPODA LATREILLE, 18161 ) BY

DENISE BELLAN-SANTINI

Contents. – Introduction. External morphology – General habitus – Tagmata of the body. Internal anatomy – Integument and colour – Musculature – Nervous system – Sense organs – Circulatory system – Respiratory system – Digestive system – Excretory system – Various other glands and organs – Genital apparatus – Chromosome complement – Molecular genetic markers. Reproduction and development – Reproduction – Growth – Life cycle and reproductive periods – Determination of sex. Physiology – Respiration – Osmoregulation – Calcium metabolism. Ethology – Behaviour – Feeding. Ecology – The influence of environmental factors – Interrelationships with other species – Distribution and biogeography – Importance of amphipods in biocoenoses. Origin and phylogeny of the Amphipoda – Palaeontological origin – Phylogenetic classification. Amphipods and man. Systematics – The present state of amphipod taxonomy – Suborder Gammaridea Latreille, 1802 – Suborder Corophiidea Leach, 1814 – Suborder Hyperiidea H. Milne Edwards, 1830. Acknowledgements. Appendix. Bibliography. Note added in proof.

INTRODUCTION The order Amphipoda comprises approx. 10 000 described species. In 1991, Barnard & Karaman listed 5733 species for Gammaridea alone, subsequently Vader (2005) counted 6950 gammarideans without the Talitridae, which Serejo (2004) had earlier estimated at including about 400 species. Recently, Ahyong et al. (2011) calculated a total of 9896 spp. for Amphipoda as a whole. The representatives of this order occur in all permanent aquatic habitats and even in some terrestrial biotopes. In the marine realm they are found from the littoral zones down into the hadal trenches (Halice subquarta, at 10 500 m depth). Some live on land, on 1 ) The original edition of 1999 by D. Bellan-Santini was updated by the author October 2012; latest

additions February 2015. © Koninklijke Brill NV, Leiden, 2015

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and in the soil, though they are sparsely represented there, whereas they frequently occur in almost all continental waterbodies, fresh and brackish. Their occurrence up to high altitudes in the mountains (Hyalella curvispina, at 4100 m a.s.l. in the Andes) is well documented. Hardly any ecological niches have not been occupied by amphipods: there are pelagic species, benthic forms as well as benthopelagic representatives, while there also are species that thrive in forest litter, and a few live as commensals or parasites. The order Amphipoda was, in its classical concept, divided into four suborders: Gammaridea, Hyperiidea, Caprellidea, and Ingolfiellidea. Dahl (1977) and subsequently Bowman & Abele (1982) reduced this complement to three suborders by including Ingolfiellidea in Gammaridea. Myers & Lowry (2003) revised the Corophiidea and reunited these with the Caprellidea thus creating a suborder Corophiidea. Hence, currently the Amphipoda are to be divided into three suborders, i.e., Gammaridea, Corophiidea and Hyperiidea. (However, see also the Note added in Proof at the end of this chapter.) Amphipods are classified in the superorder Peracarida Calman, 1904, i.e., among forms that are conceived as Malacostraca Latreille, 1806, deprived of a carapace. The head is fused with one or two thoracic somites, the eyes are sessile if present at all, the antennules are often equipped with an accessory (second) flagellum, the antennae are uniramous. The pereiopods have no exopodite, while some bear a gill. The anterior pereiopods are often modified as prehensile organs, the first pair always being transformed into maxillipeds (though in descriptive diagnoses these are never considered pereiopods but instead as ranking among the mouthparts). The second and third thoracic appendages are typically subcheliform, but may be cheliform as well; these are denoted as gnathopods. The five succeeding pairs are true pereiopods that serve locomotion. The first three pairs of pleopods are adapted to swimming but these appendages can be reduced in some species. The three following pairs are denoted as uropods. The telson is typically free. In most species of Amphipoda the development is direct and takes place in the brood pouch of the female.

EXTERNAL MORPHOLOGY General habitus Size. – In general, amphipods are small species of crustaceans. By far the majority has a body length hardly above 1 cm, while the smaller ones measure approx. 1 mm. As a giant representative, often Alicella gigantea has been cited with no less than 14 cm in total length. However, observations made with the aid of submersible cameras at bathyal depths, allowed Hessler et al. (1971) to produce photographs of an amphipod reaching 28.2 cm in length, while Schulenberger & Hessler (1974) report Amphipoda of over 30 cm. At present, amphipods of these sizes have been collected already many times: their generalized attribution to the species Alicella gigantea, however, remains doubtful.

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Fig. 56.1. General habitus of a typical amphipod.

General body shape. – The overall shape of the body varies distinctly among the various amphipod suborders. In Gammaridea, by far the best represented suborder comprising 80% of the known species, the shape varies according to the various families. Nonetheless, most amphipods conform sufficiently to a general, common Bauplan to be recognized as an amphipod without any problem. No matter how differentiated the various species can be, there always is a certain number of characters that links them to that common morphotype. A typical amphipod (fig. 56.1) is a small crustacean, approx. 1 cm in total length, with a laterally compressed, arched body, divided into three distinct parts: a head, a pereion that is most often composed of 7 somites (thoracomeres), and a pleon comprising 6 somites. The pereion bears seven pairs of pereiopods in two groups: four are directed anteriorly, three towards posterior. The first two pairs of pereiopods are most often transformed into gnathopods. The coxae of the pereiopods are flattened like shields (coxal plates) and thus extend the lateral parts of the exoskeleton of their corresponding somite. The pleon bears the classical arrangement of six pairs of appendages: three pairs of pleopods and three pairs of uropods. In addition to this average shape, much variation is found and some deviant forms are both widespread among amphipods and of grossly different shape. The body can be strongly dorso-ventrally compressed (Phliantidae and Cyamidae), or somewhat less strongly (Corophiidae), or else be filiform (the genus Ingolfiella as well as the Caprellidea), or, in contrast, be globular in shape (some Hyperiidea) (fig. 56.2). As regards the pereiopods, these can be vestigial (Caprella) or, to the contrary, be extremely developed (2nd gnathopods in the genus Melita; pereiopods 5, 6, and 7 in the species of Haustorius) (fig. 56.3). Also the coxal plates can vary considerably in shape and development: these may be reduced, accentuating the filiform body shape (Ingolfiellidae, Melphidippidae,

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Fig. 56.2. Various types of amphipods. A, Neohela monstrosa (Unciolidae); B, Corophium affine (Corophiidae); C, Ceinina japonica (Eophliantidae); D, Quasimodia enna (Phliantidae); E, Caprella acanthifera (Caprellidae); F, Hyperia galba (Hyperiidae); G, Cyamus ovalis (Cyamidae).

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Fig. 56.3. Different types of pereiopods. A, Phtisica marina (Caprellidae); B, Melita palmata (Melitidae), both external (ext) and internal (int) side; C, Haustorius algeriensis (Haustoriidae), pereiopods 6 and 7 (P6, P7).

certain Corophiidae) or, instead, be developed to gross proportions to form a kind of lateral girdle that more or less covers the appendages (Lysianassidae, Stenothoidae, Stegocephalidae) (fig. 56.4).

Tagmata of the body T HE HEAD Though the term “head” is in common use in amphipod taxonomy, it is basically incorrect, as the body part denoted as such represents the fusion of the cephalon proper and the first thoracomere: it is, in fact, a cephalothorax. The fusion of the true head with the thorax even includes also the second thoracomere in certain Caprellidea and in Metaingolfiella. The appendages of the first thoracic somite that is fused with the cephalon have been transformed into prehensile organs, the maxillipeds. The head itself usually bears the eyes, two pairs of antennae, and the mouthparts. The shape of the head is mostly cylindrical or spherical, but may also be elongate as in Caprella, or bear a rostrum,

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Fig. 56.4. Different types of coxal plates. A, Stomacontion pepinii (Lysianassidae); B, Stegocephaloides christianensis (Stegocephalidae); C, Peltocoxa gibbosa (Cyproideidae); D, Stenothoe marina (Stenothoidae).

sometimes of enormous size, that gives the species the appearance of a long drawn-out stylet (Oxycephalidae, some Phoxocephalidae, and Oedicerotidae) (fig. 56.5). The eyes are sessile and composed of numerous ommatidia in apposition, while some authors are of the opinion that the eyes with lenses of Ampelisca in fact represent simple, ocelli-like eyes. The compound eyes are developed to varying extents, being absent in cavernicolous species and showing large to even enormous sizes in some Hyperiidea as well as in the males of a variety of benthic forms. The antennules (or 1st antennae, first antennae, antennae 1, antennae I) consist of a peduncle of three segments, a multisegmented principal flagellum, and sometimes also an accessory flagellum that is, if present, often short. The antennae (or 2nd antennae, second antennae, antennae 2, antennae II) have a five-segmented peduncle and a single, multisegmented flagellum. The antennae can bear setae, scales, and calceoli (fig. 56.26). Their size often differs according to the sexes. In Hyperiidea, there generally is a reduction in the number of segments of the peduncles of the antennae 1 and 2. The flagella may be composed of a small number of undivided segments. Accessory flagella are absent.

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Fig. 56.5. Different types of heads. A, Oxycephalus piscator (Oxycephalidae); B, Leptophoxus falcatus (Phoxocephalidae); C, Mandibulophoxus uncirostratus (Phoxocephalidae); D, Monoculodes carinatus (Oedicerotidae).

Most amphipods are equipped with mouthparts that conform to a common scheme (fig. 56.6), but in various groups substantial transformations can be observed, up to and including major reductions. The most frequently occurring type comprises an upper lip (labrum) in front of the mouth opening and a lower lip (labium) behind. The cephalic part anteriorly of the labrum is sometimes drawn out into an acute point or into a lobe called epistome, which organ is often used in taxonomic descriptions (e.g., Lysianassidae). The labium is deeply bilobate and in some cases even quadrilobate. Between those lips on both sides of the mouth, the mandibles are situated, each consisting of a molar process that can be provided with grooves and may bear specialized setae (Saudray, 1971), an incisor process ending in toothed lamellae and teeth, and finally bear a palp that most often is triarticulate but that may also have undergone reductions up to and including its total disappearance. Sometimes there is a lacinia mobilis (an articulated toothed lamella) on one of the mandibulae, as an accessory structure at the level of the incisor process. Behind the labium a pair of maxillulae (first maxillae or maxillae 1) is inserted, each of which is composed of two lobes fringed with setae and/or spines, and a palp. The maxillae (second maxillae or maxillae 2) follow posteriorly, and these are much simpler than the maxillules: they merely comprise two lobes bearing long setae. The appendages next in line are the maxillipeds and these correspond to the appendages of the first thoracomere that has been fused with the head proper. As primarily prehensile

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Fig. 56.6. Mouthparts of Elasmopus rapax (Maeridae). A, Labrum. B, Labium. C, Mandible, with: c1, molar process; c2, incisor process; c3, lacinia mobilis; c4, palp. D, Maxilla 1. E, Maxilla 2. F, Maxillipeds, with: f1, inner plate; f2, outer plate; f3, palp.

organs they arise from an undivided segment formed from the fusion of the pair of coxae; the basis and ischium are equipped with strongly developed masticatory lobes (endites) while the remaining segments make up a palp. The mouthparts may show considerable modifications: either significant enlargement, or severe reduction, up to total disappearance of some of these parts (fig. 56.7). Enlargements can affect the labium, which may bear internal lobes, sometimes themselves bilobate (Ampithoe); the palps of the maxillules (Stilipes, Pardalisca); as well as the incisor process of the mandible (Pardaliscidae). Reductions often affect the palps, which can disappear as is the case in the mandibular palp in Phliantidae and Dexaminidae. Also other mouthparts

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Fig. 56.7. Modifications of mouthparts. A, Labrum, of: a1, Dulichiopsis nordlandica (Dulichiidae); a2, Stegocephaloides christianensis (Stegocephalidae). B, Labium, of: b1, Bumeralius bucholicus (Zobrachoidae); b2, Ampithoe ramondi (Ampithoidae); b3, Stegocephaloides christianensis. C, Maxilla 1, of: c1, Bumeralius bucholicus; c2, Iphimedia obesa (Iphimediidae); c3, Iphimedia minuta; c4, Ochlesis innocens (Ochlesidae). D, Maxilla 2, Bumeralius bucholicus. E, Mandible, of: e1, Hippomedon massiliensis (Lysianassidae); e2, Bumeralius bucholicus; e3, Ochlesis innocens; e4, Bircenna fulva (Eophliantidae). F, Maxilliped, of: f1, Ampithoe ramondi; f2, Bumeralius bucholicus; f3, Bircenna fulva; f4, Liljeborgia psaltrica (Liljeborgiidae).

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can show either strong or weak reductions, as, e.g., the incisor and molar processes in Kerguelenia, but sometimes only the molar process is reduced, in which case the mandible has become shaped as needle (Iphimediidae). Certain genera, like Anamixis, show a strong atrophy of the buccal apparatus as a whole, which lacks mandibles, a labium, maxillae, as well as endites on the maxillipeds. The total complement of the mouthparts is considered important from a systematic point of view, and various taxa have been either split up, or fused, based on variations in the features of the mouthparts. In contrast, the taxonomic importance of their fine structure remains only limited: Oleröd (1975) studied microstructures of the mouthparts with the scanning electron microscope (SEM) and could demonstrate that the wear experienced by various parts precluded these from providing significant, discriminating characters. T HE PEREION The pereion or mesosome is composed of seven free somites, thus disregarding the originally first thoracic somite that is now fused with the head. Only in Caprellidea and part of the Ingolfiellidea the number of free somites has been reduced to six. Those free body segments are generally well separated but can be partially coaslesced in some Hyperiidea. They bear the pereiopods, basically one pair per somite, hence a maximum total of seven pairs, that have been regrouped into two series: four anterior and three posterior pairs. The anterior pairs are directed to the front, with the exception of the dactyli that are turned backwards. The three posterior pairs show the reverse orientation. The pereiopods are often long and slim, but the two anteriormost pairs are usually transformed into gnathopods, i.e., prehensile appendages. Numbering the thoracic appendages differs according to authors and can be found along two different schemes: the first nomenclature, and the one commonly, in fact exclusively, used nowadays, lists gnathopods 1 and 2, and pereiopods 3-7. The second scheme speaks of gnathopods 1 and 2, and pereiopods 1-5: this numeration has been in use among some Anglo-Saxon authors, be it that the most important author among those, J. L. Barnard, has abandoned that scheme and adopted the other one from 1976 onward. Amphipod pereiopods sensu lato exhibit the typical structure of malacostracan appendages, and by far the majority of authors recognizes the classical composition of that leg. The division into segments, mentioning the preferable terminology along with alternative names used earlier (and sometimes even today) runs, from proximal to distal, according to the well-known sequence: coxa (coxopodite), basis (basipodite), ischium (ischiopodite), merus (meropodite), carpus (carpopodite), and dactylus (dactylopodite) (fig. 56.8). Nonetheless, some taxonomists prefer numbering the various articles merely as 1 to 7. The coxa is often flattened in the form of a plate, the coxal plate, which is separated from the border of the tergum (tergite) by a suture. In Caprelloidea and Hyperiidea the coxae are poorly developed and similar to the other segments. In Gammaridea, the coxal plates vary in both shape and size. In some families of the suborder last mentioned, i.e., Amphilochidae, Lysianassidae sensu lato, Stegocephalidae, and Tulearidae, the ante-

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Fig. 56.8. Pereiopod of Maera inaequipes (Maeridae).

rior four are more strongly developed, especially the 3rd and 4th , which thus make a kind of lateral girdle (fig. 56.4). In some Lepechinella and Epimeria these plates take the form of most characteristic, recurved points (fig. 56.9). In the Amphipoda as a whole, the two pairs of gnathopods present a complete series of evolutionary stages between the simple thoracic appendage of which the segments resemble shorter or longer cylinders or cones (Ichnopus, Leptocheirus), and the gnathopods of advanced evolutionary stages of which the articles have been (strongly) transformed and articulate with one another most effectively. The type most widespread is the subchela, in which the dactylus has been transfromed into a nail or claw that refolds on the large propodus that has been transformed into a handpalm, sometimes provided with a gutter- or spoon-shaped hollow and with a spine as a guide — i.e., for making the proper closing movement (Elasmopus, Maera). A true chela is the most rarely encountered (Seba). In some cases, the subcheliform pincer can be composed of the last three articles: carpus, propodus, and dactylus (Ericthonius) (fig. 56.10). Pereiopods other than the first two pairs may also have been transformed into prehensile organs. This concerns the first pair in Ensayara (fig. 56.11), the 5th and 6th pairs in certain Hyperiidea, and even all pereiopods with the exception of the last pair in some species of Phrosina. Pereiopods nos. 3 and 4 are generally long and lean, closely similar

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Fig. 56.9. Coxal plates of species in which these plates have a pointed shape. A, Epimeria cornigera (Epimeriidae); B, Actinacanthus tricarinatus (Epimeriidae); C, Lepechinella manco (Lepechinellidae).

to the typical thoracic appendage. The nos. 5, 6, and 7 most often have an enlarged basis; they may even be extremely long (Melphidippidae, Pardaliscidae). In Corophiidae and Hyperiidea they can be reduced or even completely absent. Mostly, pereiopods bear a gill that is inserted on the basis, i.e., between that segment and the body, and that corresponds to an epipodite (= epipod). Such gills are generally found on the 2nd to 7th pereiopod, but their number is variable and may diminish to three in Phronima and to two in Cyamus. In Corophiidae and Ampeliscidae, pereiopods 3 and 4 can be equipped with complex glandular systems that secrete mucus and that end at the level of the dactyl in a pore, through which they can extrude silk for constructing their tube. The oostegites are generally large and fringed with setae so as to form the brood pouch, but they can also be straight and bear only a few setae, or none at all (Metaingolfiella).

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Fig. 56.10. Different types of gnathopods. A, Leptocheirus pilosus (Corophiidae), gn2 male; B, Maera inaequipes (Maeridae), gn2 female; C, Amphilochus neapolitanus (Amphilochidae), gn2 male; D, Eusirus microps (Eusiridae), gn1 male; E, Leucothoe incisa (Leucothoidae), gn1 male; F, Tmetonyx cicada (Uristidae), gn2 male; G, Seba aloe (Sebidae), gn2 female; H, Ericthonius punctatus (Ischyroceridae), gn2 male.

T HE PLEON The pleon is composed of six body segments, the first three of which comprise the metasome and bear natatory appendages, the pleopods (fig. 56.12). The final three somites make up the urosome and bear styliform appendages, the uropods. Some of the somites of the pleon may have been fused, either in part (Ampeliscidae, Dexaminidae, Hyperiidea), or in whole and as such be reduced to a stub (Caprellidae, Cyamidae). These can also bear a carina. A most peculiar structure has been described from the dorsal portion of the first two somites in Ampelisca remora (cf. Bellan-Santini & Dauvin, 1995)

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Fig. 56.11. Different types of pereiopods. A, Ensayara carpinei (Endevouridae), pereiopod 3; B, Urothoe poseidonis (Urothoidae), pereiopod 5; C, Lepidepecreum longicornis (Lysianassidae), pereiopod 6; D, Lepidepecreum longicornis, pereiopod 7; E, Syrrhoites pusilla (Synopiidae), pereiopod 7.

(fig. 56.13). This structure, in the form of a gutter, resembles a kind of sucker, large on the first somite and continuing as a flat area on the second, that has a weakly granulose surface equipped with setae arising from small openings. The function of this structure is as yet unknown. Finally, the telson has the form of a shield attached to the last urosomal somite; it may be large, entire, and either without indentations, or it may be cleft, and armed with spines and setae, or in contrast be strongly reduced, thus resembling a kind of additional swelling or collar only on its supporting somite. The features of the telson are often used as taxonomic characters (fig. 56.15). The pleopods are normally directed forwards and are composed of a peduncle (sympodite or sympod) that bears two multiarticulate rami that are provided with long setae. The internal borders of the peduncles of a pair bear distal spines that serve in coupling the two appendages and in a similar way the corresponding endopodites (endopods) are linked to

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Fig. 56.12. Pleopods. A, Ampelisca typica (Ampeliscidae), male pleopod; B, Ampelisca sp., hooks present on pleopod peduncle [= sympod]; C, Ampelisca sp. [Courtesy of R. A. Kaïm-Malka and C. Bezac.]

Fig. 56.13. Pleon of Ampelisca remora (Ampeliscidae): A, whole animal in lateral view; B, somites 1 and 2 of the pleon. [Courtesy of D. Bellan-Santini and C. Bezac.]

each other by one or more hooks. These structures obviously enhance the effectivity of the pleopods, whose function essentially is natatory (fig. 56.12). The uropods are rather short and robust; they are situated in a ventro-lateral position. Their structure, much simpler than that of the pleopods, consists of a peduncle and one or two rami that are most often composed of a single, or at most two, segments. Usually, the uropods are armed with rows of spines and can also bear long setae (fig. 56.14). In some species, the male has uropods 3 that are very different from those of the female, i.e., much longer and equipped with many more setae. Also, as the number of pleonal somites becomes reduced through fusion, it follows that one or more pairs of appendages have disappeared in various species or groups.

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Fig. 56.14. Different types of uropods. A, Ampelisca brevicornis (Ampeliscidae), uropod 1 female; B, Chelura terebrans (Cheluridae), uropod 1 male; C, Ileraustroe ilergetes ilergetes (Synopiidae), uropod 1 female; D, Lembos websteri (Aoridae), uropod 2 male-female; E, Ichnopus spinicornis (Uristidae), uropod 2 female; F, Ampelisca provincialis, uropod 3 male; G, Ampithoe ferox (Ampithoidae), uropod 3 male-female; H, Chelura terebrans, uropod 3 female; I, Hyale grimaldii (Hyalidae), uropod 3 male-female.

INTERNAL ANATOMY Integument and colour Amphipoda have an exoskeleton of which the outside can be either smooth, or be ornamented with pores, with tooth-like emergences, or with elevations or depressions in the form of, respectively, knobs or pits. Its surface bears epicuticular structures, like “hairs”, spines, setae, or scales. The integument (see chapter 3 in vol. 1 of the present series: Compère et al., 2004) mediates in all exchanges between the external and internal environment of the animal. The body wall is, over most of its surface, strongly calcified and sometimes coloured; according to species, it may also have a certain degree of opalescence. Many Hyperiidea are totally transparent. The integument is composed of two strata that are unequal in thickness: the epicuticle and the procuticle (fig. 56.16): • the epicuticle is thin and composed of lipo-proteins, without chitin, and not mineralized either;

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Fig. 56.15. Different types of telson. A, Tuldarus barinius (Urohaustoriidae); B, Ochlesis lenticulosus (Ochlesidae); C, Iphimedia eblanae (Iphimediidae); D, Urohaustorius pulcus (Urohaustoriidae); E, Bumeralius bucholicus (Zobrachoidae); F, Rhipidogammarus karamani (Gammaridae).

Fig. 56.16. Comparative scheme of the cuticle in different species of Amphipoda. Hg, Hyperia galba, a nektonic species; Gl, Gammarus locusta, a benthic species; Og, Orchestia gammarella, a benthic species. The thick black line on top represents the epicuticle (ep); the arrowheads represent the limits between, respectively, from outside to inside, the epicuticle and the procuticle (pro), and between the two layers of the procuticle, i.e., between exocuticle and endocuticle. [After Pütz & Buchholz, 1991.]

• the procuticle is thicker, and is distinguished into three layers that comprise an organic matrix of fibrous proteins associated with chitin; from the outside to the inside, these layers are: • the pigmented layer, which is mineralized, and which is composed of compact lamellae; • the principal layer, mineralized as well, composed of lamellae of substantial height that are also rather well delimited individually; • the membranous layer, composed of extremely thin lamellae that are visible only with the aid of the transmission electron microscope (TEM).

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Throughout Malacostraca the integument is not of a uniform ultrastructure. Putz & Buchholz (1991) demonstrated that the intricate structure of the integument is influenced by the species’ ability to swim. The degree of mineralization and sclerotization as well as the thickness of the lamellae can vary. In pelagic species, the integument is only weakly mineralized and its thickness does not increase with the animal’s size. In contrast, in benthic species the integument is much harder and heavily mineralized; its thickness increases with the size of the animal. The various layers of the integument thus give the cuticle a stratified structure, which is traversed by many, diverse canals. The actual structure, formation, and rigidity of the integument as a whole play an important part in the phenomenon of moulting and consequently several biochemical and histochemical modifications take place in the course of the moulting cycle. The cuticular canals show a great diversity in shape, ranging from a simple passage through the cuticle of uniform structure along its length, up to elaborate systems with secondary branches, tubules, and cavities (Halcrow & Powel, 1992). Pores of various sizes have already been described (250 nm in Gammarus, 120 nm in Hyale). In Hyale and Gammarus (Halcrow, 1985) these pores correspond to systems with a tubular part in the procuticle and the epicuticle, while the tubule is strongly and abruptly dilated in the proximity of the surface, whereas in its deeper part an anastomosing network of straight tubules and cavities is found (Hyale) (figs. 56.16, 56.17). This dense complement of canals

Fig. 56.17. Diagram of the tubular system of the pores in Hyale nilssoni; p, pore; c, cavity in the epicuticle; ep, epicuticle; ex, exocuticle (= the external part of the procuticle); t, tubules.

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and cavities would allegedly enable Hyale the production, transport, and diffusion of a secretion, probably of a lipidic nature, which would protect the animal from desiccation. Some authors (for an overview, see Halcrow & Bousfield, 1987) have suggested the canalicules might add to the rigidity of the cuticle by transporting calcium carbonate, while they would also be instrumental in facilitating the passage of various compounds that could protect and lubricate the cuticle; the actual diffusion of pheromones would constitute another functional use. Not all parts of the body are covered with a single, uniform type of cuticle. The integument can, in contrast, be thicker in some areas and bear various modifications, like ridges, spiniform outgrowths, tubercles, or grooves and pits. Such modifications are primarily found (and also most easily interpretable as regards their presumed functions) on the mouthparts as well as on certain surfaces of the gnathopods. Recent studies with the aid of the SEM have shown that those integumental formations can be most complex and intricate, without, however, giving clear clues as to their functionality in the living animal. Zimmer et al. (2009) described seven different types of setae in Hyalella: simple, cuspidate, serrate, serrulate, plumose, pappose, and papposerrate. Each type may further vary as regards its apex, which can be rounded, pointed, or flattened, and in addition can be provided with a pore, or not. The denticles constituting the serrations may be spaced to a greater or lesser extent, thus resulting in variations in their density along those setal types. Among the epicuticular formations (fig. 56.18), microtrichs may be present, whether or not of a sensory nature, and situated on the general surface of the cuticle, or bordering the circumference of pores. The morphology of such microtrichs is very variable, and can include linguiform structures, or can be styliform, or lanceolate, or be shaped as scales or combs. On the cuticular surface also polygons can be observed, delimited by thin and shallow grooves, as well as rows of microtrichs that, according to Graf & Sellem (1970) would correspond to the borders of the epidermal cells underlying such parts of integument. Halcrow & Bousfield (1987) examined the head as well as the coxa of the second gnathopod of 124 species with the scanning electron microscope and they think that the structures they observed will be found among all Peracarida. They suggest that, from an evolutionary point of view, features related to microstructures of the cuticle would correspond with convergent developments that merely reflect the effects of similar environmental conditions. The gnathopods bear microtrichs of very different shapes, some with a sharp point, others shaped as pectinated scales, and always precisely located. It is surmised that such formations play a role when the animal seeks a holdfast on the substrate, or in locomotion, and/or when it is feeding or cleaning the setae of the gnathopods or of the antennae. Another function might be presumed in phases of precopulation, when a male firmly holds on to a female (Holmquist, 1982). The striae found on the asymmetrical maxillipeds in Hyperiopsis voringi have been interpreted as making a stridulation organ, just as formations of the same type situated on the anterior edge of the carpus of the first gnathopod in Grandidierella japonica. Pigmentation in Amphipoda primarily results from carotenoids of exogenous origin, and the actual expression of the pigment is thought to be controlled by various factors,

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Fig. 56.18. Different types of epicuticular formations. A, Echiniphimedia hodgsoni, pore on coxal plate 1; B, Stomacontion pepinii, pores on the head; C, Stomacontion pepinii, combs on the basipodite of pereiopod 7; D, Stomacontion pepinii, different types of microstructures and microtrichs at the end of the pleon; E, Ampelisca remora, microtrich with pore on somite 7 of the mesosome; F, Hippomedon kergueleni, seta on the edge of uropod 1. [Courtesy of D. Bellan-Santini and C. Bezac.]

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some likewise exogenous in nature (conditions involving light intensity), others probably endogenous (hormonal factors). While it was considered that cavernicolous species of the genus Niphargus would not contain carotenoids, Gibert (1977) did measure these in Niphargus virei. That author is of the opinion that, in contrast, the melanic spots that can be observed in some individuals may result primarily from defence reactions against external agents, whether physical attacks or encounters with concentrations of chemical substances, or local disorders caused by (parasitic) micro-organisms. Dickson (1979) noted significant variations in colour depending on the food in the troglobitic Crangonyx antennatus. Some amphipods display brilliant colours: Eurythenes gryllus, Epimeria cornigera, Amphilochus spp., and Peltocoxa spp. Often also homochromy can be observed in species according to their biotope, which means the coloration of the same species may vary depending on the site of collection (Dexamine spinosa, Hyale spp.). On the other hand, amphipods seem to provide only a few examples of polychromatism, although some species do show quite a range of colours (Bocquet, 1974).

Musculature As a result of its morphology, the amphipod body is only capable of movements involving either extension, or flexion. The body musculature thus comprises two antagonistic systems: extensors and flexors (fig. 56.19). The flexor muscles constitute a complex system. The longitudinal flexors insert on the arches of the successive sternites. The lateral flexors make a network of obliquely running bundles that cross each other and insert on the anterior edges of the sclerites of the body segments. The extensor muscles comprise longitudinal bundles inserting on each somite and oblique muscles. This system is developed in extremis in saltatory species, like those of the genus Talitrus. The locomotory appendages are connected to the body by a fan of muscle bundles. The movements of their segments relative to each other are effectuated by two groups of antagonistic muscles, which show particularly strong development in the gnathopods. The mouthparts connect to the trunk by a whole series of muscular bundles of which the insertions are located on the dorsal integument of the head. The digestive tract is enveloped in a strong muscular network, instrumental in moving and ultimately discarding the (remnants of) the food; the parts most muscularized are the stomach and the rectum.

Nervous system The nervous system essentially comprises a supra-oesophageal ganglion mass or “brain”, a ventral ganglion chain and a peripheral system (fig. 56.20). About the sympathetic system hardly any information is available. T HE BRAIN The supra-oesophageal ganglia (fig. 56.21) constitute a brain or cerebrum composed of the usual three parts: protocerebrum, deutocerebrum, and tritocerebrum.

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Fig. 56.19. Muscular system. A, Body musculature in Lysianassa longicornis: the somites are numbered from head to telson; ed, dorsal extensors; fd, caudal flexors; fo, oblique flexors; fv, ventral flexors; mb, muscles of the mouthparts. B-C, Musculature of the pleopods and uropods in Orchestia cavimana. D-F, Musculature of pereiopods 7 and 3, and of gnathopod 2 in Maera grossimana. [A, D-F, After Della Valle, 1893; B-C, after Vogel, 1985.]

The protocerebrum is well-developed: in its median part two centres of association are included, i.e., the protocerebral bridge and the central body, both composed of several glomerular masses and transversally extended. Laterally, the optic lobes contain the centres associated with vision: the medulla externa, medulla interna, and the lamina ganglionaris; in very compact species, the two structures last-mentioned are often

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Fig. 56.20. Nervous system. A, In Vibilia; B, in Cystisoma. Abbreviations: lc, cephalic lobe; lo, optic lobe; na, antennary nerve; ngn1, nerve of gnathopod 1; ngn2, nerve of gnathopod 2; nli, nerve of labium; nls, nerve of labrum; nmd, nerve of mandible; nmx1, nerve of maxilla 1; nmx2, nerve of maxilla 2; nmxp, nerve of the maxillipeds; no, optical nerve; 1-7, somites of the pereion; 1’-3’, somites of the pleon; 1”-3”, somites of the urosome. [A, After Della Valle, 1893; B, after Brusca, 1981.]

superimposed. Between the medulla interna and lamina ganglionaris, there is a chiasma; the links between the medullae do not cross. The optical centres obviously are only little developed in blind forms or in species with reduced eyes. The deutocerebrum is quite distinct from the protocerebrum. It contains three paired associative centres: the lateral lobes, the olfactory lobes, and the antennular neuropils. In its posterior part, the deutocerebrum smoothly passes into the third section of the brain.

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Fig. 56.21. A, Brain of Gammarus pulex; B, cephalic nervous system of Gammarus. Abbreviations: cc, central body; cp, perioesophageal ring (= connectives); lam, lamina ganglionaris; lo, optic lobe; lol, olfactory lobe; me, medulla externa; mi, medulla interna; na1, nerve of antenna 1; na2, nerve of antenna 2; nm, mandibular nerve; nmx1, nerve of maxilla 1; nmx2, nerve of maxilla 2; no, optical nerve; nr, recurrent verve; nt, tegumentary nerve; ppro, protocerebral bridge; tr, tritocerebrum. [A, After Gräber, 1933; B, after Henry, 1948.]

This tritocerebrum primarily holds the antennary neuropils and posteriorly gives rise to the circumoesophageal ring. From this relatively simple brain a small number of nerves depart. The optic lobes of the protocerebrum extend exteriorly to form the optic nerves, according to species, as individual tracts to a greater or lesser degree but mostly rather short, because of the often compressed body of amphipods. From the dorsal part of this section of the brain another pair of, quite thin, nerves arises that traverse the optic ganglia and exit at the site where the lamina ganglionaris covers part of the medulla externa: there the pseudo-frontal organ is situated that also gives its name to this pair of nerves. The pseudo-frontal nerves continue obliquely downwards and backwards to dissolve on the sides of the sub-oesophageal ganglion. Finally, an unpaired nerve with two roots originates from the protocerebrum that innervates the likewise unpaired frontal organ. From the deutocerebrum a single pair of large antennulary nerves arises, while the tritocerebrum sends the tegumentary nerves from its dorsal surface. These nerves innervate two groups of hypodermic cells situated both above and below the eye. To conclude, this third section of the brain releases from its ventral part the pair of very thick antennary nerves, as well as the unpaired nerve that extends to the ventriculus. T HE VENTRAL NERVOUS CHAIN The ventral nervous chain (figs. 56.20, 56.21) is typically composed of 12 pairs of ganglia (that basically include the very short transversal commissures), which are in an antero-posterior sense connected by the longitudinal connectives. The anteriormost pair (sub-oesophageal ganglia) in reality results from the fusion of a series of primitive ganglia that innervate the mouthparts. This pair is followed by seven thoracic pairs, one

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per somite, that innervate the corresponding pereiopods, and next four pairs of abdominal ganglia. This scheme is in accordance with the location of the ventral nervous system in the majority of Gammaridea, but as a result of shortening of some of the connectives, or even their disappearance in certain species or groups, ganglion pairs may approach each other partially, or even fuse. Thus, in Corophiidea, the abdominal ganglia are still distinct in young just after eclosion, but fuse with one another subsequently. In Hyperiidea the condensation of the nervous system reaches its maximum: often no more than three pairs of abdominal ganglia are present while, in addition, the pairs of the thoracic part are only free in the middle of the chain; one or two anterior pairs may fuse with the sub-oesophageal ganglia, while the two posterior ones become fused with each other. Concurrently, the nerves that depart to the mouthparts split off from the branches of the peri-oesophageal ring almost immediately at their origin from that part of the brain. In amphipods, we thus find a significant trend towards cephalization. T HE PERIPHERAL NERVOUS SYSTEM This system is represented in fig. 56.22. It has been studied in particular by Wetzel (1935) in Caprellidea. The peripheral nerves are bipolar cells with a fusiform body that contains a large nucleus. The free ending of these sensory neurons is rather precisely circumscribed and is always situated in the integument. The nerve fibres end either abruptly (Caprella), or as a button (Gammarus). Within the same species, the number of free terminals for a given articulation is nearly constant, but it can vary significantly according to the regions of the body. With respect to motor-innervation, each muscular fibre receives two nervous fibrils that in general arrive at the same site (the Doyère eminence), of which one definitely is a motorneuron, whereas the role of the other fibril is less clear. T HE VISCERAL NERVOUS SYSTEM The innervation of the viscera is shown in fig. 56.22. Alexandrowicz (1954) described a cardiac innervation that is quite complex. At the dorsal surface of the heart a local system forms a glanglionic trunk that send branches to the muscle fibres of this organ. Two pairs of cardiac nerves ensure the connection between this local system and the central nervous concentrations. One connects to the posterior part of the sub-oesophageal ganglia, the other joins the ventral chain between the first and second pair of ganglia of the pereion. Other nerves, probably issued from the sub-oesophageal centre, are sent out to innervate the cardiac valves. Alexandrowicz (1954) supposed that the local system would be responsible for the cardiac rhythm, while the higher nerve centres would play a regulatory role through the mediation of the cardiac nerves. The sub-oesophageal ganglia also send a pair of nerves to the pericard. These nerves on their turn send a longitudinal branch to the aliform muscles and may play a role in regulating the blood pressure. The remainder of their fibres radiates into the wall of the pericard in a plexus that is reminiscent of a secretory neuropil.

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Fig. 56.22. Nervous chain in Marinogammarus and innervation of the heart as well as of the extensor muscles. Abbreviations: ch nerv, nervous chain; gi, infraoesophageal ganglion; m ext, extensor muscle, cut; n ao p, nerve of the posterior aorta; n card 1, cardiac nerve 1; n card 2, cardiac nerve 2; n o p, nerve of the pericardial organs. [After Alexandrowitch, 1954.]

Sense organs T HE EYES There is much variation in the development of the eyes among Amphipoda. Throughout the order, all stages of development can be found, thus ranging from a total absence of eyes up to a truly enormous hypertrophy of the visual system. In most representatives of the group the eyes are sessile. They are paired and occupy part of the lateral sclerites of the head, close to its frontal end. These compound eyes are round, oval, or reniform and are composed of large numbers of ommatidia (Strauss, 1909). Some forms show a division of the eye in several parts, with different orientation. Many Ampeliscidae have a pair of large, supplementary anterior eyes on each side of the head, while some species of this family even have three pairs of eyes, where a small eye, without dioptric apparatus, appears after the other two pairs. In other forms (Oedicerotidae) the eyes are really huge and fuse dorsally into a single organ that occupies the entire anterior part of the head. In some Hyperiidea, the eyes do not essentially differ from the basic type described above, but in certain species the surface of the eyes has become very large,

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Fig. 56.23. Eye of Ampelisca: c, cornea; cv, vitreous body; o, ommatidia. [After Land, 1996.]

resulting in the head being completely covered by those gigantic eyes, which sometimes can even be divided into two secondary pairs, one dorsal and one ventral. Some authors apparently found that the structure of the ventral eyes does not completely correspond to that of the dorsal pair, although the actual differences are minimal and primarily concern an elongation of the dorsal crystalline cones. Some species, e.g., Metaingolfiella mirabilis, bear a pair of so-called “articulated ocular lobes” below the insertion of the first antennae, but in reality the function of those organs is still unclear (Ruffo, 1969). In a general sense, the eyes of the Amphipoda can be distinguished from those of the remaining malacostracans through the absence of corneal lenses on the ommatidia. The cuticle of a gammaridean, for instance, is just smooth while covering the eye. Nonetheless, there are exceptions to this rule: in all members of the family Ampeliscidae, as referred to above, the total field of ommatidia is covered by one enormous corneal lens (fig. 56.23). Some Hippomedon also have lenses. In Melphidippella macra, finally, an eye structure has been observed that is identical to what is found in other higher crustaceans, viz., every ommatidium possesses its own cuticular lens. Amphipod eyes are of the apposition type, in which the rhabdom is in contact with the crystalline cone; the rays of light that go through the cone only reach the corresponding sensory element. Even when the eye and its retinal pigments are in the “darkness mode”, the rays can not pass from one ommatidium to another, since the whole space between those components is occupied by cells full of a reflecting white pigment (Interommatidial Reflecting Pigment cells; Hallberg & Elofsson, 1989). Also, detailed observations have demonstrated that the retinal pigment does not completely disappear at the level of the rhabdoms. These amphipod eyes consequently never function as true superposition eyes — at least in species that have until now been studied with sufficient precision (Gammarus, Echinogammarus, Orchestia). In this context, it may be relevant to note that Carinogammarus roeselii is the species in which the moving of ocular pigments was first discovered in the eyes of crustaceans. Reduction, or even complete disappearance of the eyes has been established in many species of Amphipoda representing all larger groups. Consequently, a whole series of increasing reductions can be composed: a decrease in the numbers of ommatidia, absence of the crystalline cone, followed by disappearance of the sensory apparatus, and finally atrophication of the optic ganglion as well as of the optic nerve. Studying these stages

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has been used in attempts at phylogenetically linking a number of forms with each other. The genus Niphargus, comprising inhabitants of subterranean waters, has been extensively examined in this respect. Thurston & Bett (1993) have statistically studied the disappearance of the eyes in marine amphipods as a function of their geographical and bathymetric distribution. They conclude that loss of the eyes affects approx. 50% of the families; colonization of the large oceanic basins as well as the adaptation to the confinement of subterranean biotopes would appear to constitute two major causes leading to the disappearance of the eyes. Hence, from a phylogenetic point of view the absence of eyes in Amphipoda should be considered an advanced character state, more specifically, a true apomorphy. As regards giving a truthful image of the surroundings of an animal, the eyes found in amphipods should not be considered as necessarily providing this. Their vision permits them, at least in certain cases, to follow the movement of displacing objects at some distance, and Williamson (1951b) demonstrated that the visual sense of Talitridae was instrumental when the animals were returning to the sea. However, normally developed amphipod eyes can be capable of detecting the polarization of light. Also, in Caprellidae (Caprella dentata), Wetzel (1933) succeeded to establish a certain degree of colour vision through observing the differential extension of chromatophores in animals illuminated with monochromatic light. A review of the work done on the phenomena of vision, adaptation to ambient light conditions, sensitivity to polarization, as well as damage to photoreceptors in crustaceans was compiled by Meyer-Rochow (2001), but the data concerning amphipods included are only sparse. Blind Niphargus in caves would still detect light and would show a negative phototaxis, permitting them to choose for the darkness of the cave, their protective environment (Borowsky, 2011). Frelon-Raimond et al. (2002) described vestigial photoreceptors in Talitrus saltator, specifically in the medio-dorsal part of the brain, that could determine the ambient light conditions through the locally very thin cuticle. Our knowledge concerning the effect of light on amphipod behaviour is more extensive, in particular with regard to littoral species (see section Ethology, below). O RGANS OF BALANCE Various organs have been described that would allegedly constitute statocysts, at least according to some authors (Langebugh, 1928; Thore, 1932): the paired frontal organ, the X-organ, and the organ of Bellonci. These organs comprise vesicles that contain a statolith, which, in this case, is not to be considered an inanimate object, as protoplasmic extensions of the epithelial cells of the vesicle penetrate into such a statolith. Neuronal fibres connected to sensory cells distributed within the vesicular epithelium depart from there and together form a nerve that runs to the protocerebrum. The cavity of the organ communicates with the environment by a canal in Ampelisca and Gammarus locusta, whereas the vesicle is completely closed in Gammarus pulex. However, the actual role of the organs mentioned in maintaining equilibrium has not yet been established satisfactorily, as the results of ablation experiments proved hard to interpret and may

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even be considered doubtful. The indications we have with respect to the activity of these statocysts can at most be considered indirect proof of their involvement in maintaining balance. Elofsson et al. (1980) studied the organ of Bellonci and concluded that it definitely has a sensory function, but in addition a secretory component as well. M ECHANORECEPTORS AND CHEMORECEPTORS Setae as well as cuticular hairs, often well developed on the antennae (especially in males), the mouthparts, and the legs, would ensure the perception of tactile and chemical stimuli by the amphipod (see also the chapter “The non-visual sensory organs” in vol. 1 of the present series: Hallberg & Chaigneau, 2004). We discuss four types of such receptors herein: a. Sensory microtrichs. – These have been described from many Amphipoda (Gammarus roeselii, Gammarus setosus, Ampelisca remora) (fig. 56.24). Such hairs are mainly found on the head and on the dorsal surfaces of the body, though their actual distribution varies with the species. They consist of a tiny seta of less than 25 μm in length, inserted in the centre of a cuticular depression. Oshel et al. (1988) distinguished two types, based on the shape of the cuticular orifice: • A bowl-shaped depression with a vaulted protrusion at one side (type 1); • a simple, circular depression delimited by one or more circular ridges of cuticle (type 2). Type 1 is divided into three subtypes according to the morphology of the seta: • seta with a terminal pore and lateral scales; • seta with additional filaments; • seta short and plumose.

Fig. 56.24. Schematic representation of a microtrich sensillum with its sensory unit. Abbreviations: c1-c4, cells of the cavity of the microtrich; end, endocuticle; ep, epicuticle; exo, exocuticle; s, seta; ur, sensory unit. [After Steele & Oshel, 1987.]

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Fig. 56.25. Callynophore in Scopelocheirus hopei: A, antenna 1 male with callynophore; B, close up of the same callynophore. [Courtesy of R. A. Kaïm-Malka and C. Bezac.]

Type 2 includes a short seta of 5-6 μm with a bifid tip. Ultrastructural investigations of those formations have shown that they comprise the typical anatomy of chemosensory setae, without any characteristic structure that might indicate mechanosensitivity (Steele & Oshel, 1987). b. The callynophore. – This sensory organ (fig. 56.25) was described in detail by Lowry (1986); it is located at the proximal end of the principal flagellum of the antennules. The organ bears transversal rows of aesthetascs that together often form a brush. A callynophore can be present in both sexes of the same species. In Gammaridea, species that are provided with the organ are found in various superfamilies; it occurs, as far as known, in all Hyperiidea. The probable functions of the organ have been described as follows: • it serves as a general chemoreceptor; as such: • in the reproductive period, it would serve, in the male, to detect the pheromones released by the female; • it would, in both sexes, serve in locating food; • it would be instrumental in planktonic, parasitic species to find their hosts. c. Calceoli. – Descriptions of calceoli can be found in Hurley (1980) and Lincoln & Hurley (1981) (see fig. 56.26). These are complex structures present on the antennae of approx. 10% of Gammaridea. Their size ranges from 20 to 300 μm. Various basic structures have been recognized, which are more or less characteristic for certain families. Lincoln & Hurley (1981) distinguished nine types of calceoli, of which the common structure comprises, from distal to proximal: • a distal element that bears either concentric ridges, or annular formations; • a more proximal element shaped as a part of a disc, or shaped as a complete, parabolic disc, that bears the distal element;

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Fig. 56.26. Calceoli in Scopelocheirus hopei: A, on antenna 1; B, on antenna 2. [Courtesy of R. A. Kaïm-Malka and C. Bezac.]

• a dilated basal element that supports the other two elements; • a thin stalk. The occurrence of calceoli can be limited to the males (Haustoriidae, Phoxocephalidae, Lysianassidae) or extend over both sexes (Gammaridae, Eusiridae); they can be present on only one or on both pairs of antennae and either be restricted to the peduncle, or be dispersed over the whole appendage. Various roles have been attributed to calceoli, among which those of mechanoreceptors and chemoreceptors for pheromones (Dahl et al., 1970). Without excluding these possibilities, Lincoln & Hurley (1981), who studied these organs with the SEM, were struck by the resemblance of these structures with receivers of radio waves; accordingly, they think calceoli could be wave receptors as well as receptors of pressure. d. The spatheform organ. – From a variety of species, various authors have described an organ composed of series of microtrichs on the dorsal and lateral surfaces of all somites (Platvoet, 1985; Notenboom, 1986; Oshel et al., 1988). They essentially compared it with a lateral line system of fish and proposed functions as either chemoreceptive, or as a pressure detector, or possibly an organ of balance. Kaïm-Malka (2010) subsequently made a detailed study of the organ in 18 species of Amphipoda distributed over 12 families, while also involving four species of isopods. He described the elementary structures, which he called unispathes, while naming the organ as a whole the spatheform organ (fig. 56.27). A meticulous study with the aid of the SEM enabled him to observe the presence of these structures on all metameres, with the exception of those of the head. Accordingly, he was able to give a description of the typology and distribution of these structures in the species studied as well as to establish the presence, in their proximity, of knobbed, i.e., bulbous setae, of which the knob represents

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Fig. 56.27. The spatheform organ. A, Unispathe in Tmetonyx similis; the pore, in the depression, is surrounded by many concentric, circular ridges (arrow); note the length of the shaft and the apical part with its opening, the edge of the open end here splayed, more or less shaped as a pair of diverging lips. B, An arrangement of unispathes in Dexamine spinosa, pereion segment 2 (Pe2), the Laterodorsal metameric spatheform Line (LdmsL); 1, example of spatheform organ as a row of (here seven) unispathes; 2, unispathe l; 3, the surrounding surface with its granular appearance. C, Schematic drawing of the structure of a unispathe in the integument of Scopelocheirus hopei; 1, epicuticle; 2, pigmentary layer; 3, main layer; 4, the pore, here with one concentric ridge; 5, wall of the canal; 6, the splayed apical part; 7, the internal vesicle; 8, nerve innervating the unispathe; 9, peripherical subcuticular nerve; 10, cuticular unispathe canal. D, Unispathe of Euonyx biscayensis, on Us2 (urosomal somite 2): cross section through a knob (2), on which the seta (microtrich) (1) can be seen, partly extending from a sheath; in the pigmentary layer (6), the statocyst (3-5) is present, composed of an external envelope (3, dark), an internal envelope (4, light), and a central nucleus, the statolith (5). [Courtesy of R. A. Kaïm-Malka and C. Bezac.]

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a statocyst. With the TEM, he could demonstrate the unispathes to be constituted of a vesicle situated below the body surface, as well as their innervation from a peripheral, subcuticular nerve. The statocysts revealed being composed of a dark, i.e., electron dense nucleus representing the statolith, and an envelope surrounding that core that appeared as less dense, hence more clear when observed. The hypothesis regarding the function of the organ, taking also into account the results of examining the ethological and ecological characteristics of the species studied, seems to be in favour of a use in maintaining equilibrium as well as providing the possibility of varying ballast in vertical displacements, whether descending or ascending, hence adapting, or distinguishing, the individual vis-à-vis the actual mass of the ambient water. The size of the organ varies according to the body size of the species and also to the sex of the individual.

Circulatory system The circulatory system (fig. 56.28) can be understood most easily by considering the amphipod body as being divided into two cavities, a dorsal and a ventral one, by means of a continuous membrane, equipped with elastic fibres as well as muscles, i.e., the aliform muscles, attached to the outer walls of the thorax and the abdomen. This membrane, the pericardial septum, sends an extension into each appendage, thoracic as well as abdominal. As a result, the appendages contain two separate ducts, a superior or external one, and an inferior or internal one. However, through the rotation of the planes of flexion of the thoracic legs, the ducts thus formed have ceased to be primarily external or internal but instead have become rather anterior and posterior in orientation. Inside the appendages the septum separating the two ducts is perforated with holes that allow communication between the two cavities; in addition, the septum does not reach until the end of the appendage. These openings as well as the terminal lacunae constitute, together

Fig. 56.28. Circulatory system of Gammarus pungens with: aa, anterior aorta, dividing into three branches: bs, a superior branch; ms, an intermediate branch; and, bi, an inferior branch; ap, posterior aorta; c, heart; ap, posterior sinus; sv, ventral sinus; o, ostiole. [After Della Valle, 1893.]

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with the blood vessels and the cephalic lacunae, the only possible routes of communication for the blood between those dorsal and ventral cavities in the body of the amphipod. T HE HEART In the middle of the pericardial cavity, suspended from a number of sites on the tergites, a long, swollen tube is found that constitutes the heart. The heart extends, depending on the species, from the second, third, or fourth thoracic somite up to the sixth or seventh. The tube as such is connected by its lower midline to the pericardial septum and its wall contains external longitudinal muscle fibres. The wall of the heart is provided with ostioles that can vary in number (three pairs in Gammarus pulex, a single pair in Corophium) that serve communication between the pericardial cavity and the internal space of the heart. T HE AORTAE AND THE LACUNARY SYSTEM In order to guide the circulation of the blood, a number of vessels departs from the heart. The anterior aorta serves the head, first as a sagittal ring around the cerebral, sub-oesophageal ganglia, next a transversal ring around the oesophagus, prior to open up into the cephalic lacunae. In Phronima (Haffner, 1935), the rings seem to be absent and the anterior aorta simply ramifies at the level of the various ganglia, including the sub-oesophageal ones. In Gammarus, the base of the anterior aorta immediately gives off two lateral arteries that irrigate the masticatory muscles and the mouthparts; in Niphargus virei there are even four such arteries. The posterior aorta originates from the caudal end of the heart and runs to the telson. Towards the end of its track, this vessel dives under the septum and opens up freely in the ventral lacunae. However, this is not the case in Phronima, where the posterior aorta simply opens into a terminal dorsal sinus. At any rate, the posterior aorta does not extend further than the fourth somite of the pleon. Finally, it should be noted that the two aortae do not connect directly with the anterior and posterior ends of the heart, but instead cover these as a sleeve and the blood passes from the heart into the vessels through two slit-shaped cardiac valves. In addition to these aortae, either two (Hyperiidea), or three (Gammaridea) pairs of arteries have been established that originate from the inferior face of the heart near its midline: the stomacal or hepatic arteries. These arteries ramify around the digestive organs or discharge into a peristomacal sinus. The remainder of the circulatory system is lacunary and consists of sinuses, in particular in the head. A large ventral sinus in which the digestive tube as well as the ventral nervous chain are immersed, sends afferent lacunae to the appendages. The blood leaves the appendages via efferent sinuses that guide it to the pericardial sinus, from where it returns to the heart through the ostioles. So, what we have here is an incompletely closed, or rather open circulatory system. This means the blood is not forced to pass through the gills at every cycle and as a result the heart always contains a mixture of oxygenated blood and blood that has already given off its oxygen to the tissues.

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Studies reporting on the coincidence of the ratios of heart beats and the beating of the pleopods are not very clear. Dubuisson (1928) had observed that their frequency would be equal and also rather high (285-360 beats per minute). In his concept, the cardiac systole, the only driving force behind the circulation, sees its action amplified by the synchronous dilation of the ventral sinus, which dilation itself would result from the movements of the pleopods. These considerations have been discussed by Schwartzkopff (1955), who did not believe the dilation of the ventral sinus could be effectuated by pleopod beating. After all, Dubuisson worked under experimental conditions that made it difficult to precisely observe movements at this speed. Schwartzkopff’s (1955) own studies on the cardiac rhythm and the respiratory rhythmicity in many Crustacea did not reveal any synchronicity in Gammarus pulex. That author thus thinks it is probable that the same would apply in other Gammaridea. He also experimentally studied the effect of temperature on the heartbeat frequency of gammarids and found these factors varied in the same sense, i.e., in concordance. Yet, discrete differences are observed if the amphipods have earlier been adapted to cold (5°C) or warmth (20°C). In the latter case, raising the temperature triggers a relatively higher increase in the frequency of cardiac contractions. The heart rate is also dependent on the weight of the animal, large individuals having a less rapid pulsation than small specimens. T HE BLOOD The blood or haemolymph of amphipods is a colourless fluid that, according to Goulliart (1952) would all the same contain haemoglobin (found in Urothoe grimaldii). The fluid, or plasma, contains corpuscular elements shaped either as lenses, or as spindles. In Gammarus pulex, Austreg (1952) isolated three types of globules: • leucoblasts; • leucocytes with basophilic cytoplasm, i.e., basophilic leucocytes; • leucocytes with eosinophilic granules, or eosinophilic granular leucocytes. Gibert (1972) recognized two primary types of globules in Niphargus virei: • hyaline leucocytes; • granulocytes; as well as all types intermediate between these two. These globules, or blood corpuscles, originate from organs with an aspect of lymph glands, the haematopoietic organs that Bruntz (1907) discovered in the head near the insertion of the antennae and that Gibert (1972) retrieved in Niphargus virei. The blood corpucles are mobile; they are capable of phagocytosis, instrumental in removing undesired objects from the blood, and also play a role in excretion, as they can concentrate certain dissolved compounds. However, the tasks last-mentioned, i.e., phagocytosis and excretion, are also fulfilled in part by cells that are fixed in the walls of the heart and in those of the larger arteries.

Respiratory system The respiratory function, i.e., gaseous exchange, takes place over all parts of the body where the cuticle is thin, though notably in the gills. In most cases the gills are formed as

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coxal epipodites of the pereiopods. They may be shaped as lacunary sacs, either simple or ramified, mostly flattened, and are either covered by smooth integument, or the body wall may locally form ridges and folds in order to increase the respiratory surface. The maximum number of gills found in Amphipoda is six pairs, in which case each of the thoracic appendages bears a gill, with the exception of gnathopod 1. This condition is the most primitive and occurs in many gammarideans. In more advanced states, the gills on one or more pairs of pereiopods may be absent, so as to yield species with five, four, or even three pairs of gills only. In Caprellidea, three pairs is a number only rarely reached, i.e., when the second gnathopod and the two successive pereiopods bear gills. The gnathopodial gill is often lacking, in which case the two pereiopodal ones constitute the only vestiges of the thoracic appendages that have otherwise disappeared in this group. The last thoracic leg never bears a gill in Hyperiidea, and consequently the number of respiratory appendages does not exceed five pairs in this taxon; the number is often lower. The sternal gills that are found in Crangonyctidae as well as in species of Hyalella are simple, median structures generally extending over somites 2-5 or 2-7 of the pereion. Next to serving in gas exchange, the gills also are the sites where ion transfer takes place, i.e., osmoregulation. This phenomenon has been studied in supralittoral and terrestrial Talitridae (Tsubokura et al., 1998). According to these authors, the epithelium of the gills, beneath the cuticle, would be composed of two layers, i.e., an external, thin apical layer, termed Apical Infolding System (AIS), as well as an internal layer, the Basal Infolding System (BIS), well developed, rich in mitochondria, and with profuse interdigitation. In Eurythenes gryllus, a species occurring at greater depths, the epithelium is reduced and contains less mitochondria (Matsumasa et al., 1998). Yet, in amphipods the respiratory function is not always restricted to the gills. As mentioned above, all body parts with a thin integument, as well as the flattened segments of various appendages (coxal plates, some bases, oostegites, maybe also the uropods) equally well play a role in oxygenating the blood. There the haemolymph circulates through capillary lacunae comprised between the two layers of the integumental epithelium, exactly as in the gills. Graf & Magniez (1969) demonstrated with the aid of silver salts that the permeability is high in certain non-calcified areas of the cuticle (regions on gnathopods 1 and 2 that are provided with epicuticular structures) and low in calcified areas. In this respect it may be noted that in males of Cyamus the presence of “accessory gills” has been described, that, however, in reality would be vestigial oostegites. The constant irrigation of the gills is ensured through the beating of the pleopods, and the current resulting from those movements is channelled by the coxal plates. The rhythm of pleopod beating depends on various factors, being variable according to species, and being accelerated under the influence of raised temperatures as well as raised carbon dioxide levels in the ambient environment.

Digestive system For a long time, the digestive tube of the Amphipoda was considered a relatively simple structure, but it is now known to be complex, both as regards its morphology, and in view of its functions.

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Fig. 56.29. Digestive apparatus in: A, Orchestia gammarella; B, Niphargus virei. Abbreviations: b, mouth; cai, unpaired caecum (= pyloric caecum); ch, hepatic caeca; cp, posterior caeca; e, stomach; im, middle intestine; oe, oesophagus; r, rectum. [After Graf, 1969.]

In its most comprehensive composition, the digestive tract comprises nine distinct regions: (1) the mouth, (2) the oesophagus, (3) the stomach, (4) the pyloric caecum [also: coecum], (5) the hepatic caeca, (6) the middle intestine or mesenteron (also anterior intestine according to some authors), (7) the posterior caeca, (8) the posterior intestine, and (9) the rectum (figs. 56.29, 56.30, 56.31). Although there is some confusion among authors with regard to the correspondence of the various parts in different species, a general scheme can all the same be drawn up as follows: 1. Directly following the mouth, which is a simple opening surrounded by mouthparts of which the triturative function can be very important, the oesophagus begins.

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Fig. 56.30. Anatomy of the digestive tract: A-B, in Marinogammarus obtusatus; C, in Bathyporeia sarsi. Abbreviations: cc, central lumen; cd, dorsal lumen; cda, anterior dorsal caecum; cdg, dorsal digestive caecum; cdv, ventral digestive caecum; cf, filter chamber; cpd, dorsal pyloric chamber; f, filter; i, intestine; o, oesophagus; rpv, ventral pyloric ridge; vp, pyloric valve; vv, ventral valve. [A-B, After Martin, 1964; C, after Kanneworff & Nicolaisen, 1969.]

Fig. 56.31. Morphology of the posterior caeca in various types of amphipods. A, Melita; B, Corophiidae; C, Maera; D, Gammarus and Dexamine; E, Cyrtophium; F, Hyale; G, Orchestia, rectum. [After Graf, 1969.]

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2. The oesophagus is located entirely in the head; its position is perpendicular to the longitudinal axis of the body in its first half, after which it bends in an obtuse angle vis-à-vis that first part. The wall of the oesophagus is composed of four longitudinal “strands” connected by thin, chitinous membranes. According to Kanneworff & Nicolaisen (1969), each of these strands consists of a band of chitin folded to form a gutter, the lumen of which is filled with a mass of cells that are arranged in a row. The posterior strand forms a ridge at the entrance of the stomach, the lateral strands constitute shutters that, together with the valve formed by the superior [= anterior] strand, allow to close the stomach. The musculature of the oesophagus is circular and five pairs of dilator muscles are inserted either at the level of the flexure, or between that site and the (entrance to the) stomach. 3. The stomach (proventriculus) is situated behind the eyes and its anterior end is located at approx. one-third of the distance between the eyes and the posterior border of the head; it continues through the first and second somite of the pereion. The stomach comprises, from its connection with the oesophagus, a ventriculus with on its lateral sides a pair of hemispheres that protrude into the stomacal lumen and that are equipped with a row of strong denticles that are curved backwards. This ventriculus, fixed through ligaments to the exoskeleton of the posterior part of the head, is provided with powerful muscles. Martin (1964, 1966) described the structure and functioning of the stomach in detail for Marinogammarus obtusatus, as did Kanneworff & Nicolaisen (1969) for Bathyporeia sarsi (fig. 56.30). The stomach essentially comprises a large sac, divided into various parts, the largest ones of which are the pars cardiaca (or cardiac stomach) and pars pylorica (pyloric stomach). The structures dividing the total consist of septa and rows of setae, and these are instrumental in keeping apart the nutritional matter, as both solid and liquid components, that circulates in and between those compartments in complex patterns. Oshel et al. (1988) have studied the variation in those structures for various species, according to the types of food they nourished themselves with. A considerable number of muscles is present in order to ensure the proper movements of the diffferent parts of the stomach. The food circulates in the oesophagus by virtue of peristaltic contractions that are synchronous with the movements of the ventriculus. In this ventricle, which does not seem to have a truly triturative function but is more equipped for exerting pressure (Kanneworff & Nicolaisen, 1969), the lateral parts make circular movements that push the solid fraction of the food mass from the central part of the stomach towards the intestine. In addition, there is a pumping system that moves the liquid fraction mixed with digestive juices and forces it through two filter systems as well as through the solid fraction. This rather quick circulation of the liquid fraction, under pressure, seems to ensure an adequate draining of the solid mass that is contained in the central lumen. The type of stomach as here described seems to be widespread among Gammaridea, with only slight variations primarily in regard of the shape of the internal septa and the density of the setae at the various locations at issue.

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5.

6.

7.

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Siewing (1963) realized a reconstruction of the various folds and wrinkles both at the cardiac and the pyloric level in two species of Ingolfiellidae. In the anterodorsal part of the stomach the pyloric caecum is found, simple in Gammaridea, double in Caprellidea. This structure may also be reduced, or even absent. The hepatic caeca resemble two long sacs that open laterally in the posterior part of the stomach. Graf & Michaut (1975) demonstrated that, contrarily to what was supposed earlier, these caeca never protrude into the lumen of the posterior aorta but are adjoining that vessel. The hepatic caeca are much dilated as a result of containing large quantities of fluid. The epithelium is composed of secretory cells and cells for stocking nutrients. An active pumping system driven by powerful peristaltic contractions moves the digestive fluid from one caecum to the other in a rhythm that can reach 12 cycles/min in Bathyporeia sarsi. The hepatopancreatic fluid contains large droplets of oil. The middle intestine (= anterior intestine according to some authors) departs from the stomach. This part of the digestive tract approximately runs along the anterior half of the body, i.e., to the sixth metasomal somite in Orchestia gammarella. It is a thin tube, from inside to outside composed of an epithelium comprising cells with a ciliated border that rest directly on a basement membrane; this structure is enclosed in a muscular layer that is not very thick, while that total is covered in the peritoneal membrane, made up of a simple squamous epithelium. The posterior intestine is located in the last mesosomal somite as well as in the metasome and it is evidently much more complex than the middle intestine. The epithelial lining contains three longitudinal folds, two dorsal and one ventral. In transverse section, the following six layers can be distinguished from inside to outside (Graf, 1969): • a cuticular layer ornamented with epicuticular spines; • an epithelium composed of prismatic cells; • a rigid basement membrane; • longitudinal muscle fibres; • circular muscle fibres; and • the peritoneal membrane. At the junction between the middle and posterior intestine two dorsally situated tubes join the digestive tube: the posterior caeca that are, however, absent in Caprellidea. In Orchestia gammarella, the posterior caeca first run anteriorly and next bend backwards. This spatially doubling of the tubes earlier evoked the idea that four caeca, i.e., two pairs, would be present in the Amphipoda. The length and precise shape of these structures varies according to species (fig. 56.31). The posterior caeca are essentially of an endodermal origin; they comprise: • an epithelium identical to that of the middle intestine; • an in all probability elastic basement membrane; • a muscular layer and peritoneal membrane of much reduced thickness.

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These posterior coeca are generally considered homologous with the Malpighian tubules of insects. Their role in the excretion of calcium has been established (Graf, 1969). The precipitate in the form of calcium carbonate can only be found in the proximal section, while the calcium solution that precipitates there has been secreted by the distal section. These calcium formations, in the form of spheroliths or rhombohedral crystals that are formed during the pre-exuvial stage, constitute a stock of calcium that will immediately be used after the moulting event in order to strengthen the new exoskeleton. This phenomenon of securing a stock of calcium before the moult is in concordance with the lifestyle of the animal and the possibilities that it will be able to rapidly find the calcium necessary for mineralizing its integument in the external environment. In Gammarus, however, these formations are rare and are more likely meant for actual excretion. 9. The rectum is entirely comprised in the urosome; it differs from the posterior intestine by the fact that its external wall is well developed. The anterior one-third is equipped with four to six pairs of sarcoplasmic tubules. Schmitz & Scherrey (1983) studied the various types of epithelial cells in the different parts of the digestive tract of Hyalella azteca and were able to correlate these with the functions those epithelia fulfil in digestion. A histochemical study on Gammarus pulex (cf. Mabillot, 1955) has shown that the absorbing sections are restricted to the anterior part of the stomach and the hepatic caeca. These parts also exhibit and intense activity of alkaline phosphatase. The same was already found by Husson (1953) for the anterior mesenteron in Niphargus. In addition, in stages C and, even more, D of the moulting cycle, the oesophagus as well as the posterior part of the ventricle also show alkaline phosphatase activity. In that phase ribonucleic acids are abundant in those secretory regions and carbohydrates occur exclusively in the form of glycogen. Investigations of Agrawal (1964a) and Halcrow (1971) also indicated a cellulase activity in the digestive caeca in Orchestia gammarella and Gammarus oceanicus. Some morphological and functional modifications can be observed in various species as a result of their mode of life. The parasitic lifestyle of Cyamus has led to profound adaptations in its digestive tube; its stomach is not divided into the usual cardiac and pyloric chambers. The hyperiidean Parathemisto gaudichaudi has, according to Sheader & Evans (1975), a far more simple digestive tract than most amphipods, i.e., with a large digestive compartment, likely resulting from the fusion of oesophagus, stomach, and middle intestine. This species would also have only one pair of digestive glands. The authors think that in fact all Hyperiidea that feed on medusae, ctenophores, and pelagic tunicates (all soft preys of large size), will have developed a single large digestive chamber at the expense of the other parts of the digestive tube (Sheader & Evans, 1975). Agrawal (1964b) studied the correlations between the digestive tract and the lifestyle of nine amphipods. It appears that both the shape of the mouthparts and that of the digestive tube are directly connected with the quality of the food. Macrophagous forms (Orchestia, Talitrus) have strong mouthparts and their stomach is provided

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Fig. 56.32. Diagram showing adaptations for stocking food: A, in the stomach of Orchomene; B, in the intestine in Paralicella, Eurythenes, and Hirondellea. Abbreviations: ch, hepatic caeca; est, stomach; i, intestine. [After Dahl, 1979.]

with sturdy ridges for the trituration of nutritive matter, whereas microphages (Bathyporeia, Haustorius) rather have filtering mouthparts and a stomach with a much smoother wall. The author (Agrawal, 1964b) considered that the size of the food would constitute one of the primary factors determining the shape of the mouthparts as well as the organization of the digestive tract in Amphipoda. Dahl (1979) has made clear that in the carnivorous Lysianassidae two types of stocking nutritive matter can be found, i.e., either in the stomach (Orchomene), or in the middle intestine (Paralicella, Eurythenes, Hirondellea) (fig. 56.32). In Chelura terebrans, a species living on and in wood, the hepatic caeca would be the sites of secretion of a lignocellulolytic enzyme (Green et al., 2010).

Excretory system In the basal part of the antennae the antennary gland is situated (fig. 56.33), which has since long been recognized as an excretory organ. The first part of this gland consists of a reservoir, the sacculus, which communicates with the labyrinth through a pore that is equipped with a valve. This labyrinth in fact is a long tube, curled up as a ball. That tube becomes swollen to form a bladder just before opening up to the exterior, most often with the external pore at the top of a blunt cone situated on the second segment of the antennal peduncle. This type of excretory gland is found, with slight modifications, in all amphipods examined so far. Histochemical studies (Husson, 1951) have established an intense phosphatase activity at the level of the sacculus, of which

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Fig. 56.33. Antennary gland in Corophium curvispinum: A, position of the antennary gland (ga) in the basal segment of antenna 2; B, morphology of the gland. Further abbreviations: c, coelomosac; ce, excretory canal; s, sphincter; te, efferent tubule. [After Taylor & Harris, 1986.]

the athrocytotic properties2 ) were already known. Taylor & Harris (1986) have studied the osmoregulatory function of the organ, which would show a significant capacity of reabsorbing Na+ . Masses of athrocytes have also been observed at various sites in the body of amphipods, mostly at the sites of insertion of the appendages of pereion and pleon, i.e., coxal athrocytes (Della Valle, 1893; Bruntz, 1904). In some species, this also occurs in the mouthparts as well as, in Niphargus, in the carpi of the gnathopods (Husson, 1951). All those athrocytes seem to be referable to distinguishable types. Under the name of nephrocytes, Bruntz (1907) described pericardial cells having both athrocytotic and phagocytotic properties. That author also reported the presence of phagocytes around the digestive tube, that together constitute the phagocytotic organ. Graf (1971) described in certain Niphargus spp. cells concentrating ureum salts that are located near the pericardial septum and that would extend along the vessels up to the basipodites of the pereiopods. As these ureum cells appeared totally different from the cells referred to above, Graf supposed these to be homologous with the Zenker’s organs of isopods, or with the ureum cells of insects. The presence and quantity of ureum cells would depend on the environmental conditions as well as on the food. These cells could constitute sites for stocking urates, pigments, and/or various ions. The posterior caeca of the digestive tube are excretory organs, too. Graf (1969) demonstrated the importance of these caeca as well as their role in the storage of calcium and in its subsequent release into the circulation in species in which the external environment has a deficit in calcium. In species that can obtain the necessary calcium from their habitat in order to mineralize their exoskeleton after the moult, those same storage cells effectuate the excretion of surplus calcium. Finally, the hepatic caeca appear to play a role in the excretion of certain compounds that can be dialysed, and blood cells that have a possibility to concentrate dissolved substances from the haemolymph also seem to have some role in excretion.

2 ) Athrocytotic, athrocytosis, athrocytes = cells concentrating [alien, superfluous, or waste]

substances within their cellular body in a granular form.

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Various other glands and organs E NDOCRINE AND NEUROCRINE GLANDS The studies of Stahl (1938) showed that in the vicinity of the optic lobes a glandular organ occurs in Gammarus locusta that joins a blood sinus: this is the sinus gland, homologous with those present in the majority of Malacostraca, but smaller in size. The gland is innervated by a neuropil that, running through both the medulla interna and externa, is issued from the protocerebrum. In Talorchestia martensi and Orchestia platensis, Shyamasundari (1973) described six types of neurosecretory cells distributed throughout the brain, the peri-oesophageal ring, and the ventral nervous chain. The presence of a Y-organ (Gabe, 1953) has been established in eight species of Gammaridea. This endocrine gland that controls the moulting cycle is present in all malacostracans and definitely comprises the equivalent of the ecdysial glands (= prothoracic glands) of insects. V ENOM GLANDS In Hyperiidea as well as in various Caprellidea, certain tegumentary glands have sometimes been considered to constitute poison glands. In particular where glandular formations are found that discharge at the apices of spines on the gnathopods, or even on the epimera. S ILK GLANDS Some species classified under the suborder Corophiidea, e.g., in the family Aetiopedesidae as well as some species of the gammaridean family Ampeliscidae, construct tubes. For this purpose they possess glandular systems in pereiopods nos. 3 and 4, that are capable of secreting a mucous substance that solidifies as a kind of silken thread and that can trap and aggregate particles from the environment. Shillaker & Moore (1978) were the first to describe these structures as well as the concurrent behaviour in Corophiidea. Kronenberger et al. (2013) recently made a more detailed study of this phenomenon. These silk glands occur in both sexes and they contain endoplasmic reticulum with vesicles in which the mucous compound is stored. This mucus is a complex polysaccharid emitted through a pore at the tip of the dactyl, which also bears striations and a seta, probably to shape and guide the resulting fibre. L UMINOUS ORGANS The only luminous organs described in amphipods are those from a hyperiidean of the genus Streetsia (cf. Fage, 1934). They consist of small, cup-like structures with pigmented walls that contain large cells with a glandular appearance. The membrane closing off the organ has a polygonal structure. These photophores, directed backwards with regard to the body, occur in three pairs, two situated between the coxa and basis of pereiopods 6 and 7, the third on the coxa of the last appendage.

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In this context, it should also be noted that the alleged photogenic properties of the modified eyes in Scypholanceola must be qualified as most doubtful. On the other hand, luminescent cells, or photocytes have been observed in various species. The size of such cells is usually in the order of 15-25 μm, with 40 μm as a maximum and their cytoplasm is either granulose, or contains many vacuoles. The position of such cells is variable according to the species at issue, and they can thus occur on the antennae, the pereiopods no. 5, and the uropods in Scinidae; at the basis of pereiopods 7 in Parapronoe; at the level of pereiopods 3, 4, and 6 as well as at the basis of the uropods and at various sites on the uropods and telson in Cyphocaris, Thoriella, and Danaella. The actual emission of light, i.e., the triggering of the luminescence, can be elicited by a (mechanical) shock, as well as by an electrical or chemical stimulus. The response is very fast and may be repetitive, while the intensity of the light produced has been measured and was established as 16 · 10−6 mW.cm−2 at a distance of 1 metre (Herring, 1981). Many Talitroidea (Talitrus, Orchestia, Hyale) also show a bioluminescent phenomenon, usually over the whole body, but in these cases the source is an infection with a luminous bacterium.

Genital apparatus T HE GENITAL APPARATUS OF THE MALE The male genital apparatus comprises two tubes, symmetrical relative to the animal’s sagittal plane, and situated above the digestive tract. The testes themselves extend from the 2nd to the 3rd body segment in Orchestia gammarella (cf. Berreur-Bonnenfant, 1971) and from the 5th onto the 6th somite in Niphargus virei (cf. Reygrobellet, 1977). They are joined through an adipose-mesenchymous tissue. The posterior part of the organ, i.e., in the 4th , 5th , and 6th thoracic somites in Orchestia gammarella and in the 5th , 6th , and 7th in Niphargus virei constitutes the seminal vesicle in which the spermatozoids accumulate; this vesicle has a larger diameter than the tubular testis. A spermiduct or vas deferens departs from there in backward direction, then bends towards the outer regions of the body to follow the lateral body walls and ends on a genital apophysis or penis that protrudes between the 7th pereiopods. Before the curve made by the spermiduct to bend around the muscles of the seventh coxopodite, the androgenic gland joins the tube (fig. 56.34). In Orchestia gammarella, the activity of the testes is cyclical and five phases have been described. This cyclical pattern is independent of the moulting cycle and continues throughout the year, with only a lower intensity during winter. T HE GENITAL APPARATUS OF THE FEMALE The overall structure of the ovary is comparable to that of the testes. The germinative zone, similar in the two sexes, merely contains a much lower number of 1st stage germ cells than that of the male. Vitellogenesis is a phenomenon that occurs in synchrony with the moulting cycle. The oviducts open on the fifth segment of the mesosome, into the marsupium. This brood pouch is formed by oval plates (oostegites) fringed with setae,

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Fig. 56.34. Male genital apparatus. Abbreviations: ag, genital apophysis; cd, deferent duct; ga, androgenic gland; t, testis; vs, seminal vesicle; zg, germinative zone, with the arrow indicating the direction of spermatogenesis. [After Berreur-Bonnenfant, 1971.]

that are attached to the internal face of the coxal plates. Gammaridea and Hyperiidea generally have four pairs of oostegites (2nd to 5th somite) but many exceptions exist to this rule: some Lysianassoidea have six pairs (large Eurythenes; cf. Stoddart & Lowry, 2004), but in some Oxycephalidae these structures are either much reduced, or even absent (Rhabdosoma); Caprellidea have two pairs only. The size of the oostegites increases with each moult and the setae appear upon the parturition moult.

Chromosome complement The composition of the chromosome complement of amphipods has been investigated primarily in the Gammaridea and in Niphargus, and appears to show considerable variation. Niiyama (1959) was the first to attempt summarizing the knowledge in this field, which was in part redone by Reygrobellet (1974) and later by Rampin (2008). The values of 2n vary from 8 in Aora gracilis to >100 in Hyperia galba (cf. Rampin, 2008). Salemaa (1985) found in species of Gammarus from Lake Ohrid quite variable numbers of chromosomes, ranging from n = 12 in Gammarus salemaai to n = 34 in Gammarus lychnidensis, whereas among the gammarids collected in the Baltic (Salemaa, 1986), i.e., Gammarus oceanicus, Gammarus locusta, Gammarus salinus, Gammarus zaddachi, and Gammarus duebeni, those numbers appear to vary between n = 26 and n = 27, and thus are most homogeneous. Some genera seem to have a truly homogeneous caryology, like Niphargus in which 2n = 50 throughout (Reygrobellet, 1974). Laval & Lécher (1975) found 2n = 30 for two species of Phronima, Phronima sedentaria and Phronima atlantica, as well as a remarkable homogeneity in the sizes of the chromosomes themselves. Also, quite some cases of supernumerary chromosomes have been observed: Laval & Lécher (1975) specifically observed these in male lines in Phronima, distinctly more often than in female lines. Those same authors, finally, report several cases of segmentation of unfertilized ova that resulted in polyploidy, though never at a level higher than octoploidy. However, it seems that after reaching that stage, those oocytes degenerated. Salemaa (1984) studied

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a type of polyploidy in Pontoporeia and suggested that would be related to the evolution of the genus. He considered the ancestral forms would have been diploid (like Pontoporeia femorata with n = 14), while the evolved forms would be polyploids (as Pontoporeia affinis with n = 26), which forms then would have constituted generalists and thereby could become invading pioneer species. In 1994, Coleman made a comprehensive overview of all caryological results on Amphipoda available so far, and added many unpublished data from his own studies. He concluded that: • in amphipods the number of chromosomes is most variable; • the number of chromosomes can not serve, at least at the current state of knowledge then, for basing taxonomic, nor phylogenetic, conclusions on. Rampion (2008) confirmed the great variability in chromosome numbers in certain families (Aoridae, Ischyroceridae, etc.) whereas in other families numbers are much more uniform (Niphargidae, Caprellidae, etc.). Attempts at sequencing a complete genome in Amphipoda have been made, but only very few have succeeded as of today. The complete sequence of the mitochondrial genome has been obtained (Ki et al., 2010) but it appears as yet to merely raise many questions as regards this kind of data known from other crustaceans.

Molecular genetic markers Many recent studies in ecology as well as in systematics use one or more so-called “molecular markers”: sequences of DNA or RNA derived from molecular genetics. Populations within a single species, or various different species (and then also higher taxa) can be compared with regard to the similarity or dissimilarity in certain genes. Genes frequently used to make sequences of nucleotides for such comparisons are the mitochondrial genes, COI and 16SmtDNA and the nuclear genes for the ribosomes, 18SrDNA and 28SrDNA. Using the mitochondrial DNA, various authors have either demonstrated the existence of a significant genetic differentiation between populations as, e.g., in Paracalliope fluviatilis (cf. Hogg et al., 2006); or analysed the phylogeny of a genus as in Gammarus (Hou et al., 2007); or pointed out the lack of coherence between a molecular phylogeny and the classical morphological classification as in the Antarctic Lysianassoidea (Havermans et al., 2010). With the aid of these techniques it also appeared possible to reconstruct, in a biogeographical sense, the various stages of colonization as in Hyalella azteca (cf. Witt et al., 2008); or the adaptive evolution in a species complex like Gammarus duebeni (cf. Krebes et al., 2010); as well as the phylogenetic history of the Gammaroidea in Lake Baikal (MacDonald et al., 2005). In 2009, Costa et al. recommended the use of “DNA barcoding” to extend our knowledge of the genus Gammarus, specifically in order to retrieve cryptic species, to facilitate identification of its various forms, and to establish their phylogeography at the generic level. Though indeed most commendable, actually using barcoding in amphipods will require many extensive studies and is, hence, not within immediate reach yet.

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REPRODUCTION AND DEVELOPMENT Reproduction In this specific chapter on Amphipoda, we shall not reiterate the general hormonal and physiological phenomena or reproduction that have already been treated extensively in vol. 1 and 2 of the present series (see Charmantier-Daures & Vernet, 2004; CharmantierDaures & Charmantier, 2006; Legrand & Juchault, 2006). Thus, as we have seen, the Amphipoda are equipped with a rather simple genital apparatus, they are considered to generally be gonochoristic, and then usually exhibit a sexual dimorphism that, in certain species, can be much accentuated. S ECONDARY SEXUAL CHARACTERS The most important secondary sexual characters affect six features of the body: 1. Size of the individual. – Adult males and females may be very different in body size. In Phronima sedentaria the female is 3-4 times as large as the male (Laval, 1975). 2. Antennae. – The length and armature of the flagella differ in the two sexes. In Lysianassidae, males have very long A2, whereas these are short in females. In Ampeliscidae the lengths of the male and female antennae are also strikingly different. The armature of the antennae consisting of setae, calceoli, and callynophores is also quite distinct, as the males often have these structures on either one, or both pairs of antennae, whereas they are usually lacking in the females; this is found in Haustoriidae, Phoxocephalidae, and Lysianassidae. In some cases (Eusiridae) both sexes may bear calceoli (Hurley, 1980). 3. Size of the eyes. – In the males the eyes are often larger than in the females, as, e.g., in the Urothoidae. The male of Ampelisca brevicornis has a pair of accessory lenses, behind the first pair. 4. Shape and pilosity of gnathopods and pereiopods. – The shape and size of the gnathopods are in many species the most obvious characters of use in distinguishing the sexes. Males generally have large gnathopods, most often especially gnathopod 2. Sometimes the shape makes an excellent taxonomic character, as in the genus Hyale. Various authors have already reported that the gnathopods are important instruments for the male to hold the female in precopula, whence the functionality of this difference is evident. Also, the male often has claws on the pereiopods. Arimoto (1976) described a new genus of caprellids (Heterocaprella) in which the male has an elongate ventral protrusion on pereionite 4, on the apex of which the fourth pereiopods are inserted as well as the branchial lamellae. 5. Shape and ornamentation of the uropods. – In the male, the uropods may in some places be fringed with long, plumose setae or with modified spines, as in the genera Bogidiella, Lysianassa, and Ampelisca.

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6. Presence of organs directly linked to reproduction. – Females in the reproductive phase bear oostegites or brood plates that together make a brood pouch or marsupium, viz., by overlapping each other as well as by the interlocking of the setae that fringe them. Inside this brood chamber the eggs are carried during their development prior to eclosion, and next the young during their first moults. There generally are four pairs in Gammaridea and Hyperiidea, but exceptionally either five pairs or none at all, while in Caprellidea always two pairs are present. Males may bear copulatory papillae or even penes in the proximity of the gonopores on the 7th somite of the pereion. Some authors also consider the sternal processes as secondary sexual characters. P RECOPULA AND COPULATION In most cases an either shorter, or longer precopula (or mate guarding) precedes the actual copulation in amphipods, which itself is always of short duration. The female is fertilized without intromission. The mechanisms evoking the realization of the precopula as well as the actual fertilization are chemical in nature. The compounds involved are emitted by the female, of which the ovaries contain ripe oocytes. According to Borowsky & Borowsky (1987) the most important stimulus to elicit reproductive behaviour of the male would originate from the exoskeleton of the female, suggesting the existence of contact pheromones. Conlan (1991) distinguished two main categories of precopula: 1. Active precopula in which the female is seized either from dorsal or from lateral and then is carried along by the male for some time, whether walking or swimming. 2. The male keeping guard close to the female, without contact, until the moment of copulation. In this case, the author distinguishes between males that move into the water column and those that stay on the bottom. According to their specific lifestyle, the various families have developed appropriate strategies of precopula (fig. 56.35). The most widespread scenario involves that the male places itself above the female and grasps her with his gnathopods. Then they swim together for some, quite variable, time. Goedmakers (1981a, b) estimated the duration of mate guarding to last for six days in Gammarus at 15°C. The actual period of precopula varies with temperature and salinity (Hartnoll & Smith, 1978), the intensity of predation (Strong, 1973), the number of competitors and the number of available females (Ward, 1983) as well as, of course, the stretch of time the male succeeds in effectively holding the female. In terrestrial species (Talitridae), the female can not be carried. Williamson (1951c) mentions for semiterrestrial amphipods like Orchestia gammarella a very quick copulation, varying from 10 s to 1 min, which is repeated four or five times. Moore (1981a) described a possible variant of the relative position of male and female in the precopulatory and copulatory modus in Epimeria cornigera (fig. 56.35). This species has no robust, prehensile gnathopods but does have a sturdy, keeled body skeleton as well

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Fig. 56.35. Precopulation positions in: A, Hyalella azteca; B, Caprella danilevskii; and copulation position in, C, Epimeria cornigera. [A, After Borowsky, 1987; B, after Aoki, 1996; C, after Moore, 1981.]

as coxal plates 1-4 that together make a large furrow, transversal with regard to its body axis. With these lateral extensions the male keeps the female perpendicular to himself, caught in the cleft formed by the coxal plates 4-5 and, by bending its pleosome forward, can thus reach the genital pores of the female. His pereiopods 5 and 6 would facilitate the actual act of copulation, while pereiopods 7, through their large basipodite, would prevent spilling of the sperm. The sperm is deposited on the female’s ventral body surface; the female next sheds her eggs and these are fertilized in the brood pouch. Fertilization occurs shortly after the moult, while the cuticle is still sufficiently flexible to allow the eggs to pass through the gonopores without any obstruction. Williamson (1951c) suggested that, in terrestrial amphipods, the spermatozoids would be activated by a secretion originating from the non-fertilized eggs, or else from the female during shedding. In Talitrus saltator, the spermatozoids can live for at least four days in the marsupium, probably as a result of their inactivity and their size. Hence, in this species the following sequence could be established: (1) female moult; (2) a 4-day period in which a very short copulation, with or without ‘carrying’ of the female would allow the male to deposit his sperm in the brood pouch of the female; (3) shedding and fertilization of the eggs.

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F ECUNDITY The size of the brood is variable: it ranges from 1 egg in Bogidiella (Ruffo, 1973) to 500 eggs in Gammaracanthus loricatus (cf. Steele & Steele, 1976). Nelson (1980), who studied data of 65 species from 14 genera, considered there would be a correlation between brood size and the size of the reproductive females. He also thought the broods of brackishwater species would be significantly larger than those of fully marine species, and that the smallest broods would occur in species inhabiting fresh waters. Within the same species, the number of eggs produced depends on the size of the female, though this can not always be decribed as a linear function (Van Dolah & Bird, 1980) (fig. 56.36). Also the ambient temperature affects brood size in a species, as demonstrated by Kinne (1959), who found that above 18°C the numbers of eggs in Gammarus duebeni strongly decrease. The specific ecology of a species would also be of influence, as Van Dolah & Bird (1980) have shown that, with only few exceptions, species living in the epifauna produce larger litters than those occurring in the endofauna (fig. 56.36). The actual dimensions of the individual eggs would also be strongly influenced by the geographical latitude and the season. Larger eggs are found in populations at higher latitudes as well as in the cold season (Van Dolah & Bird, 1980). Nelson (1980) demonstrated that the average size of the eggs is significantly larger in reproductive cycles involving a single brood (univoltine) than in those in which multiple broods are produced

Fig. 56.36. Comparison of the numbers of eggs per brood in amphipods: a, of the epifauna; and, b, of the endofauna; both as a function of the body size of the female (in mm). [After Van Dolah & Berd, 1980.]

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(multivoltine). According to Van Dolah & Bird (1980) the eggs are larger in endofaunal forms than in species that are part of the epifauna, as stated above. The number of broods is rather variable, again depending on temperature, latitude, and various ecological as well as ethological factors. Many specific reports on this aspect of reproduction have been published on certain target species in different regions of the world. The total of the above issues, i.e., size and frequency of broods, the duration of egg development, and growth and longevity of the adults, together constitute the life cycle of an animal. In view of the many species of Amphipoda, various strategies with regard to life cycles have been established and we shall treat those further below. E GG DEVELOPMENT In amphipods there usually is no larval phase of development, because development is direct. The eggs normally develop in the brood pouch of the female. Generally, development is synchronous for all eggs of the same brood, and its duration varies according to the species as well as to the ambient environmental conditions. This duration may range from a few days to several months; Morino (1978) reported that the period from shedding the eggs until release of the young varied from two weeks in spring, to 7-11 days in high summer, to 20 days in autumn for the species Orchestia platensis in Sirahama (Japan). Klein et al. (1975) indicate one month for Ampelisca brevicornis on Helgoland, while Mills (1967) mentions 15 days for the congeneric Ampelisca abdita in the northwestern Atlantic. Ginet (1960) gives an account of 3 months at 9°C for Niphargus virei. Kanneworff (1965) reported 5 months for Ampelisca macrocephala in the Øresund. Most polar species would show an egg development varying between 4.5 and 6 months (Arndt & Beuchel, 2006). Laval (1975) estimated that the development of the eggs in the pelagic species Phronima sedentaria would last approximately 15 days at temperatures between 15 and 18°C. The only general rule that could be derived from the studies thus made, would be that the larger eggs of species from higher latitudes show slower development and that, for the same species, development seems to be faster at higher temperatures. Alwes et al. (2011) have started to investigate the first stages of cleavage in the egg of Parhyale hawaiensis and the subsequent pathways of cellular lineages from the moment of gastrulation, aiming at disclosing the molecular mechanism that regulates the process of development. Dahl (1946) noted five stages of development in the eggs of terrestrial amphipods, which have been confirmed and described by Fish (1975) for Bathyporeia pilosa (fig. 56.37): • Stage 1 (duration 3 days). The eggs still form one mass; each eggs divides several times. • Stage 2 (2 days). First appearance on the ventral surface of the primary flexure of the body. • Stage 3 (5 days). The Anlagen of the appendages appear. • Stage 4 (2 days). The vitellus is dorsally reduced; the caeca have become evident. The first eye Anlage may be visible at this stage.

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Fig. 56.37. The five stages of development in Bathyporeia pilosa; c, heart; d, dorsal organ; fc, caudal flexure; g, germinal disc. [After Fish, 1975.]

• Stage 5 (8 days). The heart starts beating: 15 strokes/min at first; the frequency rises and attains 200 strokes/min prior to eclosion. The juvenile is ready for eclosion. Magniette & Ginsburger-Vogel (1982) produced a very precise chronological table of the development of Orchestia gammarella at 10, 17, and 25°C; at these temperatures, total duration was established to take 44, 19, and 12 days, respectively. In Haploops vallifera, the females have no oostegites and the eggs are shed and develop inside the tubes in which the females live (Dauvin, 1996). Laval (1980) and Dittrich (1987) described a slightly different type of development in some parasitic Hyperiidea. Upon leaving the egg, the animal has not attained its specific shape yet, but is still a larva that needs two or three stages (termed pantochelis and protopleon), separated by moults, to attain its juvenile stage. Stages 1 and 2 are completed inside the maternal marsupium, and the final stage in the barrel-shaped tunicate (a salp) in which they live. In these larvae, various appendages are still present as Anlagen only (fig. 56.38). E CLOSION Eclosion takes place in the brood pouch of the female. In stage 5 of embryonic development, the animal’s body is actively contracting and these contractions are capable of rupturing the egg membrane. Where the body is bent, the antennae and the head are the first parts to emerge from the membrane. While the embryo ruptures the egg membrane, the telson and uropods are still covered by the embryonic cuticle that does not bear setae.

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Fig. 56.38. Larvae of the hyperiidean Vibilia armata: A, pantochelis stage; B-D, protopleon stages 1-3, respectively; E, first juvenile stage. [After Laval, 1980.]

Specific eclosion spines have been observed in Gammaridae. According to Fish & Mills (1979) such spines are absent in the genus Corophium; however, the cuticle of the liberated animal does bear spines (2-4) that may have served the same purpose at the moment of eclosion, but that persist throughout its life. As the antennae emerge from the egg, they bear setae, which might indicate that the embryonic cuticle has already been torn in the anterior part of the body. The juvenile next frees itself from the egg membrane as well as from (the remnants of) the embryonic cuticle through vigorous movements. These juveniles are at most a few millimetres long and will stay inside the brood chamber for 1-3 intermoult stages before actually being released into the environment. In Parathemisto, the juvenile ecloses at 0.8-0.95 mm and is released at the 3rd moult. At this stage, the animal’s growth rate is very high: about 40%. In Corophium volutator, the juvenile stays 5 days in the mother’s marsupium after eclosion (Muus, 1967). Birklund (1977) measured young of 845 μm in the brood pouch of Corophium insidiosum. In certain species at least, the release of juveniles is bound to have a cyclic character, since broods can be manifold over the year. Mills (1967) considered that in Ampelisca abdita in which the development of the eggs covers 15 days, a release of young would take place at all full moons, so with cycles of 28-29 days. Various authors (Berezina, 2005; Yu & Suhl, 2006; Delgado et al., 2009) considered that within one species the size of the broods as well as the volume of the embryos is positively correlated with the size of the female.

Growth As in arthropods in general, growth in amphipods is accomplished through successive moults. The physiological processes as well as the actual mechanisms behind these

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periodic moulting events are under the influence of complex hormonal systems (see chapters 5 and 12 in vols. 1 and 2 of the present series: respectively, Charmantier-Daures & Vernet, 2004; Charmantier-Daures & Charmantier, 2006). M OULTING Sheader (1981) has most commendably described the moulting of the pelagic species Parathemisto gaudichaudi. First of all he remarks that, as in another pelagic species, Parathemisto gracilis as well as in the benthic Gammarus chevreuxi, exuviations take place at night with a preference of some 80%. Two or three hours before the actual moult, the animal does no longer feed, its activity diminishes, and a decrease in pigmentation can be noted as a result of the contraction of the chromatophores (this may be an advantage, rendering the animal less visible for predators during the time it is particularly vulnerable). The first crack occurs between the head and the pereion, next extends laterally up to the first pereional somite, and subsequently along both sides on to the junction pereion-pleon. The head is the first part of the body to free itself, followed by the mouthparts, the antennae, and, finally, the pereiopods in their antero-posterior order. Then the pleon and the urosome are gradually extracted from the posterior exoskeleton, together with pereiopods no. 7. The whole process of exuviation lasts from 15 min up to one hour. During this period, the gnathopods, the mouthparts, and the masticatory ridges of the stomach are continually moving. The author (Sheader, 1981) noted two types of contractions of the body. The first type comprises local contractions of musculature, which allow the separation of the old from the new integument; contractions of the second type are quick movements that involve the body as a whole and serve to release the animal from its old exoskeleton. The growth in size of the animal can not be seen directly after the moult, but occurs gradually, reaching its maximum approximately two hours after the exuvium has been discarded. Boero & Carli (1979), who observed the behaviour of Jassa falcata, remarked that moulting took 45 min in that species. With the exception of those rare cases in which the young upon eclosion is not morphologically identical to the adult and does only become so after a limited number of moults (three in Phronima sedentaria, cf. Laval, 1975; four in Hyperoche mediterranea, cf. Hoogenboom & Hennen, 1985), three further types of moults are distinguished. At first, there are juvenile moults, in which the animal merely grows significantly in size; next are the puberty moults, in which it acquires certain secondary sexual characteristics; and finally there is the maturation moult, in which the animal becomes sexually mature: now it is no longer a juvenile, but has become an adult. This maturation moult, or maturity moult is, in the case of a female, always followed by a process of reproduction: fertilization, shedding of the eggs, incubation, and eclosion of the young. Some species show, by the end of their reproductive period, a moult in which the females have lost the setae on their oostegites; there are good reasons to consider this comprises, at least in certain cases, a process of senescence that precedes the death of the individual. In the course of these moulting processes, the animal does not just increase in size, but it has been established that some appendages (especially antennae and pleopods) can acquire

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additional segments as far as growth proceeds. This phenomenon has been extensively studied, because it was thought that this aspect of growth would be instrumental in establishing, with certainty, the age of animals collected in the environment. However, this method of calculating age has proven to be too little precise, since the acquisition of articles on appendages is not constant over time; it slows down when the animal gets older. In Parathemisto gaudichaudi (cf. Sheader, 1981), the first three moults concur with the acquisition of one segment on each ramus of a pleopod: up to a body length of 8 mm most moults are accompanied by the addition of one segment to each ramus; above that size, one segment is usually added to one of the rami, whether the inner or the outer ramus. When the length of the body grows to more than 15 mm, there no longer is a regular addition of ramal segments, other than occasionally, and so, generally, the numbers of segments remain unchanged. Maruzzo & Minelli (2011) followed the growth of the pleopods in Gammarus roeselii. These appear to grow by the addition of one article on the exopodite and two on the endopodite, originating from a proximal site of growth. In both rami, the new setae and the new article are produced by splitting of the first article, counted from proximal. Charniaux-Cotton (1957) established that in Orchestia gammarella the number of segments of the flagellum of antenna II increases with one unit at each moult by the division of the proximal article. In Orchestia platensis, the juveniles would, according to Morino (1978), acquire one article on the antenna II at each moult, whereas the adults would get one additional article every two moults. Page (1979) reported that in Orchestia traskiana males and females would acquire one article on the antenna II at every moult, up to a total of 13 articles; above that number, a difference between the sexes in the frequency of acquiring a new article would become evident, linked to the respective growth rate of either sex at each moult. Caprella laeviuscula, which has two articles on the flagella of antenna II at birth, gains an article per moult, and hence reaches a total of 12 articles at the 10th ecdysis (Caine, 1979). Louis (1977) presented a table in which, on the one hand, the acquisition of articles on the flagella of antennae II is recorded as a function of growth, while, on the other hand, the differences between four species of Orchestia occurring in the same region are stated (table I). The number of moults is very variable, both between species and within a single species, as functions of the sex of the individual and of the ambient environmental conditions. The total number of moults is estimated at 22-23 in Orchestia gammarella. The number of puberty moults depends on the size of the juvenile upon eclosion, on the size of the adult at the beginning of maturity, as well as on the specific growth rate. The number of maturity moults is linked to the life cycle of the species, i.e., to the possible number of broods for a female as well as to the possible number of fertilizations for a male. The intermoult period is the time elapsing between two successive moults. Its duration is most variable. Yet, this is dependent on only two factors, viz., temperature and the age of the animal. In some species, the winter intermoult period can take several months, just as the incubation of the brood or the period of reproductive arrest, while

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TABLE I Theoretical correspondence between the successive moults, the stage of the individual, and the phase of development, in four co-occurring species of Orchestia, O. plat = Orchestia platensis; O. med = Orchestia mediterranea; O. mont = Orchestia montagui; O. gamm = Orchestia gammarella; nb. art = number of articles in the flagellum of the A2; Juv = juvenile; Inter = Intermediairy [after Louis, 1977] Moult

1 2 3 4 5 6 7 8 9 10 11 12 13

Stage

1st stage 2nd stage 3rd stage 4th stage 5th stage 6th stage 7th stage 8th stage 9th stage 10th stage 11th stage 12th stage 13th stage 14th stage

O. plat

O. med

O. mont

O. gamm

nb. art

Phase

nb. art

Phase

nb. art

Phase

nb. art

Phase

3 4 5 6 7 8 9 10 11 12 13

Juv I Juv I Juv I Juv II Juv II Juv II Inter Inter Adult Adult Adult Adult Adult Adult

3 4 5 6 7 8 9 10 11 12 13 14 15 16

Juv I Juv I Juv I Juv II Juv II Juv II Juv II Inter Inter Inter Inter

4 5 6 7 8 9 10 11 12 13 14 15 16

Juv I Juv I Juv I Juv II Juv II Juv II Juv II Inter Inter Inter

5 6 7 8 9 10 11 12 13 14 15 16

Juv I Juv I Juv I Juv II Juv II Juv II Inter Inter Inter Adult Adult Adult

the intermoult periods in spring can be in the order of a few days only. In Parathemisto gaudichaudi (cf. Sheader, 1981), the intermoult lasts for 60 days at 4°C, versus 10 days at 16°C; it thus decreases with a rise in temperature. With regard to the animal’s age, Ginet (1960) recorded in Niphargus virei, a species with a great longevity (14 years), two moults a year in the young adult, later on only one. Variations in salinity do not seem to influence the duration of the intermoult period (Kinne, 1961). Also other factors seem to affect the number of moults, hence the number and duration of intermoult periods, i.e., the availability of food as well as, possibly, the photoperiod. G ROWTH RATE AND LONGEVITY As already mentioned, growth rate in amphipods varies strongly between species, and for the same species it strongly varies in the course of life. The currently known data on the growth of Amphipoda have been obtained through two methods: rearing in the laboratory, and measuring in the environment. Though taking into account variations according to species as well as the ambient environmental conditions, both methods can only approach the actual conditions to an average level, whence the results risk to be rather imprecise. In fact, the influence of all deviations in conditions depends on the species as such. This recognition will apply even more prominently when the problem of the life cycles is to be tackled. Nonetheless, from the

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TABLE II Growth in Gammarus zaddachi [derived from Kinne, 1961] Age in days after eclosion

Increase in size in mm

10

20

30

40

50

60

80

100

2.74

1.88

1.22

0.92

0.47

0.46

0.53

0.55

available works some conclusions can be reached, albeit that these will appear rather heterogeneous. Sheader (1981) considered that, in the pelagic species Parathemisto gaudichaudi (= Themisto gaudichaudii), the growth rate of a juvenile amounts to about 40% per moult, and successively dwindles as a function of its increase in size. Watts et al. (2011) studied this species in Cumberland Bay (South Georgia) between May 2005 and October 2006 and measured on the primary cohort (that of September-October) an increase of 0.1 mm/day in the first four months and subsequently of 0.07 mm/day for the four succeeding months. With this growth rate, the authors thus estimate that the main cohort would reach its size of maturity at the time of production of the second cohort (January). Kinne (1961) studied growth in Gammarus zaddachi at 19-20°C and a salinity of 10 psu [practical salinity units]. From his results, the data shown in table II can be derived. Greeze (1972) gives values that can be quite simply interpreted for several benthic species from the Black Sea, expressed in relative growth of their body length (%) (table III). Although their results can only be preliminary and are also expressed in heterogeneous ways, these authors clearly demonstrate that growth rate (1) decreases with the ageing of the animal; and (2) stabilizes in accordance with Kinne (1961); as well as (3) amounts to only a few percent at an adult age, according to Greeze (1972). Longevity definitely varies according to species: Niphargus virei can reach an age of 14 years in captivity (Ginet, 1960), while Ampelisca brevicornis may live for 5-6 months at Marseille (Kaïm-Malka, 1970). The maximum age attained also varies for the same species according to the latitude at which it occurs, since Ampelisca brevicornis can reach 18-23 months at Roscoff (Dauvin, 1979) and 12 months at Helgoland. Longevity also TABLE III Relative growth as a function of time in several species of Amphipoda [after Greeze, 1972] Months

Gammarus insensibilis Gammarus olivii (= Echinogammarus olivii) Ampithoe vaillanti (= Ampithoe ramondi) Dexamine spinosa Pleonexes gammaroides (= Ampithoe gammaroides)

1

2

3

4

5

206 71 300 140 160

42 66 65 37 53

48 32 22 48 23

13

9

20 14

6 2

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varies with sex: females of Ampelisca macrocephala can live for 2-3 years, while males of that species reach 1.5 years as a maximum (Kanneworff, 1965); in contrast, for Gammarus wilkitzkii an age of 6 years was recorded for males and 5-6 years for females (Beuchel & Lonne, 2002). Maturity and longevity both are, in a general sense, more extended for species that live in extreme environments, like polar regions or very deep troughs (Arndt & Beuchel, 2006).

Life cycle and reproductive periods A massive literature has accumulated on the life cycle of different species of amphipods from all over the world. T HE VARIOUS CYCLES AND PERIODS OF REPRODUCTION Several types of reproductive cycles can be distinguished: a. Biannual or pluriannual cycle. – The maturation of the female can require several years and she will produce only a single brood during her lifetime. b. Univoltine cycle. – See fig. 56.39: there is a single generation per year class. The individuals do not reproduce until they have passed a winter period in sexual arrest. After the period of reproduction, two categories of individuals are present:

Fig. 56.39. Life cycles in Ampelisca: A, univoltine cycle; B, bivoltine cycle. Abbreviations: c1, first cohort; cn, intermediate cohort; cn+m, last recruted cohort; c’1, first cohort of the second generation; c’n+m, last cohort of the second generation; cl f, offspring class; cl m, parental class; semi-circles represent ovigerous females. [After Bellan-Santini & Dauvin, 1988.]

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(1) The survivors of the parental class (that may still pass another winter); and (2) the class of the offspring. The generation of the running year may contain several cohorts, corresponding with the successive broods of the maternal class. c. Bivoltine cycle. – There are two generations per year class. In favour of a rapid development, the young-of-the-year that were born early enough can reproduce already during the same annual reproduction period as their mothers. By the end of the reproductive season three categories of individuals are collected: (1) The survivors of the parental class. (2) The annual offspring class, comprising: (a) individuals of the first generation of offpring of which some have already reproduced themselves, while others have not (so these represent various cohorts); (b) the individuals of the second offspring generation. The total of the offspring class will constitute the parental class of the following year. In the genus Ampelisca, two types of cycles can be observed: (I) The univoltine type: Ampelisca brevicornis at Arcachon (Salvat, 1967) and at Roscoff (Dauvin, 1979). (II) The bivoltine type: Ampelisca tenuicornis at Roscoff (Dauvin, 1979), and Ampelisca vadorum as well as Ampelisca abdita along the northeastern coast of the United States (Mills, 1967). d. Multivoltine cycle. – There are several generations per class. Steele (1973) indicated for Parhyalella pietschmanni that, as a result of a very high growth rate at Nosy-Bé, a generation would last 4-5 weeks and that, by consequence, 12 generations per year would be possible, because there is no interruption in the course of the year in that tropical climate. On Corsica, De Casabianca (1975) counted 5-6.5 generations a year in Corophium insidiosum and 4 in Corophium volutator. The reproductive period is most variable, both as to the time of the year it takes place, as well as with respect to its duration: (1) The reproductive period may be limited to some months in the most favourable part of the year: sping and summer, or summer and autumn. (2) The reproductive period may last year-round, without any interruption. (3) The reproductive period may involve two favourable periods: shedding eggs in autumn, development of the embryos during the whole adverse season, and releasing the young the next spring. T HE VARIOUS STRATEGIES INVOLVING LIFE CYCLES Studies approaching the strategies of life cycles as a distinct aspect of amphipod biology, have somewhat exploded during the last years. As an overall impression, they have shown that such strategies can not be linked to groups of taxa, but instead to individual

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species, and then essentially to temperature, food availability, as well as to the autoecology of each species. The life cycle of a species corresponds to a strategy that it has adopted to ensure its survival in its ambient conditions. In that strategy the following factors are involved: 1. 2. 3. 4. 5. 6.

The ultimate body size attained by the adult. The time required for its full growth. The size of the brood: number and size of the eggs. The number of broods. The time required for the development of the eggs. The longevity of the species.

In the oceanic environment at high latitudes, in this case on the Southern Hemisphere, a large species, Bovallia gigantea with an adult female of about 45 mm (Thurston, 1968), needs a long time to grow with very long intermoult periods, and will thus attain maturity only extremely late: 28-29 months for the male, probably from the 9th moult onward, and 40-41 months for the female. A female of this species will only produce one brood during her lifetime, but the eggs are many: from 80 up to 139 as recorded. The number of eggs is a function of the size reached by the female, viz., 80 for a specimen of 40 mm long, 139 for females with a body length of 49 mm. These ova are relatively small, and develop very slowly; they are shed in February/March (the end of the austral summer); the young eclose in September/October (the austral spring); and they reach 12-14 mm the following May. Young males can be recognized by their still rudimentary genital papillae; the females with an age of one year have Anlagen for oostegites and measure 17-18 mm in length. During the second year, the males grow to 28 mm and are ready for reproduction as soon as the favourable season arrives. The females reach around 32 mm by then; they will attain sexual maturity at 40-41 months. From all amphipods studied in these respects so far, this seems to constitute the extreme example of a slow development, of the egg as well as of the animal. This must obviously be compensated for by the large number of eggs produced, together all the same ensuring a sufficient reproductive potential for the species. At those high latitudes, Arndt & Beuchel (2006) studied the strategy of the life cycle of two sympagic species (living in the water layer just below the ice), Onisimus nanseni and Onisimus glacialis: these live for, respectively, 2.5 and 3.5 years, are univoltine (one generation a year) but are probably iteroparous (the females producing more than one brood during their lifetime). In another kind of extreme conditions, Niphargus virei, a troglobitic amphipod, attains puberty at 2.5 years, longevity is 14 years, and the intermoult periods range from 6 months to one year in the adult. The single brood a year counts 60 eggs on average and embryonic development takes approximately 3 months at 9°C. These results have been obtained in rearing (Turquin, 1981), whereas those concerning Bovallia gigantea and the species of Onisimus were gathered through analysing samples collected in the field. At the opposite, we may consider a small-sized, tropical species, Parhyalella pietschmanni, that grows fast, i.e., 50% of the males are ripe at 4.6 mm, and females at 6.4 mm, which condition seems to have been reached in a period of three weeks, and

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the species reproduces around the year. While a brood is developing in the brood pouch, the oogonia ripen again in the ovaries and the next brood follows swiftly after eclosion of the young of the preceding litter. The number of eggs per brood is relatively low, for this species, occurring at Nosy-Bé (Steele, 1973). That author thinks, in view of the quite early attainment of maturity, that up to 12 generations a year are possible. Yet, Steele (1973) also reported that the broods are not fully equivalent over the year, as those produced in winter are smaller (4-44 eggs/young) than those shed in summer (15-59 new individuals). Between those extreme strategies, all kinds of other situations seem to be possible, as many intermediate conditions were described that have obviously been realized in nature. At high latitudes, where temperatures are low and the optimal environmental conditions only occur during a short time window, the time of release of the young is most critical and only one brood may be produced. In such conditions, large broods, i.e., with many, large eggs, will represent the best strategy to survive. On the other hand, at low latitudes where conditions are favourable for long periods, eventually throughout the year, rapid development will allow many broods to be realized: there the numbers of eggs may be lower and those eggs can be smaller as well. S EX RATIOS The sex ratio is the relative contribution of the two sexes to the total of 100% individuals of a population. This ratio depends on the prevailing environmental conditions, the structure of the population at issue, as well as on the species concerned. Basically, the sex ratio should be close to 1. Yet, in collecting samples one will find almost exclusively a predominance of females, but the sex ratio approaches unity in the pre-reproductive periods, thus ensuring a maximum of reproductive potential by the time actual reproduction starts. Then, after fertilization has been completed, the ratio may drop significantly, as indeed is often the case, by a massive death of the, now superfluous, males. The causes affecting the dynamics in the relative proportions of the sexes in a population are ascribed primarily to temperature (Kinne, 1953a, 1970), or to the maturity stage of the individuals (Hynes, 1955). However, those causes are not completely known, given the current state of the investigations. Poltermann et al. (2000) studied the reproduction strategies of two sympagic species, Gammarus wilkitzkii and Apherusa glacialis. They noted very different sex ratios, viz., 1.5/1 in favour of males in Gammarus wilkitzkii, and 3/1 in favour of females in Apherusa glacialis. They concluded that the high fecundity in both these species, disregarding some retarded juveniles, the large proportion of females in Apherusa glacialis, and an extension of longevity, including multiple broods in Gammarus wilkitzkii, both would constitute possible adaptations to the special conditions of life in a relatively thin layer of water, directly under the ice.

Determination of sex S EX DETERMINATION Sex determination in amphipods is a complex phenomenon (Ginsburger-Vogel, 1985). The subject has been largely treated in vol. 2 of the present series (cf. Legrand & Juchault,

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2006; also Charmantier-Daures & Charmantier, 2006), i.e., in the framework of the general aspects of sex determination throughout Crustacea as a whole. Also, Charniaux-Cotton and collaborators have produced a comprehensive literature on the subject (e.g., CharniauxCotton, 1954, 1957), to which is referred. Herein, we shall simply recall the major issues of the process of sex determination, specifically for the Amphipoda. In 1954, Charniaux-Cotton discovered that in Orchestia gammarella the androgenic gland is responsible for that part of hormonal regulation that evokes sexual differentiation into a male. This endocrine gland controls the development of the primary and secondary sexual characters of the male, and also stimulates male sexual behaviour. A hormonal control of the sexual characteristics was also demonstrated for females. In contrast to the males, in which the gonads themselves have no endocrine function, the ovaries are the source of hormonal stimuli that determine the permanent or temporary formation of secondary sexual characters. A hormone is probably responsible for the development of oostegites in the young female; during vitellogenesis, a second female hormone is produced that is responsible for the development of the long setae that fringe the oostegites at the time reproduction is actually taking place. In various species of Gammarus, extrinsic factors, like photoperiod, can have an influence on the determination of sex. The same can be said about the activity of several parasitic protozoans, that act as epigenetic factors with a feminizing effect. I NTERSEXUALITY In species of many genera, intersex individuals have been observed in nature. Sars (1863) described a male of Gammarus lacustris bearing oostegites. In Gammarus duebeni, various types of individuals have been reported representing several levels of mixing of female and male characters. Hynes (1954) described a male with oostegites. Bulnheim (1975) noted five types of intersexes, ranging from fertile females that bore male papillae and some calceoli, up to functional males bearing one or more oostegites without setae, that did not regenerate following amputation. The percentage, however, is very low: in a lot of 7408 specimens collected in nature, 51, or 0.7%, were intersexes to varying degrees. In the family Talitridae, intersexuality is well known. A female of Talitrus saltator with one or two male genital papillae was reported by Fried-Montaufier (1968); Wildish (1970a) described the same phenomenon in Orchestia mediterranea, and Ginsburger-Vogel (1972, 1973) in Orchestia montagui and Orchestia gammarella. In 1981, Ginsburger-Vogel & Magniette-Mergault described abnormal sex ratios, specifically an excess of females and intersex males in Orchestia gammarella, which appeared to be evoked by a feminizing parasite, Paramarteilia orchestiae. The thelygeny disappeared above 22°C; between 25 and 30°C, an increase in the number of males was observed, as an expression of the normal genetic potentialities of the neofemales, as well as a concordant decrease in the proportions of intersex males. Various authors have spotted intersex individuals in Ampelisca spp. Mills (1953) described feminized males in Ampelisca vadorum and Ampelisca spinipes. Hastings

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(1981) collected five intersexes of Ampelisca brevicornis on the Isle of Man in July, that bore both male genital papillae and oostegites without setae. Further examiniation of these five individuals, taken from the same, otherwise normal, population, yielded interesting results: their body length varied between 13.0 and 15.6 mm, while the normal males of the population had an average length of 11.0 ± 0.8 mm, these reached the adult stage in June and from that moment on their growth stopped. The proportional body dimensions and the setation of the antennae corresponded with that of females or immature males. The five specimens appeared to have testes, but the functioning of those seemed to be inhibited. Four of these animals were infected by metacercariae and the fifth contained approximately 30 small cysts that were not further identified. Consequently, in this particular case it seems that a parasitic castration of males was observed. Christensen & Kanneworff (1965) noted an infection of Ampelisca macrocephala by the turbellarian Kronborgia amphipodicola concurring with sterilization and a reduction of secondary sexual characteristics. According to Bulnheim (1975), behind these transmissible parasitic castrations that may result in exclusively female broods, there would be a factor linked to environmental conditions. That author surmised the sex ratio could be affected to become biased in favour of females by short daily photoperiods and, in contrast, in favour of males by a long circadian photoperiod, but these considerations were based on experimental results only. Dunn et al. (1996) demonstrated that the frequency of intersexes is significantly correlated with an interaction of photoperiod and temperature in young Gammarus duebeni during the time of sexual determination in the course of development. They suggested that an intersex would represent an individual for which the ambient conditions would have inhibited the onset of male development. Yet, although this phenomenon may be spectacular as well as interesting, it all the same is rare in nature. Pavesi et al. (2009), who analysed the life cycle of Macarorchestia remyi on a beach in the Tyrrhenian Sea, collected in the course of one year (May 2006 to April 2007) 3484 specimens, and the population was found to be composed as follows: 729 males, 1728 females, 707 juveniles, 54 young of indeterminable sexual destination, and 268 intersexes or 7.6%. Lowry & Stoddart (1986) described in Lysianassidae: Conicostomatinae, which are animals commensal with sponges, coelenterates, bryozoans, and tunicates, phenomena of protandric hermaphroditism. This would encompass a reproductive strategy adapted to their environment. PARTHENOGENESIS There are some arguments that would elicit considering that parthenogenesis could be possible in certain species. Moore (1981b) seems to have been convinced in this respect with regard to Corophium bonellii. The same phenomenon might be observed also in Talitrus alluaudi and Haustorius arenarius, but anything of an irrefutable proof has not yet been provided.

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PHYSIOLOGY Respiration In amphipods, respiration is largely accomplished through the gills. Terrestrial species, that live in moist air, can for some time effectuate respiration without intervention of the branchiae, viz., with the aid of those zones of the integument in which the cuticle is thin and permeable. For aquatic species goes that the water current that flushes the gills is activated by the beating of the pleopods, usually at a rate of some 30-180 beats/min, according to the different species (Walshe-Maetz, 1956). The degree to which the respiratory movements are regulated is in agreement with the variations in O2 pressure in the environment. The stimulus to regulate seems to be of internal origin: as the oxygen content of the ambient environment diminishes, the speed of pleopod beats increases, but it will slow down at very low temperatures. Oxygen consumption varies with the activity of the animal. Williams (1982) demonstrated that, in Talitrus saltator, the consumption of oxygen rose from 150 to 200% in the course of the night. Such a circadian rhythm in oxygen consumption is endogenous, and persists under total darkness for at least 50 h. There is no such rhythm in respiratory amplitude, nor any influence of the tidal cycle. The basic daily oxygen uptake amounts to 0.65 ml O2 mg−1 h−1 in Talitrus saltator. Clark (1955) indicated a consumption of about 200 mm3 O2 g−1 wet weight h−1 for Talitrus sylvaticus at 15°C and Edwards & Irwing (1943) reported values of 2.5 mm3 O2 g−1 wet weight h−1 for Talorchestia megalophthalma: both are terrstrial species. In Antarctic species, Opalinski & Ja˙zd˙zewski (1978) measured rates of O2 intake of 0.130 ml mg−1 wet weight in Byblis securiger and 0.047 ml mg−1 wet weight in Cyphocaris richardi. No significant difference between the sexes appeared to exist. These authors also note that the oxygen consumption of these amphipods seems to be similar to that of other Antarctic planktonic animals. Roux & Roux (1967) as well as Roux (1975) pointed out that in Gammarus the respiratory metabolism is influenced by various factors, among which temperature; in addition, there would be a differential adaptation according to species. In some species, the increase in metabolism at rising temperatures would be triggered by an increase in activity, hence by an enlarged possibility to survive. Mathieu (1983) showed that in Niphargus rhenorhodanensis the repiratory metabolism is variable under various experimental conditions, but that the essential variation actually is determined by the ambient temperature as well as by the size of the animal. Lehtonen (1996) measured the variation in oxygen consumption around the year in Monoporeia affinis, and concluded this would be linked to the fluctuating quality of the food. Derouet (1952) reported that species living in surface waters have a higher rate of metabolism than those from subterranean waters. In some species, like Echinogammarus pirloti and Echinogammarus obtusatus, adaptation to conditions of anoxia have been found, viz., the production of lactic acid. As soon as the oxygen content of the water rises again, the level of respiration is raised and a normal metabolism is restored. All the same, the time needed for recuperation is longer for Echinogammarus obtusatus, which lives in zones

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that fall dry for less extended periods, than for Echinogammarus pirloti, which resumes normal metabolism much quicker and seems better adapted to temporary anoxia (Agnew & Taylor, 1985). Hervant et al. (1998) compared the behaviour of epigean species represented by Gammarus fossarum and hypogean forms using Niphargus rhenorhodanensis. They concluded that the hypogean species have a normal oxygen consumption 1.7-3.5 times as low as their epigean counterparts and that they are better adapted to cope with a low O2 pressure in the environment. These authors postulated that the most plausible explanation for this adaptation to a decreased oxygen consumption by hypogean forms would originate from a lower energy expenditure, especially during hypoxia, as a result of reduced respiratory and locomotory activity in those species.

Osmoregulation Amphipods occur from purely fresh waters up to fully marine conditions and hypersaline biotopes. Some families are strictly stenohaline, like species of the genuinely marine plankton and benthos. Others, notably gammarids and some Corophium spp., tolerate very large variations in salinity: Gammarus duebeni, for instance, preferably lives at 312 psu, but can occur just as well at 30 psu, or in fresh water. In euryhaline species, osmoregulation essentially takes place via the gills, while the regulatory organs are the antennary glands. Sensitivity for deviant salinity values generally increases with increasing temperature, with the exception of the intertidal Chaetogammarus marinus (cf. Dorgelo, 1973). The sodium balance in euryhaline species is characterized by the relative values of external salinity and the concentration of sodium in the blood; the total volume of blood in an animal would be of influence as well, in this respect (Lockwood, 1970). The loss of NaCl in waters of low salinity is effectuated both through the production of urine and directly, via the body surface. It has been demonstrated that Gammarus tigrinus, Gammarus zaddachi, and Gammarus duebeni adapt to low salinity conditions through a reduction of the permeability of the body, the production of hypotonic urine, and by blocking the transport of NaCl through the integument. The adaptive superiority of Gammarus pulex for living in fresh water as compared to Gammarus duebeni that occurs in brackish waters, thus results from the greater capacity of Gammarus pulex to absorb Na+ from the environment and to concurrently inhibit its excretion, both through the mediation of the body wall. In Gammarus oceanicus, hyperosmoregulation involves significant changes in the ultrastructure of the gills (Milne & Ellis, 1973). In a study on sympagic species experiencing large variations in temperature and salinity that result from the cycles of the formation and melting of the ice, Kiko et al. (2009) showed that Apherusa glacialis, an euryhaline species, has to be capable, at the same time, of depressing its freezing point. In order to achieve that, regulation of the concentrations + of several ions is required: reduction of [Mg2+ ] and [SO2− 4 ] and an increase in [K ] and 2+ 2+ [Ca ]. Apparently, a strong decrease in Mg concentration also serves as an anaesthetic

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mitigating the, probably discomforting, experience of the animal that results from those low temperatures.

Calcium metabolism In Crustacea in general, calcium metabolism is of special significance, and hence it is particularly intense as well. The Amphipoda are no exception, albeit that the proportional loss of calcium as a result of the disposal of the old exoskeleton after exuviation is variable: after Graf (1974), that loss is estimated as follows: • 77% in Gammarus pulex, an epigean species of fresh waters; • 56% in Niphargus virei, also from fresh water but hypogean; • 53% in Orchestia gammarella, a supralittoral amphipod. In aquatic species the actual loss of calcium through shedding the exuvium is quite significant, whereas it is less so in terrestrial forms. The calcium economy of a species is directly related to its mode of life. The origin of the calcium used by the animal, an important component when building a new exoskeleton at each successive moult, appears to be twofold: exogenous as retrieved from the water as well as from the food; endogenous as it has been established that calcium is stored preceding exuviation, and is also provided by the old cuticle through partial resorption from the integument soon to be discarded. The ways of building up a stock of calcium are varied among Crustacea, but in certain amphipods, as Orchestia and Niphargus, it has been amply demonstrated that stocks are formed as concretions in the intestinal caeca. These formations are composed of calcium carbonate (CaCO3 ) precipitated in an organic matrix containing weakly acidic mucopolysaccharides; and they are built up during pre-exuvial stage D, while again solubilized in the hours following ecdysis. According to the life style of the organisms, the quantity of calcium stored is variable, relative to what will be needed for the new exoskeleton. If, as is the case in gammarids, the animal lives in water in which it can find the calcium required directly in the ambient environment, the stock is small: at each moult the better part of the calcium is renewed. In species that frequently live out of the water, or are even effectively terrestrial, like some Orchestia, and that consequently can only take up mineral substances through their food, the stock may represent more than two-thirds of the quantity required. After all, the animal needs to consolidate its new cuticle as quickly as possible, because it can only start feeding again when the new exoskeleton has become rigid. With respect to Niphargus, its representatives seem to comprise a stage intermediate between the two preceding examples and their calcium economy should probably be linked to the general slowing down of their metabolism. In these cavernicolous species, calcium stocks are necessary in order to provide for the immediate needs for mineralizing the new exoskeleton, which can not be realized by a slow metabolism. The transport of calcium in amphipods takes place via the intercellular route, and involves the same cells that both build up, and resorb the calcium concretions. The calcium cycle is under control of the moulting hormone: building up the stocks is realized when the hormone is present, resorption in its absence.

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ETHOLOGY Behaviour H ABITATS Amphipods have colonized all aquatic realms as well as certain moist terrestrial habitats (damp beaches, forest litter). However, the world’s oceans doubtlessly house the largest number of amphipod species and these can be divided into two major groups: planktonic and benthic forms. Continental waters, as a result of their generally limited depth, essentially contain only benthic species. a. Planktonic species live in the water column but mostly, at least for part of their lives, associated with another planktonic organism. This group basically comprises the Hyperiidea, with in addition some bathypelagic Gammaridea. Amphipoda as a whole constitute an important part of the macroplankton, but are particularly abundant in colder waters where they are preyed upon by birds, marine mammals, and pelagic fish. These species live either as autonomous individuals, or, in part or in whole, associated with another planktonic organism. The morphology of each taxon is obviously adapted to the life style of its members, including their actual habitat: large, well-developed eyes are present in Phronimidae, much elongated appendages in Stilipedidae and Vitjazianidae, and a translucent body in Hyperiidea. In this group the sole example of what can be called a larval stage is found (Laval, 1980), as the young does not complete its development in the brood pouch but is deposited precociously into the animal parasitized by its mother. Inside the host, i.e., still in a rather protected environment, it will now further complete its final intermoult period and then moult to reach the juvenile stage, which is similar to the adult morphology. This process evidently extends the period during which the young can grow relatively safely and can get fixed to its host. The planktonic forms encompass all large trophical classes, notably carnivores (as predators on small organisms like larvae, small crustaceans, or worms), herbivores (grazers on phytoplankton), suspension feeders (including filter feeders), and necrophages. Circadian vertical migrations have also been observed in amphipods, some involving large amplitudes. Hurley (1969) considers the Hyperiidea a cosmopolitan group and, though their biology and ecology are only poorly known, he thought that some species that apparently would have a very wide distribution, might include populations that will show differences in a micromorphological and/or physiological sense, related to the differences in environmental conditions over such a large area. France & Kocher (1996) demonstrated that in Eurythenes gryllus genetically differing populations exist at different depths, with the largest discrepancies occurring between the bathyal and abyssal zones. These authors suggest that physical and ecological factors would be of great influence on the mechanism of genetic isolation. b. Benthic species are more numerous and have also been studied more intensively. They occur at all depths and on all types of substrate. Some of them may live in the plankton during quite short periods of time.

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Fig. 56.40. Haploops tubicola in its tube, in a position to capture food. [After Enequist, 1999.]

(1) In soft-sediment substrates, three main types of behaviour can be noted: • Tubicolous species construct tubes of sand or mud, mostly glued together with mucus (some species have mucus secreting glands on their 3rd and 4th pair of pereiopods). The tubes, common in Ampeliscidae, can be constructed from selected particles: pure clay or organic material in Haploops, sand grains and foraminiferan tests in certain Ampelisca. Mills (1967) described the tubes of Ampelisca vadorum and Ampelisca abdita and indicated that the interior of the tube is purely mucous, without any sand grains protruding. The tubes are of varying length, according to the species involved (they can attain two times the length of the animal) and of varying width as well. The animals also occupy their tubes in different manners: Haploops tubicola normally lies across the opening, but can retreat into the tube if required; then the entry closes upon the inhabitant and completely hides it (Enequist, 1949) (fig. 56.40). Other species are situated, under normal conditions, along the length of their tube, whether totally inside or partly extending from it. A variant of the behaviour of tubicolous species is found in those that inhabit empty gastropod shells, like Photis conchicola (cf. Carter, 1982) or shells of pteropods: Pterunciola spinipes (cf. Just, 1977). • Burrowers dig themselves actively into the sediment, using their pereiopods that are, accordingly, broad and profusely provided with setae so as to dig a proper hole for the animal to hide itself in. Haustoriidae and Bathyporeiidae belong to this category. Their tunnels can reach a depth of approx. 30 cm into the sediment. Other species use their rostrum and/or general movements of their body, i.e., writhing to penetrate into the soft substrate. Interstitial species may be considered a subcategory of burrowers, but yet in a most special way. These forms, usually of small size, subcylindrical in shape, without any rough parts on their body surface, glide through the interstitial network constituted by the spaces between the sand grains. This group, including the Bogidielloidea and the Ingolfiellidae (sensu lato), is well represented in continental waters.

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• Free-living species tend to rest on their side on the bottom between periods of activity, as, e.g., Liljeborgiidae. Some species live near the bottom and thereby constitute a special ecological group, showing characteristics of both planktonic and benthic forms simultaneously: the suprabenthos. The Amphipoda of the suprabenthos are primarily natatory species that are able to make cyclical migrations and that find abundant food in the near-bottom layer of the water column (Dauvin et al., 2000, 2006). (2) On hard substrates, notably rocks, five types of behaviour are found in direct connection with the (micro-)habitat: • Tubicolous species construct their tubes on some supporting structure: algae, branches of hydrozoans, or bryozoans. The tubes of these forms are made of fragments of algae and other organisms, other kinds of small particles, and mucus. Most of the time the animals are (partially) inserted in their tube, while the anterior part of their body extends from it; this situation is found in Corophium and Ericthonius. The nest constructed by Ampithoe rubricata using various algae, should also be mentioned here. • Climbers live clinging to the substrate with their pereiopods, and as such seek holdfast on algae, branches of hydrozoans or other Cnidaria, as well as on bryozoans. They graze or capture preys with their gnathopods while moving around (Caprella). In trying to be as inconspicuous as possible for predators, they sometimes present remarkable mimicry (Bocquet & Peltier, 1963). • Swimmers are species that move around in the vicinity of algae, sometimes even using the mucus that the algae secrete; they hide in the small spaces and/or under roughened structures of those, or under epilithic organisms; many Hyale species belong to this group. • Inquilines hide themselves in the cavities and other hollow structures of other animals, like the hollows of sponges, the tunica of ascidians, inside branchial chambers of molluscs and brachiopods, and on or between the spines of echinoderms, or on the cuticle of those. Futher in this chapter, we shall investigate this category somewhat closer, within the framework of interrelations of amphipods with other species. • Xylicolous forms are the Cheluridae. These have a specialized habitat because they are adapted to living in immersed pieces of wood that bear holes of various kinds. Thus, together with some isopods, they constitute the basis for a characteristic faunistic assemblage. In this context, finally, it should also be remarked that some benthic species live on floating substrates: Hyale grimaldii lives on the carapace of marine turtles and Parajassa pelagica inhabits marine macroalgae of the genus Sargassum. The terrestrial species of Amphipoda mainly occur in tropical forests, where they live in the top soil layer. Birch & Clark (1953) reported numbers up to 4000 specimens per m2 in forests near Sydney. A physiological adaptation has taken place following the

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colonization of the terrestrial domain. The gills are remarkably large but are not especially protected; the exoskeleton is smooth and fragile, the pleopods often vestigial, and in various species there is a large spine between the rami of uropod 1 that seems to be used in tearing the exuvium after the moult. The eggs are larger and less numerous than in marine species but when released the juveniles are larger and more developed (Hurley, 1968). Morritt & Richardson (1998) demonstrated how the female of Mysticotalitrus cryptus controls the moistening of the interior of the marsupium through secreting urine. The eggs and embryos are humidified via capillarity and are hence maintained during their development in an environment that is compatible with their possibilities of survival. VAGILITY AND MIGRATION a. Types of locomotion. – The general way of locomotion in amphipods is swimming. The movements used by aquatic species for swimming are (1) flexion of the posterior part of the body; and (2) the beating of the pleopods, although the primary function of pleopodal beating would rather be to maintain a circulation of water for respiration. The position of the body while swimming is variable: the most common position of horizontal, with the back upwards. Many species, in contrast, swim with the ventral side up: Corophium, Urothoe, Ampithoe. The natatory movements can also be made in a lateral position, i.e., with one of the lateral sides facing upwards; this is the way Liljeborgiidae swim, while lying on, or being very close to, the bottom, while their locomotion is assisted, in addition, by the five pairs of pereiopods. Species of Caprella swim by contracting the body as a whole, but can also move by climbing the dendriform colonies of hydrozoans or the algae among which they live. Species that live in interstitial habitats wriggle and writhe between the sediment particles. Some actually dig into the sediment, with the aid of either their antennae (Urothoe), their pereiopods (Talorchestia, some Haustoriidae), or their pleopods. These animals may dig deep into sediments that are not too tightly packed, e.g., Haustorius arenarius can reach depths up to 30 cm (Macquart-Moulin, 1984). Littoral and terrestrial Amphipoda can also leap, but their usual way of moving is by crawling. When they move jumping, as, e.g., Talorchestia is able to, animals of 1-2 cm length can reach a height of 20-40 cm and cover a horizontal distance of 1 m. The jump, which has only been observed in Talitridae, is performed by a sudden, strong extension of the posterior part of the body, mostly accompanied by strong strokes of the uropods. Yet, Talitridae can also move forward by crawling on their side. Depending on the actual conditions of the habitat, some species successively use all modes of locomotion: jumping, creeping, swimming. b. Large migrations. – Explanations for migration in amphipods have been furnished from different points of view: searching for food, connected with reproduction, looking for shelter, fleeing from danger, whether supposed or real, and simply seeking better conditions to live. Movements in search of food can have different amplitudes: Talitrus spp. move on a beach searching for vegetable debris, the main component of their diet. Such remains are

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deposited on the sandy shore by the tides. In view of the abundance of this type of organic remnants, the movements involved will be in the order of several metres or at most tens of metres. In contrast, species living on the bottom in deep waters, like the necrophagous Lysianassidae, may well undertake considerable displacements when a suitable prey is presented. Hessler et al. (1978) observed the first amphipod to arrive between 5 and 20 min after a bait had been placed. These authors counted 30 individuals after half an hour and by then stopped counting because of the increasingly large numbers of amphipods. Taking into account the low density of these organisms in the deep sea as known from other collecting methods, like nets or dredges, which yield only a few individuals in a haul of several hundreds of metres, migrations over longer distances seem to be required to assemble several hundreds of individuals in a time span of a few hours. Movements pertaining to reproduction are generally made in the water column. However, only relatively little research has been done on the subject: most of the knowledge we have originates from the results of fishing activities at the surface, in which for some species only adults were collected, in some cases of one sex only. MacquartMoulin (1984) thus found in plankton samples over 500 individuals of Urothoe elegans in a proportion of 90-100% males versus a corresponding 10-0% females. The same author found in comparable samples only males of Paraphoxus maculatus, and between 95 and 100% males in Metaphoxus pectinatus, Metaphoxus fultoni, Perioculodes longimanus, Pontocrates arenarius, and Atylus vedlomensis. He considered that this phenomenon of circadian migrations might extend the reproductive territory of certain species. The littoral Talitridae are much dependent on the degree of moisture of their biotope and, as this is variable, they must move in order to remain in the conditions that are optimal for their survival. In experiments, Talitrus saltator, Orchestia gammarella, and Talorchestia deshayesi survive 9-16 h at a humidity of 95% saturation but only remain viable for 1 h to 1:45 h at a relative humidity of 36% (Williamson, 1951a). Hence, it is concluded that the intensity of the migrations of Talitrus saltator would be directly related to the degree of moisture as well as to the quantity of food available (Geppetti & Tongiorgi, 1967a, b). Also other factors influence amphipod migrations, like temperature, light conditions, the tidal rhythms, etc., but these have all been only sparingly studied to date. c. Migrations: significance and processes. – In amphipods, two types of migrations have been studied: vertical migrations in the water column in which both benthic and planktonic species are involved, and (largely horizontal) migrations of Talitridae on beaches. • Diurnal-nocturnal vertical migrations are extremely difficult to investigate in holoplanktonic species, as a result of problems in adequate sampling (at the right time and place) given the (often irregular) distribution of the various species. Thurston (1976), however, established the relative distribution at day- versus nighttime for the 30 most common species in the Canary Islands (table IV). Some species appear to make no migrations (Primno macropa), others migrate either by day (Hyperioides longipes and the various species of Phronima), or at night (Anchylomera blossevillei).

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TABLE IV Relative day/night distribution of some species of planktonic Amphipoda [after Thurston, 1976]. R day/night = number of individuals collected in daytime/number of individuals collected at night Species Primno macropa Hyperioides longipes Anchylomera blossevillei Phronima sedentaria Phronima stebbingi Phronima colletti

N total of individuals collected

R day/night

2171 357 29 28 28 27

1.03 4.10 0.12 3.00 13.00 26.00

In benthic species, nocturnal migrations into the water column occur following a rather well-studied scheme, albeit that the actual cause(s) for these movements are hard to recognize. An excellent revision by Macquart-Moulin (1984), supported by many samples collected by the author personally, considers that the nocturnal migratory behaviour would be a unique characteristic of a certain number of families: Haustoriidae, Ampeliscidae, and Phoxocephalidae. However, within those families, only a limited number of genera would actually have developed this specific behaviour. In the world’s oceans as a whole, it seems that everywhere the same families and the same genera show migratory behaviour. The nighttime migrations described until now are far from being uniform, and instead display multiple modalities as regards duration and time of night of the planktonic phase, the numbers of such phases, and their sensitivity with respect towards lunar illumination, as well as to various types of disturbances. Macquart-Moulin (1984) distinguishes at least four types of migration, as follows: – hyponeustonic; – superficial planktonic; – uniform planktonic; and – deep planktonic. The daytime habitat of a species does not seem to bear any special relationship with the type of distribution in the nocturnal plankton. Anyway, after the migration has been completed, it would seem that the animal returns exactly into its original environment. The migrations of a large number of species seem to be evoked by a quite precise level of illumination. The appearance of different species in the plankton, though always in relation to the daily period of dusk, is by no means simultaneous, as the exact hour of appearance depends on the characteristics of each species. Yet, those hours can grossly change with the progress of the seasons. • Horizontal migrations have been studied by Lindström (1991) and Lindström & Fortelius (1992), in an attempt at an experimental approach to the factors that might affect horizontal migrations in the marine amphipod Pontoporeia affinis. It appeared that those movements in this species were influenced by the current, the presence of sediment, and salinity as well as temperature. • In migrations of Talitridae on beaches, the circadian rhythm of movement has been demonstrated and further studied in many species, e.g., Orchestia gammarella (cf.

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Wildish, 1970c), Talitrus saltator (cf. Williams, 1979), and Talitrus deshayesi (cf. Williams, 1982). The direct causes for migration seem to be basically, as already mentioned, searching for food as well as seeking a certain level of humidity. The results of Geppetti & Tongiorgi (1967a, b) indicate that no other factor, i.e., neither lunar phases, nor temperature, nor barometric pressure, nor the wind, will affect migrations if they do not affect either relative moisture or the availability of food. In the case of Talitrus saltator, the daily migration takes place from the shore to the dry land at 2-3 hours after midnight with the return occurring at dawn (Geppetti & Tongiogi (1967a, b). Pardi & Papi (1953) demonstrated in the same species that the direction of movement of the animals would be steered by astronomic orientation. Such an orientation, whether based on the sun, the moon, or the polarization angle of the incident light, has been established in various Talorchestia, Orchestia, and other Orchestoidea. Apparently, the phenomenon is controlled by an internal, biological clock (Papi, 1955) that is able to progressively adapt to new environmental conditions (Papi & Grassi, 1955), and would itself be influenced by the ambient temperature. In the tidal zones, the tidal rhythmicity would be more significant for certain species than the day-night rhythm. In those cases, the activity maximum is correlated with high water rather than with any other factor each twenty-four hour period. Furthmore, it may be evident that the seasonal rhythm with its variations in temperature and photoperiod will have an impact on the activity rhythm of Amphipoda. With respect to the orientation of the Talitridae, there is a certain controversy: some experiments would have shown that a possible non-visual orientation could be at issue. Arendse (1980) performed a series of experiments that proved this non-visual orientation to exist in Talitrus saltator, and this orientation would be complex as well, since the frequency distribution of individuals would be uni- or multimodal. In another paper, Arendse & Kruyswijk (1981) considered that the non-visual orientation of talitrids would be based on the earth’s magnetic field. Mezzetti et al. (2010), on the other hand, pointed out that the various forms of the compound eyes of the Talitridae, from their common basis, would have developed sufficient morphological and physiological differences to justify presuming that their vision under various conditions of illumination can have been optimized and thus permit adaptation of the species of that family to the specific conditions of their respective habitats. The various species of Talitridae that successively occur in the marine littoral zone and the increasingly terrestrial zones are subjected to multiple environmental factors, among which: the sun, the moon, the optical condition of the air, both above the seawater and above land, the magnetic field, the inclination of the substrate, and the wind — and none of those factors will act on its own. • Migrations in rivers and streams of amphipods have been observed at night; they are influenced by the velocity of the current. As the current obviously has the effect of carrying off individuals, populations can only remain in place by reproduction as well as a certain degree of negative rheotaxis: i.e., by actively moving upstream. Meijering (1977) studied the ratio of both displacements, i.e., the washing downstream and the active migration against the current in Gammarus fossarum. The ratio of recovery

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appeared to be around 50%, but this average varies with the time of year as well as with the specific conditions of the habitat. For Gammarus pulex, Hughes (1970) demonstrated that such migrations are much more significant under conditions of weak, than under a strong current. According to Goedmakers & Pinkster (1981), the phenomenon of the regular migrations of Gammaridae in a stream is complex, both for migrations upstream as for those downstream. The seasonal variations in the migration upstream are clear-cut, and the maxima are reached in summer; those downstream are less clearly marked. The daily variation corresponds to a maximum upstream at sunrise and a maximum downstream at sunset. The dominant factor would be temperature, and next in line the change in chemical composition of the water; the actual light conditions seem to be less important than is generally assumed. I NDIVIDUAL MOVEMENTS Amphipods present a whole series of movements of the various appendages in connection with the activities of prospection of their environment, including digging, the search for and acquisition of food, feeding themselves, respiration, the contruction of tubes, and grooming: all activities that may not always be easily distinguished in practice. In order to dig into the sediment, various species use different methods. Talitridae use their gnathopods to dig and push the sand toward their urosome, which then takes over and pushes the dug-up sediment further backwards (Nelson, 1980). Haustoriidae move sand by creating a water current with their pleopods and next bury themselves in the (initially shallow) hole thus formed. Species of Paraceradocus dig the sand from under a large stone by pressing their dorsal side under the stone and then push away the sand with their gnathopods 2, thereby creating a protective barricade; they then turn over and occupy the cavity thus created while protecting their long antennae under their ventral side, partly by pushing these underneath their body with their pereiopods 5-7. The setae on gnathopods 1 and 2 enable them to effectively handle the sand (Coleman, 1989). With regard to grooming of the appendages, the antennae with their setae will retain particles and need to be cleaned either to recover particles that are to be ingested as food, or else to eliminate undesired items. In general the carpi of the gnathopods are used to brush such particles to the maxillipeds. Coleman (1989) observed in Paraceradocus cleaning of the uropods with the propodi of the gnathopods, that also brushed the animal’s ventral side and the pereiopods. Most often the particles collected are transferred to the maxillipeds in order to be ingested. In Corophium, the antennae that act as the alimentary filter are cleaned with the gnathopods 1, in which action the flagella are drawn between the dactylus and the denticulate palmar edge of the propodus. The animal cleans the various sides of the cephalon as well as the uropods, the brood pouch, the pereiopods as well as the pleopods with the carpi of gnathopod 1. In Lembos websteri both sexes use their antennae to collect sediment and detritus and transport that into their tubes; cleaning the antennae is likewise done with the aid of the gnathopods. It is surmised that many of the microstructures observed on the cuticle (setae, combs, scales, etc.) are used during such cleaning activities.

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Feeding M ODES OF NOURISHMENT In amphipods, almost all major modes of feeding are represented, in fact, from whichever point of view. There are suspension feeders, detritivores, grazers, predators, necrophages, carnivores, omnivores, and phytophages; and as such macro- and microphages. These various categories may also be superimposed on one another, and sometimes mingle, replace each other in the course of time, or according to environmental conditions. We shall here classify the various groups of Amphipoda according to their mode of acquiring alimentary matter: active or passive filtering, grazing, predation, necrophagy, and we shall also examine the special case of parasitism. a. Filterers. Filtering probably is by far the most frequently encountered method of nourishment. Amphipod morphology, with its many setiferous appendages, is remarkably well suited to constitute filters, i.e., to form together a composite apparatus for catching particles that are suspended in the water. Various adaptations enhance those potentialities, so as to extend the filtering surfaces, increase their effectiveness, and to create conditions optimal for making use of environmental peculiarities, like local currents. The mechanism for filter-feeding comprises a filter, a method to create a current, and a means of cleaning the filter and recover the alimentary matter. In some families the gnathopods are strongly setiferous and can constitute a filter; species of the genus Leptocheirus have a gnathopod 2 of which the basis and merus are bordered by very long setae on their ventral side, while gnathopod 1 also bears numerous setae. The antennae constitute the filter that is most well-known, and the behaviour of the species of Haploops and certain Ampelisca has been described many times: the animal is lying on its back in the tube it has contructed, and is in a regular way beating its antennae that are equipped with long setae to capture particles (fig. 56.40). Rigolet et al. (2011) have experimentally studied filtration in Haploops nirae, a species that can develop populations with thousands of individuals per m2 over several hectares. An increase in current velocity has no significant effect on feeding activity, although we can observe a slight increase in beating frequency of the antennae. The authors cited (Rigolet et al., 2011) observed the functioning of the antennae, which in this species are as long as the body, are armed with setae that are themselves bordered by setules, and that together form a semi-circular basket with a mesh size of 10-25 μm, thus essentially retaining particles of 20 μm in diameter. Experiments with organic as well as non-organic particles have shown that these Haploops are perfectly well adapted to feed under turbulent conditions. The authors estimate that the Haploops living at 30 m depth in the Bay of Concarneau have the capacity to filter the entire water column above them in 4-5 days, and the volume of the bay as a whole in 29-30 days. In Corophium, the setae of the meri of gnathopod 2 constitute a filter filling the crosssection of the tube, which can be extended by the animal to various degrees; the filter is periodically cleaned, which operation lasts 1.5-2 seconds (Dixon & Moore, 1977).

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Polycheria antarctica, which lives in the tunica of certain ascidians, lets its antennae float outside the cavity and in that manner catches alimentary particles brought forward by the current created by the ascidian. In Haustorius arenarius, a filter has been observed that is formed by the maxillae, which would create a current themselves through vibration. The current in which the particles are carried is usually the same as that which serves respiration: it originates from the beating of the pleopods and may be enhanced by movements of the body as a whole, i.e., of the trunk, or, as in Haustorius, by vibrations of the mouthparts. Cleaning the filter is performed with the gnathopods as well as with the buccal armature, which is rich in setae and spines. Consequently, this process of acquiring food is complicated, and requires involvement of many of the animal’s appendages. b. Grazers. In this category we place animals that scrape the substrate, either to consume the film of micro-organisms that develops there, or to directly attack its vegetal support. Liljeborgia brevicornis and Eriopisa elongata scratch with their gnathopods the surface of the mud in order to ingest the film on the surface. Ampithoe, Hyale, and Jassa live among algae and apparently nourish themselves by scraping these and by consuming both the superficial bacterial mat and the supporting algal tissue. c. Predators. Many Hyperiidea are predators. In rearing experiments, Parathemisto gracilis has been observed to chase Artemia and the prey is captured with the posterior pereiopods. Once caught, the prey animal is directed forward, to the gnathopods, which tear off pieces that are subsequently brought to the mouth. The predator needs 7-15 minutes to consume an Artemia. From the stomach of Hyperia galba nematocysts have been collected, which would indicate that it feeds itself by grazing on the tissues of its host, a scyphomedusa. Many Caprellidea catch small crustaceans, worms, and hydrozoans, and are even not infrequently cannibalistic. Oliver et al. (1982) have demonstrated the significant amount of living prey in the stomachs of Phoxocephalidae collected in the sand (Annelida, Nematoda, Copepoda). Oshel & Steele (1985) found tissues and spicula in the digestive tube of Paramphithoe hystrix. Gibbs et al. (2011) observed the development of Elasmopus levis when rearing sea urchins, and watched the amphipod feed on the epithelial tissues of the urchin, thus affecting the success of rearing. d. Necrophages. This mode of feeding seems to constitute the principal way of nourishment in amphipods living in the deep sea as well as in those occurring in polar regions. The most specialized species are found among the Lysianassidae sensu lato and the Stegocephalidae. These organisms seem to be equipped with a very sensitive and effective system to locate carrion. Investigations with the aid of cameras, among which television equipment, have uncovered an extremely rapid and abundant flocking in of necrophagous amphipods on a (dead) prey (Hessler et al., 1978). The species at issue also seem to be able to devour a large quantity of food, i.e., gorging, and to store that in their digestive tract, probably in direct relation with the scarcity of food in those habitats. Paralicella would allegedly be able to increase its body volume by 3-5 times. Recent studies on four necrophagous species inhabiting the bathyal and hadal zones (Blankenship et al., 2006, 2007) have shown:

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• that each species occupies a quite distinct bathymetric stratum, a strategy that would allow the coexistence of these four species in those extreme environments; • that their trophic strategy would be remarkably flexible, i.e., if necessary they will also behave as detritivores, or even predators. This flexibility would thus enable them to survive in extreme biotopes, where food is particularly scarce hence constitutes a decidedly limiting factor. The high contents of fatty acids in four Lysianassidae in the Subantarctic confirm their diet is essentially of animal origin (Würzberg et al., 2011). e. Parasites. In amphipods, no species are known that can be characterized as totally parasitic. However, some ambiguous cases exist nonetheless. Cyamidae live on the skin of whales, and they probably graze on these. Certain Hyperiidea, Leucothoidae, Colomastigidae, and species of Leucothoe live inside coelenterates [= cnidarians], ascidians, brachiopods, or sponges, and it seems probably that at least some of them nourish themselves at the expense of their hosts. In a single family, various modes of feeding may be employed. Caine (1977) listed four for the Caprellidae: filtration, predation, necrophagy, and grazing. A special case of coprophagy has been described by Corbari et al. (2005) in Parvipalpus major. This species lives on bathyal muddy sediments and is equipped with pereiopods 5, 6, and 7 that have long, curved dactyls with which it can secure itself to the bottom. From that position, the individual can stand upright and scan the water column as well as the surrounding substrate in search for food. When all nearby alimentary matter has been exhausted, the animal moves by making a jump, which must be an effective means of locomotion in an environment that is relatively poor in nutrition; to complement other modes of feeding, it is able to practice coprophagy: “to bring its head toward its anal opening” (Carbari et al., 2005). Guerra-Garcia et al. (2009) studied the alimentary regime of 62 species of Caprellidae and concluded that detrivory accounts for 86% of their diet. C OMPOSITION OF THE FOOD AND ITS SIGNIFICANCE IN THE COURSE OF THE LIFE CYCLE

The actual composition of the food of amphipods has only been little studied in detail. The basic data available originate from a limited number of experiments performed as well as from the few observations that could be made in the field. We have already referred to Oliver et al. (1982) and seen, that for certain Phoxocephalidae goes, that their way of nourishment is effectuated at the expense of the larvae and young of invertebrates that definitely play an important role in the biocoenosis. Segerstråle (1973) already demonstrated a negative correlation between the abundance of Pontoporeia affinis and the young of Macoma balthica in the Baltic Sea. Oliver et al. (1982) found that same correspondence between Heterophoxus videns and Annelida: Polychaeta in McMurdo Sound and between the total of Phoxocephalidae and polychaetes in California. If those observations can be confirmed, the actual significance of Amphipoda as predators in biological communities and as controllers of the equilibrium in such communities, should be reappraised.

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Among herbivorous grazers, Greeze (1968) mentioned 30-40 species of plants that constitute the food of four species of amphipods in the Black Sea: Dexamine spinosa, Ampithoe vaillanti (= Ampithoe ramondi), Gammarellus carinatus, and Gammarus locusta. The qualitative composition of the food does not change fundamentally in the course of a year: there seems to be no rigorous selection of food items, but rather an opportunistic behaviour steered by actual availability. The daily rhythm of alimentation varies according to species as well as with the period of the life cycle of an individual. The duration of digestion is also variable and is influenced by temperature, sex, age, and the general physiological status of the animal. The amount of food taken per day varies considerably, and is in the order of 1.5-2 mg for Ampithoe ramondi against 5 mg for Gammarus locusta. Steele & Steele (1975) pointed out the correlation between the release of the young in Gammarus of the northwestern Atlantic and the availability of delicate, ephemeral algae, the development of which might well constitute the determining factor in the onset of the reproductive cycle in those species. In experimental trials, those authors demonstrated that, among various food items, these algae ensure the survival of the young in optimal conditions. Later on, the older young would need other types of nutrition as well, including animal matter in order to complete their growth. Dickson (1979) showed that the presence of leaves and the micro-organisms associated with those, is necessary for proper growth of the troglobitic species Crangonyx antennatus, and that author considered the distribution of this source of food would largely determine the distribution of the species. The factors that determine the choice of algae in phytophagous species are varied: the (obviously chemical and physical) composition of the algal species, their nutritive value, as well as their actual form would be of influence, but also the habits of the amphipods that will search for species they are already acquainted with from previous meals (Poore & Hill, 2006). In benthopelagic species that often occur at great depths, large swarms have been noted in certain species, like Halice hesmonectes (1000 ind.l−1 ), near hydrothermal vent sites. Sheader et al. (2000) established that such swarms are not connected with reproduction but rather with the existence of sources of food.

ECOLOGY The influence of environmental factors In the natural environment, it is very difficult to separate the impact of each individual factor on the distribution of species. This difficulty arises from the fact that the various factors interfere and may evoke actions in the organism that can be either synergistic, i.e., reinforce each other, or be antagonistic, i.e., require opposing reactions from the animal. Accordingly, the responses of organisms towards the complexity of the environment are most often pluriform. Taking these facts into account, and disregarding too much specific details, we may all the same point out the general lines along which the influence of the principal environmental factors modulate the life of animals, as far as these have been studied in their various aspects.

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T EMPERATURE The ambient temperature affects most biological processes, like metabolism, respiration, osmoregulation, reproduction, the duration of the life cycle, and growth. Most often, the limits of temperature values between which those biological functions can normally proceed are quite restricted. Gammarus pulex would be regularly adapted to average temperatures of 15-20°C, while it has the possibility to adjust to extremes of 5 and 25°C. Gammarus fossarum generally thrives at much lower averages, 5-10°C, and can adjust to an upper limit of 20°C (Roux & Roux, 1967). Talorchestia megalophthalma lives optimally at a temperature of 33°C, but dies at 43°C and goes into hibernation at 10°C (Edward & Irving, 1943). As the temperature rises within the interval compatible with a normal life, the animal’s metabolism increases and its heart beats faster (Kinne, 1961). The temperature can influence the rate of food intake, digestion, the actual cellular metabolism, and modify the proportion in which the various components of the food are effectively utilized. The rate of digestion also significantly increases when temperature rises. Greeze (1968) considered that in Dexamine spinosa from the Black Sea, digestion takes 20 h at 4-5°C versus 25-37 min at 26-28°C. Welton et al. (1983) measured the time required for intestinal transport in Gammarus pulex and found values of 119-160 min at 7°C and 45-59 min at 13.8°C, respectively. Respiratory activity also increases with a rising temperature. Gammarus limnaeus consumes 25-290 μl O2 g−1 dry weight h−1 at 10°C and 110-750 μl O2 g−1 dry weight h−1 at 23°C (Krog, 1954). Gammarus pulex consumes 175 μl O2 g−1 dry weight h−1 at 14°C and 292 μl O2 g−1 dry weight h−1 at 21.5°C. The duration of the life cycle can vary considerably. Sheader (1981) mentioned that the time necessary for an animal to grow from eclosion to maturity in Parathemisto gaudichaudi is 42 days at 12.5°C and 120-180 days at 5-6°C. Hynes (1954, 1955) gave for Rivulogammarus duebeni 14 days at 18°C versus 55 days at 5°C and for Crangonyx pseudogracilis 14-17 days at 15°C versus 48 days at 3-5°C. Reproduction is often restricted by temperature limits that are more strict than those regarding the other processes of life. Gammarus duebeni can live, in Germany, at temperatures between −1°C and 26°C, but it reproduces only between 3 and 22°C (Kinne, 1953a). In contrast, temperature evokes phenomena of preferential production of only a single (female) sex as well as intersex individuals in certain populations of Orchestia gammarella. At 17°C an excess of females and of intersex males is found, whereas at 22°C the broods are normal. Ginsburger-Vogel & Magniette-Mergault (1981) demonstrated that the epigenetic factor inducing this phenomenon, in this case is a feminizing parasite that itself is sensitive to temperature. These authors also proved that a rise in temperature during embryonic development would intervene in the resulting sex ratio, while no influence of the parasite could be traced. Mouritsen et al. (2005) presented evidence for the synergistic impact of an increase in temperature and the infection of Corophium volutator by a microphallid trematode. With the aid of a model based on data collected both from experiments and in the

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field, they pointed out that an increase in ambient temperature of 3.8°C would effectuate the extinction of the Corophium population. Studer et al. (2010) performed a series of laboratory experiments with Paracalliope novizealandiae infected by the trematode Maritrema novaezealandensis. At low temperatures, 500 hours at salinity 2, but requires a value of >5 to complete its moulting cycle and to grow, while it only reproduces at salinities in excess of 7. The euryhaline species Gammarus duebeni can produce eggs both in brackish water and in saline water. According to Kinne (1953b), females of 13-14 mm tested at salinities of 2, 10, and 30 produced a maximum of 10 eggs, at temperatures of 8-15°C as well as at 18-20°C. The percentage survival of those eggs was the same for all three salinities but there was a maximum of 10 at salinity 2 and of zero at salinity 30 for temperatures of 16-20°C. Females exposed to high salinities are more sensitive to such conditions than males. In Gammarus roeselii, the sex ratio is in favour of females under normal conditions, but may change to be in favour of males under more extreme conditions (Sornom et al., 2010). Kinne (1952) remarked that, at salinity 30, the sex ratio in Gammarus duebeni is in favour of males. However, as for temperature, discussed above, also here salinity shows an indirect effect, since the specimens Kinne studied were infected by a feminizing microsporidian. At low salinities all individuals are infected, but this is not the case at higher values, at which a normal sex ratio is realized accordingly (Bulnheim, 1969). Salinity also has an effect on the size of the animals. If Gammarus duebeni is reared at salinities of 2, 10, and 30, it shows a maximal body size at a value of 10 psu. With respect to the effect on respiration, it would seem that all species show a decrease in respiration that is more or less reversible, when salinity increases. This phenomenon does not depend on the salinity limits between which the species live in nature (Dorgelo, 1973). Salinity tolerance is of great importance in the ecological distribution of species, even beyond the major categories mentioned above. This aspect often explains the details of the species’ actual dispersal. Mills & Fish (1980) studied the distribution of two species of Corophium, Corophium arenarium and Corophium volutator in Wales. Corophium arenarium is more tolerant towards high salinities, as it tolerates values up to 45; the species lives predominantly in sand (2% mud). Corophium volutator rather tolerates low salinities, which can go down to 10 or even to 2; it lives in muddy sand (32% mud). Corophium arenarium thus lives in habitats only rarely covered by the water at a salinity lower than 10, while Corophium volutator develops there but can also thrive in zones where the salinity drops down to a value of 2. Corophium arenarium prefers less muddy substrates than Corophium volutator, that have a lower capacity to retain water, in which evaporation is easier, and hence evoke an increase in interstitial salinity. Mills & Fish (1980) believe that granulometry can not explain the distribution of these two species all by itself, but they do consider that salinity, and especially the interaction granulometry-salinity-temperature, can explain this distribution very well. Fanini et al. (2010) compared populations of Talitrus saltator from the Baltic (brackish water) with those from the Mediterranean (strongly saline) and demonstrated variations in behaviour according to the salinity of the environment, and such independent of the population from which the specimens originated.

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Another study has been performed on a population of Gammarus marinus in the Mondego estuary (Portugal), covering one year. A model of the development of the population showed that density was strongly affected by lower salinities (25% total body). 0 = No. 1 = Yes. 3, Rostrum shape. 0 = Rounded. 1 = Bifurcate. 2 = Acute/elongated. 3 = Concave/absent. 4 = With multiple spines. 5 = Square. 4, Eyes. 0 = Well developed. 1 = Eye lobes without visual elements. 5, Eye lobes with apophyses. 0 = Yes. 1 = No. 6, Pereonites with acute lateral apophyses. 0 = No. 1 = Yes. 7, Pleon shape. 0 = Narrower than pereon. 1 = As wide as pereon. 8, Pleon length. 0 = Long (>25% total body). 1 = Short (