Jawless Fishes of the World : Volume 2 [1 ed.] 9781443892407, 9781443887199

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Jawless Fishes of the World

Jawless Fishes of the World: Volume 2 Edited by

Alexei Orlov and Richard Beamish

Jawless Fishes of the World: Volume 2 Edited by Alexei Orlov and Richard Beamish This book first published 2016 Cambridge Scholars Publishing Lady Stephenson Library, Newcastle upon Tyne, NE6 2PA, UK British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Copyright © 2016 by Alexei Orlov and Richard Beamish and contributors All rights for this book reserved. No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior permission of the copyright owner. ISBN (10): 1-4438-8719-6 ISBN (13): 978-1-4438-8719-9

TABLE OF CONTENTS

Volume 1 Preface ........................................................................................................ ix M. Docker Part 1: Evolution, Phylogeny, Diversity, and Taxonomy Chapter One ................................................................................................. 2 Molecular Evolution in the Lamprey Genomes and Its Relevance to the Timing of Whole Genome Duplications T. Manousaki, H. Qiu, M. Noro, F. Hildebrand, A. Meyer and S. Kuraku Chapter Two .............................................................................................. 17 Molecular Phylogeny and Speciation of East Asian Lampreys (genus Lethenteron) with reference to their Life-History Diversification Y. Yamazaki and A. Goto Chapter Three ............................................................................................ 58 Ukrainian Brook Lamprey Eudontomyzon mariae (Berg): Phylogenetic Position, Genetic Diversity, Distribution, and Some Data on Biology B. Levin, A. Ermakov, O. Ermakov, M. Levina, O. Sarycheva and V. Sarychev Chapter Four .............................................................................................. 83 Diversity and Distribution of the Hagfishes and Lampreys from Chilean Waters G. Pequeño and S. Sáez Chapter Five .............................................................................................. 94 Hagfishes of Mexico and Central America: Annotated Catalog and Identification Key A. Angulo and L. Del Moral-Flores

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Chapter Six .............................................................................................. 126 The Structure and Taxonomy of the Gill Pore in Lampreys of the Genus Entosphenus R. Beamish Chapter Seven.......................................................................................... 154 Review of Western Transcaucasian Brook Lamprey, Lethenteron ninae Naseka, Tuniyev & Renaud, 2009 (Petromyzontidae) S. Tuniyev, A. Naseka and C. Renaud Chapter Eight ........................................................................................... 191 A Nonparasitic Lamprey Produces a Parasitic Life History Type: The Morrison Creek Lamprey Enigma R. Beamish, R. Withler, J. Wade and T. Beacham Chapter Nine............................................................................................ 231 Description of the Larval Stage of the Alaskan Brook Lamprey, Lethenteron alaskense Vladykov and Kott 1978 C. Renaud, A. Naseka and N. Alfonso Chapter Ten ............................................................................................. 251 The Need for a New Taxonomy for Lampreys A. Kucheryavyy, I. Tsimbalov, E. Kirillova, D. Nazarov and D. Pavlov Part 2: Ecology and Life History Chapter Eleven ........................................................................................ 280 Distribution and Habitat Types of the Lamprey Larvae in Rivers across Eurasia D. Nazarov, A. Kucheryavyy and D. Pavlov Chapter Twelve ....................................................................................... 299 The Potential Roles of River Environments in Selecting for Streamand Ocean-Maturing Pacific Lamprey, Entosphenus tridentatus (Gairdner, 1836) B. Clemens, C. Schreck, S. Sower and S. van de Wetering Chapter Thirteen ...................................................................................... 323 The Formation of Fecundity in Ontogeny of Lampreys Yu. Kuznetsov, M. Mosyagina and O. Zelennikov

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Chapter Fourteen ..................................................................................... 346 Advances in the Study of Sea Lamprey Petromyzon marinus Linnaeus, 1758 in the NW of the Iberian Peninsula S. Silva, S. Barca and F. Cobo

Volume 2 Part 3: Demography, Stock Assessment, Fisheries and Conservation Chapter Fifteen ............................................................................................ 2 Lampreys in Central Europe: History and Present State L. Hanel and J. Andreska Chapter Sixteen ......................................................................................... 32 Distribution of Arctic and Pacific Lampreys in the North Pacific A. Orlov and A. Baitaliuk Chapter Seventeen ..................................................................................... 57 Trends in the Catches of River and Pacific Lampreys in the Strait of Georgia J. Wade and R. Beamish Chapter Eighteen ....................................................................................... 73 Trends of Pacific Lamprey Populations across a Broad Geographic Range in the North Pacific Ocean, 1939-2014 J. Murauskas, L. Schultz and A. Orlov Chapter Nineteen ....................................................................................... 97 Observations on the Catch and Biology of Hagfish (Eptatretus stoutii) from an Exploratory Fishery in Northwest Mexico F. Márquez–Farías, R. Lara–Mendoza, O. Zamora–García and E. Ramírez–Félix Chapter Twenty ....................................................................................... 115 Sea Lamprey Fisheries in the Iberian Peninsula M. Araújo, S. Silva, Y. Stratoudakis, M. Gonçalves, R. Lopez, M. Carneiro, R. Martins, F. Cobo and C. Antunes

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Chapter Twenty One................................................................................ 149 Insights Gained through Recent Technological Advancements for Conservation Genetics of Pacific Lamprey Entosphenus tridentatus J. Hess Chapter Twenty Two ............................................................................... 160 Developing Techniques for Artificial Propagation and Early Rearing of Pacific Lamprey Entosphenus tridentatus for Species Recovery and Restoration R. Lampman, M. Moser, A. Jackson, R. Rose, A. Gannam and J. Barron Part 4: Species Interactions Chapter Twenty Three ............................................................................. 196 Common Behavioral Adaptations in Lamprey and Salmonids E. Kirillova, P. Kirillov, A. Kucheryavyy and D. Pavlov Chapter Twenty Four ............................................................................... 214 The Silver Lamprey and the Paddlefish P. Cochran and J. Lyons Chapter Twenty Five ............................................................................... 234 Relationships between Pacific Lamprey and Their Prey A. Orlov In Memoriam: Dr. Philip A. Cochran (1955-2015) ................................. 286 J. Lyons In Memoriam: Dr. Sako B. Tuniyev (1983-2015) ................................... 304 B. Tuniyev In Memoriam: Dr. Yuriy K. Kuznetsov (1937-2015) .............................. 318 N. Bogutskaya, A. Naseka, K. Fedorov and O. Zelennikov List of Reviewers..................................................................................... 323 List of Contributors ................................................................................. 325

PART 3: DEMOGRAPHY, STOCK ASSESSMENT, FISHERIES AND CONSERVATION

CHAPTER FIFTEEN LAMPREYS IN CENTRAL EUROPE: HISTORY AND PRESENT STATE LUBOMIR HANEL AND JAN ANDRESKA Introduction Lampreys do not belong to the groups of vertebrate animals in Central Europe (an area of about 1 million sq km) (Fig. 15-1, centerfold, page i), examined in detail in the past, in particular due to their cryptic way of life (larvae are sediment dwellers) and relative minor economic importance. Some partial historical information is only known from Poland (Cios 2007, 2014), Germany (Thiel et al. 2005; Fullner et al. 2009) and Bohemia (present-day Czech Republic); more important economic value of lampreys was registered in Poland and from other countries around the Baltic Sea (Stora, 1978; Sjoberg, 2011). Nevertheless, there are relatively few historical sources, both about their presence and abundance. Only in the last decades, the attention has been shifted to this ancient group of vertebrates, mainly in the context of increased interest of biologists in protection of biodiversity. Two anadromous species of lampreys (Lampetra fluviatilis and Petromyzon marinus), a parasitic potamodromous (Eudontomyzon danfordi) and three potamodromous non-parasitic species (Lampetra planeri, Eudontomyzon mariae and Eudontomyzon vladykovi) were recorded in Central Europe. Besides other Central European countries (Austria, Germany, Hungary, Liechtenstein, Poland, Slovakia and Switzerland), attention was paid especially to the region of Bohemia, which is sometimes called “the roof of Europe” since its only sources of water are atmospheric rain and snowfall. All the rivers which have their source in the area drain into neighboring countries. Parts of three river basins (the Elbe, the Oder and the Danube river basins) are located in the Czech Republic (Fig. 15-1, centerfold, page ii).

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3

Historical importance of lampreys Historical information has been obtained by studying various historical files and works, from catch records and from fish collections in museums (Hanel 1996c; Witkowski & Kotusz 1998b). Only fragmentary and often non-specific references are known about the occurrence of lampreys and their utilization by man in Central Europe. Catches of lampreys were probably never too frequent in Central Europe, they played a significant role only in Poland in the river Vistula, especially from autumn till early spring. Nevertheless numerous recipes for their preparation were published in cookery books and manuscripts. Presumably the oldest known record evidencing the presence of lampreys in Central Europe is in a rhymed verse dictionary called Glossary (dated about 1360) by Master Bartholomew of Chlumec, also called Claret (Magister Bartholomaeus de Bohemarius Solencia dictus Claretus (cca 1320-1370). The works of Master Paulus de Praga (1413-1471) also contain notable mentions of lamprey. A brief description of the lamprey body is presented in a Latinwritten encyclopedic Book of Twenty Arts originating in the middle of the 15th century (Flajshans 1926, 1928). Another author, Georg Handsch von Limus (1529-1578), described three lamprey species (sea lamprey, river lamprey and European brook lamprey) in his unfinished work Historia naturalis. He also mentioned the absence of bones in lampreys, parasitism on salmon and culinary use. He pointed out stomach disorders or poisonings as a consequence of the incorrect cooking of lampreys. The mucus and serum of lampreys were considered toxic (Handsch von Limus 1933). Indeed, even German biologist Marcus Elieser Bloch (1785) warned against eating of "summer" lampreys, which are not tasty, while he recommended "winter" individuals. Daniel Adam of Veleslavin (1546-1599), in his dictionary Nomenclator quadrilinguis issued in one volume, better known as Silva Quadrilinguis (1598) also describes the lampreys. Bohuslav Balbinus (1621-1688) dealt with Bohemian ichthyofauna including lampreys. In his major work (Miscellanea Historica Regni Bohemiae) published in Latin, he provided information about lamprey, including a number of specific habitats in this country (Balbinus 1679-1687). In his school textbook Orbis sensualium pictus (published in Germany in 1658), Jan Amos Comenius (1592-1670), called „The Teacher of Nations“, presented also lamprey as typical water animal (Comenius 1658). A remarkable record is related to 1700, when Herman Jakub Czernin (1659-1710), who served for some time as Chief burgrave of the Kingdom of Bohemia, bought pisces lampretam from Cologne for his wife Maria Josefa (Teply 1937). Detailed

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scientific information about lampreys, including determination, descriptions and habitats, can be found in the publications of famous Czech zoologist Antonin Fric (1832-1913), who was the last who personally experienced and described spawning migrations of sea and river lampreys in Bohemia. Sea lamprey had been found there in various fish traps (especially wooden wicker baskets), or attached on different subjects in water in the past (Fric 1872). Fric (1908) believed that the sea lamprey reached Prague (the city on the river Vltava, the Elbe river basin) sucked on tug boats drawn from the port of Hamburg (Germany) or on salmon. He noted that lampreys sold in the markets caused antipathy among buyers due to their toothed oral disc. Spawning grounds of the sea lamprey were documented up to 850 km from the mouth of the river Rhine in Germany. Sea lampreys reached South Bohemia (to the town of Pisek) via the river Elbe and then its tributary the river Vltava. This route covered a distance of 1035 km from the mouth of the river Elbe. It is the longest known migration route undergone by lampreys into the heart of the European continent. As mentioned above, the lampreys played a relatively important role in the Bohemian gastronomy in the past. River lampreys were probably consumed for a long time in the Elbe and Vltava river basins. Lampreys were mentioned in the writings of Master Pavel Zidek (Paulus de Praga or Paulerinus, 1413-1471). The first direct record of the consumption of lampreys is written in Czech in Spravcovna (1471), in which master Paulus de Praga wrote a popular guide to governance (including appropriate meals) for King George (George of Podebrady, 1420-1471). An order of 600 pieces of river lamprey as food in the lenten period for the court of Ferdinand of Tirol (1529-1595) in Austrian Innsbruck was documented in 1572 (Grossingova 1993). The first specific recipes, handwritten or printed, relating to Elbe lampreys were recorded in the 15th and 16th centuries. Various ingredients, such as cinnamon, cloves, ginger, pepper, cumin, mace, small raisins, saffron, almonds, honey and gingerbread played a very important role in preparing meals from lampreys. Red wine was a replaceable component used in lamprey cooking. Lampreys were cooked in sauce, smoked, pickled in brine or vinegar and jellied or just salted. Lamprey grilling over charcoal is still popular in some European regions. Recipes for lamprey cooking in cookbooks have gradually completely disappeared. This coincided with the demise of anadromous lampreys migrating to the Czechian waters. Besides being used in gastronomy, brook lampreys (larvae as well as adults) have been used as bait in commercial or sport angling for a long time (see reports from earlier times within Czechian territory). The European eel (Anguilla anguilla), the chub

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5

(Squalius cephalus) or the burbot (Lota lota) were often successfully caught by anglers in this way (Bubenicek 1898). Occurrence of lampreys in Central Europe The distribution of six lamprey species in river basins reaching to Central Europe is presented in Table 15-1. Table 15-1. The occurrence of lampreys in Elbe, Oder and Danube River Basins within Central Europe Elbe River Basin

Oder River Basin

Danube River Basin

Sea lamprey (Petromyzon marinus)

+

+

-

River lamprey (Lampetra fluviatilis)

+

+

-

European brook lamprey (Lampetra planeri)

+

+

+

-

+

+

-

-

+

-

-

+

Species

Ukrainian lamprey (Eudontomyzon mariae) Vladykov´s lamprey (= Danubian brook lamprey) (Eudontomyzon vladykovi) Carpathian brook lamprey (Eudontomyzon danfordi)

Anadromous lampreys Sea lamprey (Petromyzon marinus) The sea lamprey has never been a commercial species in the Baltic Sea. However, it is commercially important in Western Europe, France, Spain and Portugal (Maitland & Campbell 1992). The sea lamprey has been found since the past to the present in Poland and Germany. The oldest sea lamprey record dating back to the year 1855 is known from the Greifswald Bodden (54° 13ƍ 22Ǝ N, 13° 32ƍ 48Ǝ E, Pommeranian Coast,

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Chapter Fifteen

south of the island Ruegen) in the Southern Baltic Sea. The analysis of relevant records resulted in 11 observations of sea lamprey in the considered area in the time period from 1855 to 1939. From 1940 to 1989, sea lamprey was recorded 29 times. Fourteen records of sea lamprey were obtained in German and adjacent Polish waters in the 1990 to 2005 period (Thiel et al. 2009). One specimen of the sea lamprey (57 cm in length) was captured in the river Vistula in 1963 (a 15 cm-long dace Leuciscus leuciscus was found in its alimentary canal, see Penczak 1964), its catches in 1999-2001 are also known from the Szczecin Lagoon (53° 48ƍ 16Ǝ N, 14° 8ƍ 25Ǝ E) and the Dabie Lake (53° 27ƍ 57Ǝ N, 14° 39ƍ 11Ǝ E) (Raczynski et al. 2004). Kazmierczak (1965) describes that he was attacked while swimming by the sea lamprey (the length of about 70 cm) near the Ustronie Morskie (54° 12ƍ 55Ǝ N, 15° 45ƍ 17Ǝ E) (Polish seaside). Jokiel (1983) presents that only a few sea lamprey specimens with a length of 90 cm and a weight of 2 kg were observed in catches in the Vistula Bay (54° 27ƍ 0Ǝ N, 19° 45ƍ 0Ǝ E) and the Gdansk Bay (54° 22ƍ 50Ǝ N, 18° 39ƍ 30Ǝ E) in several years. The sea lamprey was caught in the river Rega flowing into the Baltic Sea in 2012. This is the first record of sea lamprey from the Polish coastal rivers (Skora et al. 2014). There is only sparse data on the distribution (spatial as well as seasonal) of sea lamprey in the German part of the North Sea because this species is caught only accidentally by commercial fisheries or scientific fishing surveys. According to historical references from around 1900, sea lamprey seemed not to be abundant in the catchments of the rivers Ems, Weser, Elbe and Eider and, as a result, was characterized as “rare”. The occurrence (or spawning) of this species was also documented for several major tributaries in the tidal reaches of the above-mentioned rivers. Meanwhile, by the 1980s the sea lamprey had become almost extinct in the northern German tributaries to the North Sea, due to heavy water pollution (especially in the estuaries), building of migration barriers and the alteration of water courses in the adjacent river systems. However, since 1995 the stocks of sea lamprey have remarkably increased again (especially in the catchment of the tidal part of the river Elbe), probably due to the improved water quality following the political changes in Central Europe after 1990 (the rivers Elbe and Weser) and the restoration of water courses (e.g. the improvement of fish passage facilities) following the commencement of the programme for management of water courses of Lower Saxony in 1992 (Curd 2009). The breeding of sea lamprey in Lower Saxonian rivers was described by Meyer & Beyer (2002) whereas Curd (2009) described breeding in the river Treene (the tributary of the river Eider). Rare occurence of sea lamprey was noticed in the Rhine

Lampreys in Central Europe: History and Present State

7

catchment area (the region of Hessen) in 1999 (Anonymus 2003). On the base of historical reports, Petermeier et al. (1996) confirmed the occurrence of the sea lamprey in the middle reaches of the river Elbe before the year 1900, and also later in the first half of the 20th century, but not yet in the period 1980-1993. After 1960, the species was registered in the tidal part of the river Elbe . Sea lamprey was also observed in artificial fish passes in the tide weir in Geeschacht (more details in the paragraph regarding the river lamprey). The estimated by-catch of the sea lamprey by commercial fyke netting in the tidal area of the Elbe River near Hamburg reached approximately 500 specimens on average. Spawning ascent and/or spawning is regularly documented in all major tributaries of the tidal Elbe in the federal states Lower Saxony (Oste, Schwinge, Aue-Luhe, Este, Seeve, Luhe, Ilmenau) and Schleswig-Holstein (Stor, Pinnau, Kruckau and some smaller tributaries of the Nord-Ostsee-Kanal), see Curd (2009). Sea lampreys are also annually documented in the middle reaches of the river Elbe by stow netting about 100 or 200 km respectively upstream of the tidal weir at Geesthacht (53°26ƍ17Ǝ N, 10°22ƍ29Ǝ E). Additionally, a number of not more than 100 individuals of the sea lamprey are annually documented from the known spawning sites in the tributaries of the tidal part of the river Weser (Hunte, Wumme, Ochtum, Delme). The estimated number of sea lampreys annually ascending through the estuary of the river Ems documented by stow net fishery is small (less than 100 specimens on average) compared to the estuaries of rivers Elbe and Weser, due to problems connected with temporary deficits in oxygen saturation and extremely high turbidity. There were 2227 lampreys caught in the Elbe estuary in northern Germany from 1989 to 1995. In total, 99.5% of this amount was the river lamprey and only 0,5% the sea lamprey during the whole study period (Thiel & Salewski 2003). Regarding individual findings of sea lamprey, one specimen was mentioned from the river Havola in Germany (= Havel, the tributary of the river Elbe) near Berlin (Barus & Oliva 1995). Lelek & Kohler (1989) mentioned rare findings of the sea lamprey in the river Rhine, in the river km 458.9 (Hammer Aue, 49° 43ƍ 45Ǝ N, 8° 25ƍ 50Ǝ E) in July 1988. Bubenicek (1898) wrote, that in the rivers Elbe and Vltava it is not uncommon and added that local fishermen fear of its sign of misfortune. In the past, sea lamprey arrived in the territory of the Czech Republic through the river Elbe. At the time of their migration, they were found in fyke nets and basket traps, sticking to tugs going to Bohemia from Hamburg (53° 33ƍ 1Ǝ N, 9° 59ƍ 34Ǝ E, Germany), or on salmon. The occurrence of this species has been confirmed in the rivers Elbe, Vltava and Otava as far as the town of Pisek (49° 18ƍ 32Ǝ N, 14° 8ƍ 52Ǝ E). A sea

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lamprey female was caught in the river Vltava downstream of the town of Orlik (49° 30ƍ 39Ǝ N, 14° 9ƍ 53Ǝ E) and is reported to measure 120 cm and to weigh 2.3 kg (Anonymous 1900). The last registered specimen in Bohemia was caught in the river Elbe near the town of Decin (50° 46ƍ 25Ǝ N, 14° 11ƍ 46Ǝ E) in 1902 (Oliva 1953, 1958). Two specimens (690 mm and 714 mm) are deposited in the Zoological Department of the National Museum in Prague. Nevertheless, sea lamprey can reappear in the Bohemian territory, as there are recent reports of their findings in the river Elbe at Bad Schandau (Germany, 50° 55ƍ 0Ǝ N, 14° 9ƍ 0Ǝ E) not far from the Czech border. River lamprey (Lampetra fluviatilis) Witkowski (1996a) summarized data on the occurrence of the river lamprey in Poland. This species inhabited the rivers Oder, Vistula and Elbe, as well as the many tributaries of the Baltic Sea at the beginning of the 19th century. All in all it was found in two rivers in the Elbe river basin, in 16 rivers in the Oder river basin and in 6 locations along the Baltic coast. The gradual population decline was evident in the upper stretches of the largest rivers in Poland at the end of the 19th century. After 1900, this species has not been detected in the river Oder, upper section of the river Rudawa (tributary of the river Vistula near the town of Krakow) and in middle sections of the river Vistula. According to this author this fact was caused by the contamination of water and the existence of hydro-technical structures (weirs and dams). The spawning run of the river lamprey was observed in the river Drweca (left tributary of the river Vistula) near Lubitz (53° 01' 52" N, 18° 44' 46" E), see Witkowski & Jesior (2000) and in rivers Wda and Parseta (Kuszewski & Witkowski 1995). This lamprey is mentioned in the river Grabowa by Witkowski & Kuszewski (1995). It is also known from the Dabie Lake (53° 27' 57" N, 14° 39' 11" E), connected to the river Odra estuary (Sobecka et al. 2000).A fundamental population decline was recorded in Poland in the period 1901-1975. Currently, reduced populations of river lamprey have been found only in 9 rivers and other aquatic ecosystems in Poland. River lampreys were caught to wickerwork fish basket in the lower river Vistula before the Second World War (Staff 1950) and they were mostly sold salted. The largest catches were achieved in November. The catches also declined after the construction of the dam in Wloclawek (52° 39ƍ 0Ǝ N, 19° 5ƍ 0Ǝ E) downstream of Warsaw in 1968. River lamprey were offered in the Polish town of Torun (53° 2ƍ0Ǝ N, 18° 37ƍ 0Ǝ E) till 1960s; in the 1950s there was even a larger consignment of fresh lamprey

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9

imported to Prague (50° 5ƍ 0Ǝ N, 14° 25ƍ 0Ǝ E) for sale once (Oliva 1953). While in the post-war period the catches in lower river Vistula were about 60 tons of adult river lamprey per year, at the end of the 1980s they was only 0.75-1 ton per year. Currently only sporadic specimens migrate to this river. River lampreys only rarely appear in the Baltic Sea tributaries now, and only in a few rivers. Owing to this fact, river lamprey was included in the Polish Red list, the list of fish and lampreys that are endangered in this country, in the category of strict protection (however, this applies to larvae only). The catch of the river lamprey in Germany in the 1950s was economically insignificant (Sterba 1952). Tesch (1967) recorded this species in the estuary of the river Elbe. Sterba (1962) mentioned that the annual catch in the river Rhine was in the range of 1.0 to 6.9 tons during 1910-1913. Thiel et al. (2005) registered 310 reports of total catches of almost twenty million individuals in the German waters of the southern Baltic during the period from 1649 to 2005. The number of findings per year was twice as high in the period between 1649 and 1939 than in 1940 and1998. Only 1 % of the total number of individuals was found in the period 1990-2005. An average 14 377 kg of river lamprey per year were caught in the years 1887-1999. Most individuals were caught in the Szczecin Lagoon (53° 48ƍ 16Ǝ N, 14° 8ƍ 25Ǝ E) and the adjacent waters, also in the lower section of the river Vistula, the Gdansk Bay (54° 28ƍ 59Ǝ N, 18° 57ƍ 31Ǝ E) and in the Curonian Lagoon (55° 5ƍ 34Ǝ N, 20° 54ƍ 59Ǝ E). These authors registered a total of 9 spawning places of the river lamprey, i.e. in Peene, Warnow and Stepenitz river basins. Overall, the current state of the river lamprey populations in this region is classified as critical and therefore a modification of the principles of the rescue program is needed. Lelek & Kohler (1989) mentioned findings of river lamprey larvae in the river Rhine, in river kilometer 759.8 in August 1987. Anadromous migration of ichthyofauna was monitored in artificial fish passes in the tide weir in Geeschacht on the Elbe (river km 585.9). During one year (August 2010-July 2011) 73 111 specimens of lampreys were caught here. In the total catch, the river lamprey was prevailing (72 924 individulas, i.e. over 99%), the sea lamprey was caught only sporadically (186 individuals) and very rarely the European brook lamprey was observed (one specimen only). The evident preference of the double slit pass over bypass was confirmed (from the totally caught river lamprey were 98 % found in the double slit pass), Adam et al. (2012); Adam & Neumann (2012); Schwevers & Neumann (2012). Pedroli et al. (1991) and Kirchhofer et al. (2007) summarized the occurrence of lampreys in

10

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Switzerland. The occurrence of the river lamprey there is a thing of the past. In the current territory of the Czech Republic, river lamprey occured mostly in the Elbe river drainage area. The last records of the occurrence of this lamprey species in the rivers Vltava, Divoka Orlice (the tributary of the river Orlice, the Elbe river basin) and Oder are available from the late 19th century. According to Fric (1872) the river lamprey was not abundant in the Bohemian Elbe river in the past. Bloch (1785) published an interesting detail about the catch of river lamprey in the river Oder as far as the town Bohumin (49° 54' 14 N, 18° 21' 27 E). Last direct evidence of the occurrence of river lamprey in Bohemian rivers comes from 1897 (Hanel & Lusk 2005). Nowadays, the river lamprey is not present in the Czech Republic. However, it is probable that it will reappear in the Bohemian section of the river Elbe, as there are recent reports of its findings at Bad Schandau (50° 55ƍ 0Ǝ N, 14° 9ƍ 0Ǝ E) in Germany. This fact was caused by the improvement of the permeability of the river Elbe in Germany and improvement of water quality. Although the first record of river lamprey from the river Danube dates before the first (known) stocking of eels in 1881 (Haack 1882), this species has most likely been introduced into the Danube system that way. A total of 2.4 million eels were introduced into water bodies within the area of what is now BadenWurttemberg (Germany) between 1893 and 1906 (Sieglin 1892). Assuming that 30 % of these fish went into the Danube system, and that the proportion of lamprey mixed in with the eels was 0.5 %, then approximately 4000 lamprey were accidentally introduced into this river system within 13 years. A further 1000 lampreys can be estimated to have entered the Danube in the vicinity of the city of Ulm (Germany, 48° 24ƍ 0Ǝ N, 9° 59ƍ 0Ǝ E), where eels were stocked at the beginning of the 20th century (Kappus et al. 1995). For now, these unintentional activities cannot be considered successful introduction.

Potamodromous non-parasitic lampreys European brook lamprey (Lampetra planeri) The occurrence of this species in Europe is similar to ocurrence of the river lamprey, the difference being that the brook lamprey inhabits waters which are more inland. Some authors believe that both mentioned species are an example of ancestral and satelitte-type (ecotype), see e.g. Espahnol et al. (2007); Docker et al. (2009). The European brook lamprey belongs to the most abundant species of lampreys in Central Europe. Hardisty

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11

(1986) pointed out the findings outside previously known European area (the rivers Volga, Tisa, Morava, Drava and Pescara). It is not exactly known, how this lamprey colonizes previously unocuppied river basins. Accidental introduction as attested by Kappus et al. (1995) for transmission of the river lamprey to the Danube basin is not excluded. The presence of the European brook lamprey has been confirmed in many locations in Poland, Germany and the Czech Republic (especially in the Oder and Elbe river basins). Witkowski & Kotusz (1998a) summarized the reports on occurrence of this lamprey in Polish Silesia in southwestern Poland. In the last 50 years they have confirmed it in 43 localities, including 38 in the Oder and 5 in the Elbe. The largest number of sites were registered in the left-sided tributaries of the river Oder (26) with mountain and foothill character. Right tributaries lie more in the lowlands and are also affected by improper modifications and pollution. Witkowski & Kotusz (1998b) presented the collection of specimens of the European brook lampreys (from river basins of Vistula, Oder, Elbe and Baltic coastal rivers) stored at the Museum of Natural History, Wroclaw. Obolewski (2008) studied the incidence of lamprey on the river Slupia in Slupsk (54° 28ƍ 0Ǝ N, 17° 2ƍ 0Ǝ E) and noticed regular migration to places with more natural character of the river bed. The European brook lamprey was registered in 276 German brooks and rivulets in 1999 (Anonymous 2011). The presence of this lamprey was confirmed in the Weser river catchment area (e.g. in rivers Lethe, Delme, Grosse Aue, Ilme, Schwulme, Oker, Sieber, Ortze, Lachte, Bohme, Lehrde, Wumme), in the Elbe river catchment area (e.g. in rivers Oste, Schwinge, Aue-Luhe, Este, Seeve, Luhe, Ilmenau) and in the Ems river catchment area (e.g. in rivers Hase and Dute), LAVES (2011). From the river Rhine it is mentioned by Schreiber & Engelhorn (1998), from some tributaries of the river Oder by Fechner (1851). Krappe et al. (2012) found this species within monitoring of the ichtyofauna in the MecklenburgVorpommern region (Libnower Muhlbach, Ziemenbach, Hellbach, Augraben, Kosterbeck, Tribohmer Bach, Beke, Schaale, Schwanheider Muhlbach). The closest locality to Bohemian borders is the brook Flajsky potok (Floeha) in the territory of Saxony (Kuschka & Meyer 1981). Mueller (1986) reported the occurrence of brook lamprey in 24 streams in the Saxonian Ore Mountains. In addition, its presence was cited in the river Mulde rooted in Bohemia between the towns of Teplice and Hermsdorf Frauenstein at Illigmuhle (Waterstraat 1989a). Other Saxon sites are stated by Brockhaus (1993). Lelek & Kohler (1989) mentioned its presence in the river Rhine in 1987-1988. European brook lamprey population was studied in detail in the brook Ziemenbach (Northern

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Germany) by Waterstraat (1989b). The overall map of the occurrence of the brook lamprey in Northern part of Germany is presented by Waterstraat et al. (2007). The populations of the brook lamprey are clasified in German waters in the last decade as stabilized everywhere (Freyhof 2009). European brook lamprey is within Slovakia only known from the Baltic basin (Dunajec and Poprad rivers and their tributaries), see Holcik (1970) and Kosco et al. (2006). The number of sites (11) is lower than in adjacent countries (Kosco et al. 2006). This lamprey was found in the past in the catchment area of the river Dunajec near the border with Poland (Kux & Weisz 1960), mainly in the river Poprad and its tributaries (Velicky potok, Lucivianka, Lubicky potok), see Kux & Weisz (1960); Kirka et al. (1978). Present occurrence in the river Dunajec and its tributaries was not confirmed (Kosco et al. 2006), the evidence is known only from the river Poprad catchment area (Zontag 2006). According to recent monitoring within system Natura 2000 (network of nature protected areas in the territory of European Union) in 2013-2014, the European brook lamprey was also found in following locations: the brook Beliansky potok at Spisska Bela (49° 12' 3.24" N; 20° 24' 53.28" E), the river Poprad at Spisska Teplica (49° 3' 15.48" N; 20° 16' 46.56" E) and the brook Velicky potok above Velka (49° 4' 3.36" N; 20° 15' 9.72" E). Spindler (1997) states that the occurrence of the European brook lamprey in Austria is rare. It penetrates here within the basin of the river Drau (= Drava, Drave, the tributary of the river Danube) in Lower Austria (see also Mrakovcic et al. 2006). Ratschan & Guttmann (2013) confirmed the occurence of the European brook lamprey in examined Austrian brooks nearby Czechian border (Igelbach, Schwarze Runse, Schrollenbach and Rotbach). Pedroli et al. (1991) and Kirchhofer et al. (2007) reported that the European brook lamprey is the only species of lamprey in Swiss waters nowadays. The occurrence and biology of the European brook lamprey was studied in detail in the Czech Republic. The originally very abundant occurrence of this species in this country belongs to the past. Bubenicek (1898) noted that "this lamprey is excluded from protection and it can be caught whenever and in any size". Lohnisky (1984) and Zitnan (1985) pointed out the permanent loss of populations in Eastern Bohemia due to pollution and inappropriate modifications of riverbeds and classify it as an endangered species, sensitive to pollution and decrease in oxygen content. Hanel & Lusk (2005) counted over 400 findings of the brook lamprey in the Czech Republic during 1961-2005 and therefore this species is the most common lamprey in this country. The species occurs in the Elbe and

Lampreys in Central Europe: History and Present State

13

Oder rivers drainage areas (98% of known localities). Only several isolated populations are found in the Morava river drainage area (the Danube river system), see Merta (2000). This lamprey inhabits brooks and rivulets in trout and grayling zones at the elevation of 130-895 m above sea level, but most of the findings come from 300-600 m a.s.l. Most findings were made in rather short streams less than 40 km in length. In total 2/3 of the findings were recorded in natural streams, the rest in those modified to a various extent. The stream gradient was mostly about 1.5-2 m.km-1, the prevalent annual average flow rate in the river mouth of the registered watercourses was lower than 1 m3.s-1. The observed abundance of larvae varied between 311 and 7067 exx. per hectare. In the Czech Republic, both sexes participate in the nest construction usually in shady areas of streams that are 1-8 m in width and a few centimeters to 0.8 m in water depth. The spawning occurs usually in May/June in the water temperatures 9-19.5 °C. The actualized saprobic index (Si), i.e. indication of the level of organic pollution, using analyzes of diatoms and benthos from water streams inhabited by the brook lamprey, was calculated. Its value was calculated as Si = 1,3 (indicator weight = 4, oligosaprobic zone - 7, ȕ-mezosaprobic zone - 3), Hanel (1997). It turned out that this lamprey larvae can survive even a water pollution accident when other ichtyofauna die. Such example was observed in detail in the creek Polanka (Central Bohemia, Sazava/Elbe river basin, 49° 41ƍ 51ƎN, 14° 51ƍ 14Ǝ E) in 1992. At that time the quantity of oil substances in water reached values of 0.3 mg.l-1 and content in the upper layers of bottom sediments ranged between 155 to 363 mg.l-1 (Hanel 1996a, 1996b, 2004). Ammocoetes of this species survived because of their cryptic way of life, as they are continuously buried in soft sediments of the creek bed during their larval stage. The lamprey still exists in the brook Polanka (ammocoetes were confirmed there in 2014 as well). The strategy of larvae during water pollution is therefore to remain in the substrate as long as possible. Only if toxicants penetrate into the substrate, then the larvae leave it and tend to get in more convenient locations (Hanel, own observations). The brook lamprey seems to be a good bioindicator with respect of long-term good quality of water environment, but its larvae can sometimes survive shortterm pollution.

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Ukrainian lamprey (Eudontomyzon mariae) and Vladykov´s lamprey (Eudontomyzon vladykovi) Some authors did not distinguish the taxon Eudontomyzon vladykovi as a valid species (e.g. Renaud 1982; Holcik & Renaud 1986; Vida 1993; Barus & Oliva 1995; Holcik 1995, 1996; Salewski et al. 1995; Holcik & Soric 2004; Kosco et al. 2006; Levin & Holcik 2006; Ahnelt 2008); others accepted this lamprey as a separate valid species (e.g. Balon 1966; Oliva & Hrabe 1968; Kottelat 1977; Freyhof & Brooks 2011; Eschmeyer 2014). According to Froese & Pauly (2014), this species is questionably a junior synonym of Eudontomyzon mariae (Berg, 1931) or in subspecies taxonomic category. They state that more studies are required. The newest opinions accept E. vladykovi as a valid species (Eschmeyer 2014). Nevertheless a detailed study of these taxa is necessary, especially within Central Europe. Considering many authors did not distinguish between these species in the past, there has been only little sufficiently detailed information about the variability of morphometric characters, occurrence and genetics (see Lang et al. 2009) separately for either taxa so far. The presumptive area of distribution of the Vladykov´s lamprey includes upper and middle Danube drainage: the Sava and Drava systems (Majer 2001) and the upper Danube north and west of the Drava (Holcik & Delic, 2000), locally in the Timis and Olt systems (lower Danube drainage), see Freyhof & Kottelat (2008). The area of distribution of the Ukrainian lamprey would then include tributaries of the Baltic Sea (the Odra, Vistula, Neman drainages), the northern Black (the Danube to Kuban drainages) and Caspian Seas (the rivers Sura, Volga drainage). In the Danube, its occurrence is restricted to tributaries below the Iron Gate, a gorge on the Danube forming the boundary between Serbia and Romania (Freyhof 2013c). In Poland, the Ukrainian lamprey is reported in several tributaries in the basin of the Vistula (Oliva & Hensel 1962; Wikowski & Kotusz 1998b; Nowak et al. 2010), it is also known in the river Oder; the river Lososna is the only single locality within the Neman river basin (Rembiszewski & Rolik 1975; Witkowski 1996b; Drag-Kozak 2011). Witkowski (1996b) summarized the findings in detail about the current occurrence in Poland. Ukrainian lamprey belongs among the least common there and it is characterized by low abundant population. Marszal (2001) assumed its spreading in Poland in recent decades. The Vladykov´s lamprey was found in the river Czarna Orawa in Poland (Balon & Holcik 1964; Rembiszewski & Rolik 1975; Augustyn & Nowak 2014). The Ukrainian lamprey was presented in the Szigetkoz (Little Schutt Island) section of the river Danube in Western Hungary (Vida 1993; Col.

Lampreys in Central Europe: History and Present State

15

aut. 2010). This species has been found also in the river Drava, nearby the mouth of the river Mur (Mura), see also Sallai & Kontos (2005). The occurrence of this species in the river Tisa is mentioned by the WWF (2002). Spindler (1997) and Gumpinger et al. (2011) summarized findings in Austria. Historical occurrence was known in the federal states of Burgenland, Lower and Upper Austria, Vienna, Salzburg, Tyrol, Carinthia and Styria. The current occurrence is known only from Carinthia, Styria and Lower Austria. It is recorded in the basin of the Drava. Ratschan (2015) newly discovered the presence of the Ukrainian lamprey in the Austrian river Pfuda (the Danube river basin). Kaufmann et al. (1991) completed the current state of knowledge of such occurrence from the upper section of the river Mur between the villages of Stadl and Bruck. It is found also in the river Salzach (Schmall & Ratschan 2011). The Vladykov´s lamprey is presented in the river Inn (Reichholf 1989). Freyhof (2013c) cited a single record of the Ukrainian lamprey from the upper Morava river system (Czech Republic). Nevertheless Freyhof & Kottelat (2008) previously presented the same population as E.vladykovi. Therefore verification of taxonomic position of this single isolated population on the periphery of the area of its distribution (the brook Racinka, 50º 02' 03'' N, 17º 01' 58'' E, elevation 406 m above sea level) is needed (taxonomic status of this population was usually designated as E.mariae in papers of Czech ichtyologists, see Hanel & Lusk 2005; Lusk et al. 2008, 2011). However, such a more detailed study of morphometrical variability and genetical characteristics is excluded due to the fact that it is an extremely small successively disappearing population. Since the detection of this lamprey in 1968, its population has significantly decreased over the next decades. The original population was distributed throughout a 2 km reach of the brook. In 1999 and 2000, the larvae of this species were found only in a 700 m long section. The state of the population was evaluated as critical with a high probability of extinction (in the examined section of the brook Racinka only about 50 larvae were estimated). The causes for this negative development include inappropriate streambed modifications, abundant brown trout (Salmo trutta m. fario) populations and the presence of insurmountable migration barriers. Some larvae and adults have been carried downstream to less suitable environments during floods and the adults cannot migrate back to the upper sections of this brook. Impermeable migration barriers divide the small lamprey population into several smaller and isolated parts. The critical situation of the population is further intensified by the high instability of sediments, which are the micro-habitat of larvae of this lamprey. The revitalization measures taken in 2004-2005 turned out to be

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insufficient for the expected development of the population (Lusk et al. 2008). The Ukrainian lamprey is quite abundant and widespread in many rivers in Slovakia. Barus & Oliva (1995) summarized its findings in following rivers: the Danube and its branches from Bratislava to confluence with the river Ipel, upper reaches of the Ipel, upper reaches of the river Hron from Bacuch (48° 51' 26" N, 19° 48' 27" E) to Banska Bystrica (48° 44' 8" N, 19° 8' 45" E) and its tributaries (Bystrica, Rohozna, Slatina), upper and middle reaches of the river Vah from Hybe (49° 02' 40" N, 19° 49' 44" E) to Trencin (48° 53' 42" E, 18° 2' 30" E) and its tributaries i.e. rivers Orava (Biela Orava, Cierna Orava, Mutnanka, Hranicny Krivan, Jelesna). Further occurrence was confirmed in the river Turiec, upper reaches of the river Nitra (Nedozery 48° 49' 00" N, 18° 39' 00" E). Kux (1985) presented collections of specimens of this species mostly from the river Rudava at Velke Levare (48° 30' 11" N, 17° 0' 4" E). Ukrainian lamprey was also found within faunistical research in 20132014 in following sites: Hron at Lopej (48° 48' 51.48" N; 19° 29' 42.72" E), Rudava at Studienka (48° 30' 5.76" N; 17° 12' 23.76" E), Biely Vah at Vazec (49° 3' 28.44" N; 19° 58' 23.16" E), Hybica at Hybe (49° 2' 43.08" N, 19° 49' 46.2" E). The taxonomic validity of the Vladykov´s lamprey would have to be taken into account in regional legislation and national Red Lists. Only E.mariae is for now presented from this point of view in Central European countries (see Tab. 2). The protection category „least concern“ is suggested for the species Eudontomyzon vladykovi within Europe (Freyhof & Brooks 2011).

Potamodromous parasitic lampreys Carpathian lamprey (Eudontomyzon danfordi) The Carpathian lamprey is endemic to the Danube System (Black Sea watershed), Renaud & Holcik (1986). This species lives within Central Europe in Slovakia in the Tisa River drainage area, mostly in the Hnilec River and its tributaries, see Holcik & Soric (2004); Kosco et al. (2006). Together 68 localities with the occurrence of Carpathian lamprey is known from Slovakian waters (Kosco et al. 2006), namely from Eastern Slovakia (upper reaches of the river Hnilec and its tributaries: Topla, Ondava, Ubla, Ulicka, Okna). In Hungary, this species is limited to the rivers Tisa, Timis and Szamos (Vasarhelyi l960a, b; Harka 1997, 2006; Gyore et al. 1999, 2013; Antal et al. 2013); in the Koros drainage system it was found by Telcean et al. (2007) and Gyore et al. (2013). The nonparasitic lamprey

Lampreys in Central Europe: History and Present State

17

Lampetra (Eudontomyzon) gracilis Kux, 1965 (described from the Tisa river basin), is conspecific with the parasitic lamprey Eudontomyzon danfordi Regan, 1911 (Renaud & Holcik 1986).

Principles of lamprey protection in Central Europe Some authors have summarised the main negative factors influencing lamprey populations. Waterstraat & Krappe (1998) studied distribution and abundance of the brook lamprey in the Peene drainage (north-eastern Germany) in relation to isolation and habitat conditions. Waterstraat (1989b) investigated the influence of stream regulation on a population of the European brook lamprey in the brook Ziemenbach in Germany. Besides enhanced larvae mortality during stream regulation, the alteration of the sediment composition of the river bed was the most important impact of human activities on the European brook lampreys. Kappus et al. (1995); Hanel (1996a); Moyle et al. (2009); Foulds (2013); Maitland et al. (2014) summarized specific threats endangering lampreys. The number of identified potential threats ranges between 13 and 18. Their elimination is vital for the survival of lamprey populations. Within Central Europe, following negative factors seem to be the most important (they are not put in order according to their importance, the synergy effect is very significant): unsuitable modification of streambeds (armoring of river banks with breeze blocks, total channelization), migration barriers (weirs, steps, dams), long-term water pollution (water acidification, input of organic nutrients, thermal pollution, eutrophication), removal of muddy or sandy sediment, trampling by livestock, extremely increased flows (floods), extremely decreased water flows (minimum summer flows or incorrect operation of hydroelectrical power stations), extremely high fish stock (in particular of salmonids), predation of lampreys by water fowls. The occurrence of lamprey larvae is also influenced by destruction or relocation of muddy sediments in riverbeds due to heavy rains. Their growing intensity may probably be related to climate changes (Basilico et al. 2009).The number of different threats for each lamprey population can range between 0 and 7 in Germany (Kappus et al. 1995). Generally, the populations in the Swabian Alps area (low mountain range in BadenWuerttemberg), face an average of 3.3 identifiable threats, whereas this number is only 2.5 for the populations in the Danube headwaters area. An similar situation has also been found in the Bohemian watercourses (number of threats between 0 and 8) with the occurrence of the brook lamprey, the population of the Ukrainian lamprey in the brook Racinka is affected by 10 negative factors (Hanel, unpublished data).

Chapter Fifteen

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All observed Central European species of lampreys are included in Annexes II or III of the Bern Convention and the Habitats Directive fish species and in the category least concern (it is average rate of endangering within their European occurence), see also classification according to IUCN categories by Freyhof & Kottelat (2008) and Freyhof (2013a, 2013b, 2013c, 2013d). In some countries, (or their internal regions) special Acts of nature conservation or Red Lists with registers of endangered species (Austria, Czech Republic, Hungary, Poland, Slovakia, Germany) classified to various categories exist (see Table 15-2). The Vladykov´s lamprey is not accepted in the presented Red Lists. Table 15-2. Various categories of endangering of lamprey species in Red Lists of countries in the Central Europe. Explanatory notes: Ex – extinct, CR – critically endangered, EN – endangered, VU – vulnerable, NT – near threatened, ż – the species is not included. Used following literary sources: Austria (A) – Wolfram & Mikschi (2007); Czech Republic (CR) – Lusk et al. (2011); Germany (G) – Wolter et al. (2003, 2005); Hungary (H) – Guti (1995); Poland (P) – Witkowski et al. (2009); Slovakia (Sl) – Kosco & Holcik (2008); Schwitzerland (Sw) – Kirchhofer (2007). Species

A

CR

G

H

P

Sl ż

Sw

Petromyzon marinus

ż

EX

EN

ż

CR

ż

Lampetra fluviatilis

ż

EX

EN

ż

CEN ż

EX

Lampetra planeri

EN

EN

EN

ż

VU

EN

EN

Eudontomyzon mariae

VU

CR

ż

EN

VU

VU

ż

Eudontomyzon danfordi

ż

ż

ż

EN

ż

NT

ż

The basic protection principles of the management of localities with the presence of potamodromous lampreys in Central Europe can be defined as follows: Ɣ Preserve the natural watercourse, including the riparian vegetation. Besides the sandy gravel bottom in the stream bed there must also be places with fine muddy sediments. Ɣ Maintain the diversification of stream water velocity (usual current velocity within the range of 0.1–0.5 m.s-1, maximum up to 0.8 m.s -1). The current speed in places above the alluvial deposits with the occurrence of larvae should be 0.3-0.5 m.s-1. Higher water velocity

Lampreys in Central Europe: History and Present State

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increases the probability of unstable sediments. Ɣ Ensure continuous water flow throughout the year, even in the dry season (keep the minimum residual flow). Ɣ Keep downstream and upstream migration permeability for lampreys in the watershed. If transverse flow obstacles are inevitable, prefer boulder chutes or bypasses. Ɣ Changes to the stream bed, including the removal of deposits, are acceptable only as the last resort, particularly in the context of flood control and restoration of the watershed after the flood. Such cases require rescue transfer of ammocoetes (electrofishing repeated 3–5 times, see Hanel & Mueller 1997). Ɣ Maintain the required water quality (oligotrophic to beta – mezosaprobic class of water quality, the average value of BOD5 (biochemical oxygen demand in 5 days) is approximately 4). Ɣ Do not tolerate long-term pollution by organic substances (Hanel 1996a, b, 2004). Biodiversity and its protection has become an important topic of the present time on both the global and regional (country) scale. In Central Europe, it is the lampreys that are considered an endangered vertebrate group. All Central European countries (excluding Liechtenstein remaining outside the European Union) created sites in the Natura 2000 network of protected European sites. The project’s focus has been the conservation of rivers or brooks identified as Special Areas of Conservation (SACs) and of relevant habitats and species listed in Annexes I and II of the European Union Directive on the Conservation of Natural Habitats and of Wild Fauna and Flora (92/43/EEC) (the Habitats Directive). Each of countries has to guarantee using this network of special areas of conservation and sustaining prosperity of populations of individual lamprey species. The summary of some LIFE nature projects focusing on lampreys (Eudontomyzon ssp., Lampetra fluviatilis, Lampetra planeri and Petromyzon marinus) with respect to Central Europe is presented by Silva et al. (2015). This financial instrument for the environment is among others focused also on improving of overall condition of river systems and increasing of populations of selected fishes and lampreys.

References Adam B. & Neumann Ch. 2012. Equipment for monitoring of fish migration in the double slit pass in Geesthacht. WasserWirtschaft 102, 44–48 (In German).

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Adam B., Faller M., Gischkat S., Hufgard H., Lowenberg S. & Mast M., 2012. Results after one year fish ecological monitoring on the double slit pass in Geesthacht. WasserWirtschaft 102, 49–57 (In German). Adam z Veleslavina D. (Adam from Veleslavin) 1598. Sylvia quadrilinguis vocabulorum et phrasium bohemicae, latinae, greacae et germanicae linguae. (Quadrilingual dictionary in Czech, Latin, Greek and German.) Praha: Nakladem Vlastnim. Ahnelt H. 2008. Identification key to fishes of Austria. Accessed on the internet at http://homepage.univie.ac.at/harald.ahnelt/Harald_Ahnelts_Homepage/ Publications_files/Bestimmungsschluessel.pdf on 19 December 2014. (In German). Anonymous 1900. Mihule morska (Sea lamprey). Vesmir 29, 238 (In Czech). Anonymus 2003. Species characteristics, Petromyzon marinus. Giessen: Hessen–Forst FENA, Naturschutz (In German). Anonymous 2011. Artensteckbriefe der relevanten Arten des Natura 2000Gebietes DE-4614-303 Ruhr Stand August 2006. Wiehl: pbs planungsbüro schumacher (In German). Antal L., Halasi-Kovacs B. & Nagy S.A. 2013. Changes in fish assemblage in the Hungarian section of River Szamos/Somes after a massive cyanide and heavy metal pollution. North-Western Journal of Zoology 9, 131-138. Augustyn L. & Nowak M. 2014. Fish fauna of the Polish part of the Czarna Orawa catchment. Scientific Annual of the Polish Angling Association 27, 51-78 (In Polish). Balbinus B. 1679-1687. Miscellany of Bohemian history. Praha: Nakladem Vlastnim (In Czech). Balon E. 1966. Fishes of Slovakia. Bratislava: Obzor (In Slovak). Balon E.K. & Holcik J. 1964. Several new species of lampreys and fishes in the Danube River Basin (Black Orava). Fragmenta Faunistica (Warszawa) 11, 189-206 (In Polish). Barus V. & Oliva O. (eds.) 1995. Lampreys and fishes 28/1. Praha: Academia (In Czech). Basilico L., Massu N. & Seon-Massin N. 2009. Climate change, impacts on aquatic environments and consequences for management. Summary of the 29-30 June Seminar, ONEMA Meetings. Paris: ONEMA. Bloch M.E. 1785. Economic and natural history of German fishes. Berlin: Comission in der Buchhandlung der Realschule (In German). Brockhaus T. 1993. Reviews of watercourses in the region Chemnitz. Chemnitz: Staatliches Umweltfachamt Chemnitz (In German).

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Bubenicek J. 1898. About fishes and catching them. Praha: Nakladatelství E. Beaufort (In Czech). Cios S. 2007. Fish in the lives of Poles from the tenth to the nineteenth century. Olsztyn: Instytut rybarstwa Srodlagowego (In Polish). Cios S. 2014. Fish as an object of Polish cuisine from the sixteenth to the early twentieth century. Warszawa (In Polish). Col. aut. 2010. Feasibility study: the rehabilitation of the Szigetkoz reach of the Danube. Prepared by Hungarian section of the working group for the preparation of the joint Hungarian-Slovak strategic environmental assessment established by the governmental delegations of the Gabþíkovo-Nagymaros project. Accessed on the internet at http://www.bosnagymaros.hu/pdf/FesaibilityStudySzigetkoz.pdf on 10 December 2014. Comenius J.A. 1658. Orbis sensualium pictus (Visible world in pictures.). Nuernberg. Dortmund (reprint 1991): Harenberg Edition. Curd A. 2009. Background document for sea lamprey Petromyzon marinus. London: OSPAR Comission. Docker M.F. 2009. A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. In: Brown L.R., Chase S.D., Mesa M.G., Beamish R.J. & Moyle P.B. (eds.): Biology, management, and conservation of lampreys in North America. American Fisheries Society Symposium 72. Pp. 71-114. Bethesda: American Fisheries Society. Drag-Kozak E., Nowak M., Szczerbik P., Klaczak A., Mikolajczyk T., Falowska B., Socha M. & Popek W. 2011. New data regarding the distribution and ichthyocoenological affinities of the Ukrainian brook lamprey, Lampetra (Eudontomyzon) mariae (Cephalaspidomorphi: Petromyzontiformes: Petromyzontidae), in southern Poland. Acta Ichthyologica et Piscatoria 41, 123-127. Eschmeyer W.N. (ed.). 2014. Catalog of fishes: genera, species, references. Electronic version. Accessed on the internet at http:// research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp on 10 December 2014. Espanhol R., Almeida P.R. & Alves M.J. 2007. Evolutionary history of paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation. Molecular Ecology 16, 1909-1924. Fechner A. 1851. Knowledge of natural history of the neighborhood of Goerlitz. Vertebrate fauna. Goerlitz: Vierzehnter Jahresbericht ueber die hoehere Burgerschule zu Goerlitz (In German).

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Flajshans V. 1926. Klaret and his company. Dictionary versification. Praha: Nakladem Ceske Akademie Ved a Umeni (In Czech). Flajshans V. 1928. Klaret and his company. Annotation of texts. Praha: Nakladem Ceske Akademie Ved a Umeni (In Czech). Foulds W.L. 2013. Anthropogenic factors affecting European river lamprey Lampetra fluviatilis in the Humber River Basin, north-east England. M.S. Thesis. Durham University. Freyhof J. 2009. Red List of in freshwater reproducing lampreys and fishes /Cyclostomata & Pisces/). Naturschutz und Biologische Vielfalt 70, 291-316 (In German). Freyhof J. 2013a. Lampetra planeri. The IUCN Red List of threatened species. Version 2014.2. Downloaded on 28 October 2014. Accessed on the internet at http://www.iucnredlist.org/details/11213/0 on 10 December 2014. Freyhof J. 2013b. Lampetra fluviatilis. The IUCN Red List of threatened species. Version 2014.2. Downloaded on 28 October 2014. Accessed on the internet at http://www.iucnredlist.org/details/11206/0on 10 December 2014. Freyhof J. 2013c. Eudontomyzon mariae. The IUCN Red List of threatened species. Version 2014.2. Downloaded on 28 October 2014. Accessed on the internet at http://www.iucnredlist.org/details/8173/0 on 10 December 2014. Freyhof J. 2013d. Petromyzon marinus. The IUCN Red List of Threatened Species. Version 2014.2. Downloaded on 28 October 2014. Accessed on the internet at http://www.iucnredlist.org/details/11213/0 on 10 December 2014. Freyhof J. & Brooks E. 2011. European red list of freshwater fishes. Luxemburg: Publications Office of the European Union. Freyhof J. & Kottelat M. 2008. Eudontomyzon vladykovi. The IUCN Red List of threatened species. Version 2014.3. Downloaded on 17 December 2014. Accessed on the internet at http://www.iucnredlist.org/details/8174/0 on 17 December 2014. Fric A. 1872. Fishes of Czechia. Archiv prirodovedecky k proskoumani Cech II, 107-129 (In Czech). Fric A. 1908. Ceske ryby a jich cizopasnici. (Czech fishes and their parasites.) Praha: Nakladem vlastnim. Froese R. & Pauly D. (eds.) 2014. FishBase. World Wide Web electronic publication. Assesed on the internet at http:// www.fishbase.org. on 10 December 2014.

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Fullner G., Pfeifer M. & Zarske A. 2009. Distribution of fish species in Annex II. of Directive 92/43/EEC. Jahresschrift für Feldherpetologie und Ichthyofaunistik Sachsen 8, 3-25 (In German). Grossingova S.-M. 1993. Shadows above Habsburg throne. Praha: Knizni Klub In Czech). Gumpinger C., Ratschna C., Schauer M., Wanzenbock J. & Zauner G. 2011. The species conservation project for small fishes and lampreys is a valuable contribution to the conservation of biodiversity in the Upper Austrian waters. Part 1, General. Österreichs Fischerei Jahrgang 64, 130-144 (In German). Guti G. 1995. Conservation status of fishes in Hungary. Opuscula Zoologica (Budapest) 17-18, 153-158. Gyore K., Jozsa V., Lengyel P. & Gal D. 2013. Fish faunal studies in the Koros river system. Aquaculture, Aquarium, Conservation & Legislation International Journal of the Bioflux Society 6, 34-41. Gyore K., Sallai Z. & Csikai Cs. 1999. Data to the fish fauna of River Tisa and its tributaries in Hungary and Romania. Tiscia Monograph Series IV, 455-470. Haack H. 1882. Report of the first findings of the eel in the Danube basin. Circulare des Deutschen Fischerei Vereins im Jahre 1881, 123-125. Handsch von Limus G. 1933. Fishery in the Elbe river in Bohemia and Meissen. Prag (reprint). Hanel L. 1996a. Negative factors affecting the occurrence of lampreys. Biodiverzita Ichtyofauny CR 1, 57-61 (In Czech). Hanel L. 1996 b. The occurrence of lampreys (Cyclostomata, Petromyzontidae) in the Czech Republic. Acta Universitatis Carolinae Biologica 40, 87-97. Hanel L. 1996c. Lamprey specimens in the museums of the Czech Republic. Bulletin Lampetra 2, 23-39 (In Czech). Hanel L. 1997. Revision of the bioindicative value of lampreys in the Czech Republic. Bulletin Lampetra 3, 87-93 (In Czech). Hanel L. 2004. Ecological requirements of the brook lamprey (Lampetra planeri) and Ukrainian lamprey (Eudontomyzon mariae) in the Czech Republic. Biodiverzita Ichtyofauny CR 5, 19-24 (In Czech). Hanel L. & Lusk S. 2005. Fishes and lampreys of the Czech Republic, their occurence and protection. Vlasim: Zakladni Organizace Ceskeho Svazu Ochrancu Prirody (In Czech). Hanel L. & Mueller U. 1997. Comment on the use of electric aggregates for recording larvae of brook lamprey in water streams. Bulletin Lampetra 3, 81-86 (In German).

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Hardisty M.W. 1986. Lampetra fluviatilis (Linnaeus, 1758). In: Holþik J. (ed.) The freshwater fishes of Europe. Vol. I. Pp. 249-278. Wiesbaden: Aula-Verlag. Harka A. 1997. Our fishes. Budapest: Termeszet-es Kornyezetvedo Tanarok Egyesulete (In Hungarian). Harka A. 2006. Changes in the fish fauna of the River Tisza. Tiscia 35, 6572. Holþik J. 1970. Number and variation of trunk myomers in Lampetra planeri with regard to population from the Poprad and Hornad river basins. Biologia (Bratislava) 25, 123-128. Holþik J. 1995. Geographical distribution of lampreys (Petromyzontiformes) in middle and upper sections of the Danube river (between Austria and Black Sea).) Fischoekologie 8, 23-30. Holþik J. 1996. Vanishing freshwater fish species of Slovakia. In: Kirchhofer A. & Hefti D. (eds.) Conservation of endangered fish in Europe. Pp. 79-88. Basel: Birkhauser Verlag. Holþik J. & Delic A. 2000. New discovery of the Ukrainian brook lamprey in Croatia. Journal of Fish Biology 56: 73-86. Holþik J. & Renaud C.B. 1986. Eudontomyzon mariae (Berg, 1931) In: Holcik J. (ed.) The Freshwater Fishes of Europe. Vol. 1/I. Petromyzontiformes. Pp. 165-185. Wiesbaden: AULA-Verlag. Holþik J. & Soric V. 2004. Redescription of Eudontomyzon stankokaramani (Petromyzontes, Petromyzontidae) - a little known lamprey from the Drin River drainage, Adriatic Sea basin. Folia Zoologica 53, 399-410. Jokiel J. 1983. Lampreys in Poland. Bulletin of the Sea Fisheries Institute 75-76, 18-22. Kappus B., Jansen W., Fok P. & Rahmann H. 1995. Threatened lamprey (Lampetra planeri) populations of the Danube Basin within BadenWuerttemberg, Germany. Miscellanea Zoologica Hungarica 10, 85-98. Kaufmann T., Muhar S., Raderbauer J., Rathschuller O., Schmutz S., Waidbacher H. & Zauner G. 1991. Ecological study of fishes in the river Mur. Wien: Abteilung Hydrobiologie, Universität für Bodenkultur (In German). Kazimierczak T. 1965. Note on the sea lamprey Petromyzon marinus L. Przeglad Zoologiczny 9, 444 (In Polish). Kirchhofer A., Breitenstein M. & Zaugg B. 2007. The red list of endangered species in Switzerland. Fishes and lampreys. Bern: Herausgegeben vom Bundesamt für Umwelt BAFU und vom Schweizer Zentrum für die Kartografie der Fauna SZKF/CSCF Bern (In German).

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Kirka A., Nagy S., Zahumensky L., Libosvarsky J., Penaz M. & Krupka I., 1978. Distribution of fishes, diatom vegetation and zoobenthos in the catchment area of Hornad and Hnilec rivers. Biologicke Prace Slovenske akademie vied, Bratislava 24, 7-98 (In Slovak). Kosco J. & Holþik J. 2008. Annotated red list of lampreys and fishes in the Slovak Republic – Version 2007. Biodiverzita Ichtyofauny CR 7, 119132 (In Czech). Kosco J., Kosuth P., Kosuthova L. & Pekarik L. 2006. Present knowledge about distribution of representatives of the family Petromyzontidae in Slovakia. In Sacherova V. (ed.): Sbornik prispevku. 14 Konference. Ceske limnologicke spolecnosti a Slovenskej limnologickej spolocnosti, Nectiny 26.-30, Cervna 2006. Pp. 107-110 (In Czech). Kottelat M. 1997. European freshwater fishes. Biologia 52, 1-271. Krappe M., Boerst A. & Waterstraat A. 2012. Habitat monitoring of cyclostomes and fishes in Mecklenburg - Vorpommern region - Part 2: lampreys, spined loach, European weatherfish and European bitterling. Natur und Naturschutz in Mecklenburg-Vorpommern 41, 92-100 (In German). Kuschka V. & Meyer U. 1981. Finding of the brook lamprey (Lampetra planeri) in the Floha river. Veroeffentlichungen des Museums fuer Naturkunde Karl-Marx-Stadt 11, 99-101 (In German). Kuszewski J. & Witkowski A. 1995. Morphometrics of the autumn spring run populations of the river lamprey, Lampetra fluviatilis (Linnaeus, 1758) from the Polish rivers. Acta Ichthyologica et Piscatoria 25, 5770. Kux Z. 1985. Growth, number of trunk myomeres and oral disc in lampreys (Lampetra planeri, Lampetra vladykovi, Eudontomyzon danfordi and Eudontomyzon gracilis. Casopis Moravskeho Musea 70, 191-207 (In Czech). Kux Z. & Weisz T. 1960. Note on knowledge of the ichtyofauna in rivers Dunajec, Poprad, Vah and Hron. Casopis Moravskeho Musea 49, 191246 (In Czech). Lang, N.J., Roe K.J., Renaud C.B., Gill H.S., Potter I.C., Freyhof J., Naseka A.M., Cochran P., Perez H.E., Habit E.M., Kuhajda B.R., Neely D.A., Reshetnikov Y.S., Salnikov V.B., Stoumboudi M. Th. & Mayden R.L. 2009. Novel relationships among lampreys (Petromyzontiformes) revealed by a taxonomically comprehensive molecular data set. In Brown L.R., Chase S.D., Mesa M.G., Beamish R.J. & Moyle P.B. (eds.): Biology, Management, and Conservation of Lampreys in North America. American Fisheries Society Symposium 72. Pp. 41-55. Bethesda: American Fisheries Society.

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LAVES (The Lower Saxony State Office for Consumer Protection and Food Safety). 2011. Rewarding experience in the protection of fish species in Lower Saxony region. - Fishes in Annex II of the Habitats Directive and other fish species with priority for conservation and development activities - Brook lamprey (Lampetra planeri). Hannover: Niedersaechsische Strategie zum Arten- und Biotopschutz (In German). Lelek A. & Kohler Ch. 1989. Analysis of fish communities in the Rhine river (1987-1988) Fischoekologie 1, 47-64 (In German). Levin B.A. & Holþik J. 2006. New data on the geographic distribution and ecology of the Ukrainian brook lamprey, Eudontomyzon mariae (Berg, 1931). Folia Zoologica 55, 282-286. Lohnisky K. 1984. Changes in occurrence and species composition of the ichtyofauna of Eastern Bohemia in recent decades.) Zpravodaj Krajskeho Muzea Vychodnich Cech v Hradci Kralove, Prirodni Vedy 11, 29-108 (In Czech). Lusk S., Hanel L. & Kresina J. 2008. Is the Ukrainian lamprey Eudontomyzon mariae population in the Raci potok inevitably doomed? Biodiverzita Ichtyofauny CR 7, 6-16 (In Czech). Lusk S., Luskova V., Hanel L., Lojkasek B. & Hartvich P. 2011. The Red List of lampreys and fishes of the Czech Republic - Version 2010. Biodiverzita Ichtyofauny CR 8, 68-78 (In Czech). Maitland P.S. & Campbell R.N. 1992. Freshwater fishes of the British Isles. London: Harper Collins. Maitland P.S., Renaud C.B., Quintella B.R., Close D.A. & Docker M.F. 2014. Conservation of native lampreys. In Docker M.F. (ed.). Lampreys: Biology, conservation and control I., Fish & Fisheries Series 37. Pp. 375-417. Dordrecht, Heidelberg, New York, London: Springer. Majer J. 2001. Checklist of lamprey of Somogy county (Cyclostomata, Hyperontia: Petromyzonidae. Natura Somogyiensis 1, 437-438 (In Hungarian). Marszal L. 2001. Distribution of European brook lamprey Lampetra planeri (Bloch) and Ukrainian brook lamprey Eudontomyzon mariae (Berg) in the rivers of central Poland - the present state and the tendencies of changes. Roczniky Nauk, Polski Zwiazek Wedgarski 14, 313-319 (In Polish). Merta L., 2000. History and present of distribution of the brook lamprey (Lampetra planeri) in upper Morava river basin. Bulletin Lampetra 4, 132-141 (In Czech). Meyer L. & Beyer K. 2002. On the spawning behavior of the sea lamprey (Petromyzon marinus) in the lower reaches of the tidal influenced Luhe

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(Lower Saxony). Verhandlungen der Gesellschaft für Ichthyologie 3, 45–75 (In German). Moyle P.B., Brown L.B., Chase S.D. & Quinones R.M. 2009. Status and conservation of lampreys in California. In Brown L.R., Chase S.D., Mesa M.G., Beamish R.J. & Moyle P.B. (eds.) Biology, management, and conservation of lampreys in North America. American Fisheries Society Symposium 72. Pp. 279-293. Bethesda:. American Fisheries Society. Mrakovcic M., Brigic A., Buj I., Caleta M., Mustafic P. & Zanella D. 2006. The red book of freswater fishes in Croatia. Zagreb: Ministarstvo kulture, Drzavni zavod za zastitu prirode (In Croatian). Mueller K. 1986. Zur Verbreitung der Bachneunaugen im Bezirk KarlMarx- Stadt. (The occurrence of the brook lamprey in Karl-Marx-Stadt region.) Aquarien-terrarien 158-159. Nowak M., Szczerbik P., Klaczak A., Epler P. & Popek W. 2010. Diversity of lampreys and fishes of the Upper Vistula River drainage, Poland: present state and future challenges. Aquaculture, Aquarium, Conservation and Legislation, Bioflux, Romania 3, 325-332. Obolewski K. 2008. Lampetra planeri (Bloch, 1784) of the Slupia river in the Slupsk city area. Baltic Coastal Zone, Institute of Biology and Environmental Protection Pomeranian Academy Slupsk 12, 69-73. Oliva O. 1953. Note on the preview of native lampreys (Petromyzones Berg, 1940). Vestnik Kralovske Ceske Spolecnosti Nauk, Trida Matematicko-Prirodovedecka 9, 1-19 (In Czech). Oliva O. 1958. Finding of sea lamprey (Petromyzon marinus) in the Elbe River near the city of Decin. Vestnik Ceskoslovenske Spolecnosti Zoologicke 22, 111-112 (In Czech). Oliva O. & Hensel K. 1962. On the occurrence of the South Russian lamprey, Lampetra (Eudontomyzon) mariae Berg, 1931, in the Vistula Basin. Acta Universitatis Carolinae Biologica 1, 99-104. Oliva O. & Hrabe S. 1968. Vertebrates of Slovakia I. Fishes, amphibians and reptiles. Bratislava: Vydavatelstvo Slovenskej Akademie Vied (In Czech). Pedroli J.-C., Zaugg B. & Kirchhofer A. 1991. Atlas of the occurrence of fishes and lampreys in Switzerland. Documenta Faunistica Helvetiae II. Neuchatel: Schweizerisches Zentrum für die kartografische Erfassung der Fauna (In German). Penczak T. 1964. Report on catching Petromyzon marinus L. in the river Pilica. Die Naturwissenschaften 51, 322. Petermeier A., Scholl F. & Titizer T. 1994. Historical development of aquatic communities (zoobenthos and fish fauna) in the German

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section of the river Elbe. Koblenz: Bundesanstalt für Gewaesserkunde (In German). Raczynski M., Wawrzyniak W. & Czerniejewski P. 2004. Sea lamprey Petromyzon marinus (L.) in the Szczecin Lagoon. In Vykusova B. (ed.) Sbornik prispevku z odborne konference s mezinarodni ucasti poradane ve Vodnanech 6-7.5.2004 v ramci XIV. Vodnanskych rybarskych dnu. Pp. 30-36. Vodnany: Jihoþeská univerzita v ýeských BudČjovicích, Výzkumný ústav rybáĜský a hydrobiologický ve VodĖanech (In Czech). Ratschan C. 2015. Spawning migration and population dynamics of the Ukrainian lamprey (Eudontomyzon mariae Berg, 1831) in the river Pfuda (Inn, Upper Austria) Österreichs Fischerei 68, 19-34 (In German). Ratschan C. & Guttmann S. 2013. Electrofishing survey in potential streams with the occurence of lampreys in the Vltava river basin in the Bohemian Forest. Unpublished short report (In German). Reichholf J. 1989. Ichtyofauna of the lower section of the river Inn: an overview. Mitteilungen der Zoologischen Gesselschaft Branau 5, 107110 (In German). Rembiszewski J.& Rolik H. 1975. Lampreys and fishes. Catalog of Polish fauna. Warszawa: Polska akademia nauk, Instytut zoologii, Panstwowe wydawnictwo naukove (In Polish). Renaud C.B. 1982. Revision of lamprey genus Eudontomyzon Regan, 1911. M.S. Thesis. University of Ottawa. Renaud C.B. & Holþik J. 1986. Eudontomyzon danfordi Regan, 1911. In Holþik J. (ed.): The freshwater fishes of Europe. Vol. 1/I. Petromyzontiformes. Pp. 146-164. Wiesbaden: AULA-Verlag. Salewski V., Kappus B. & Renaud C.B. 1995. Velar tentacles as a taxonomic character in Central European lampreys. Acta Universitatis Carolinae Biologica 39, 215-229. Sallai Z. & Kontos T. 2005. Fishfaunistical monitoring of the Hungarian part of the River Drava (1999-2004). Natura Somogyiensis 7, 75-104. Schmall B. & Ratschan C. 2011. The historical and current ichthyofauna of the river Salzach - a comparison with the river Inn. Beitrage für Naturkunde Oberösterreichs 21, 55-191 (In German). Schreiber A. & Engelhorn R. 1998. Population genetics of a cyclostome species pair, river lamprey (Lampetra fluviatilis L.) and brook lamprey (Lampetra planeri Bloch). Journal of Zoological Systematics and Evolutionary Research 36, 85-99. Schwevers U. & Neumann Ch. 2012. Measures to ensure the function of fish passage in Geeschacht. WasserWirtschaft 4, 23-27 (In German).

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Sieglin H. 1892. The fishing conditions in the region of Württemberg. Württenbergische Jahrbücher für Statistik und Landeskunde 2, 65-271 (In German). Silva J.P., Toland J., Nottingham S., Jones W., Eldridge J., Hudson T., Heppner K., McGlynn D. & Thevignot Ch. 2015. Life and freshwater fish. Luxembourg: European Commission. Sjoberg K. 2011. River lamprey Lampetra fluviatilis (L.). Fishing in the area around the Baltic Sea. Journal of Northern Studies 5, 51-86. Skora M.E., Bernas R., Radtke G. & Morzuch J. 2014. Report on the sea lamprey Petromyzon marinus observation in the Rega River. Chronmy Przyrode Ojczyzysta 70, 174-177 (In Polish). Sobecka E., Moskal J. & Wiecaszek B. 2000. The state of health of the river lamprey Lampetra fluviatilis (L.) from Lake Dabie compared to the pathogens hitherto found in this host. Wiad Parazitol 56, 71-76. Spindler T. 1997. The ichtyofauna in Austria. Vol. 87. Wien: Monographien des Umweltbundesamtes (In German). Staff F. 1950. Freshwater fishes in Poland and adjacent areas. Warszawa: Trzaska, Evert i Michalski (In Polish). Sterba G. 1952. Lampreys. Leipzig: Die Neue Brehm-Buecherei, Geest und Portig (In German). Sterba G. 1962. What is to be known about lampreys. Aquarien und Terrarien 9, 103-107 (In German). Stora N. 1978. Lamprey fishing in the rivers of the Gulf of Bothnia. Ethnologia Scandinavica 1978, 67-98. Telcean I.C., Cupsa D., Covaciu-Marcov S.D. & Sas I. 2007. The fishfauna of the Crisul Repede river and its threating major factors. Pisces Hungarici I., I. Magyar Haltani Konferencia, (Supplement Kotet), Debrecen, 13-18. Teply F. 1937. Contributions to the history of Czech fish farming. Praha: Nakladem ministerstva zemedelstvi republiky Ceskoslovenske (In Czech). Tesch F.W. 1967. Activity and migration behaviour of Lampetra fluviatilis, Lota lota and Anguilla anguilla in the estuary of the river Elbe. Helgolaender Wissenschaftliche Meeresuntersuchungen 16, 92111 (In German). Thiel R., Winkler H. M., Riel P. & Neumann R. 2005. Survey of river and sea lampreys in German waters of the Baltic Sea - basis of successful rebuilding programmes. CM 2005/W:06. Copenhagen: ICES Headquarters. Thiel R., Winkler H.M., Riel P., Neumann R., Groehsler T., Boettcher U., Spratte S. & Hartmann, U. 2009. Endangered anadromous lampreys in

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the southern Baltic Sea: spatial distribution, long-term trend, population status. Endangered Species Research 8, 233-247. Thiel R. & Salewski V. 2003. Distribution and migration of lampreys in the Elbe estuary. Limnologica-Ecology and Management of Inland Waters 33, 214-226. Vasarhelyi I. 1960a. On the fish fauna of Hungary. I. The Fish Fauna of the River Tisza. Vertebrata Hungarica 2, 19-30. Vasarhelyi I. l960b. Data on the the Hungarian fish fauna. The fish fauna of the Bodrog, Kraszna and Szamos rivers. Vertebrata Hungarica 2, 163-174 (In Hungarian). Vida A. 1993. Threatened fishes in the Szigetkoz. Miscellanea Zoologica Hungarica 8, 25-34. Waterstraat A. 1989a. Studies on the fish fauna of the Eastern Ore Mountains. Naturschutzarbeit in Sachsen 31, 39-46 (In German). Waterstraat A. 1989b. Influence of river development on population of the brook lamprey Lampetra planeri (Bloch, 1784) in one lowland stream in the north of the GDR. Fischökologie 1, 29-44 (In German). Waterstraat A. &, Krappe M. 1998. Distribution and abundance of Lampetra planeri populations in the Peene drainage (NE Germany) in relation to isolation and habitat conditions. Italian Journal of Zoology 65, 137-143. Waterstraat A., Krappe M. & Wachlin V. 2007. Occurrence map for Germany, Lampetra planeri (Bloch 1784). In Nationaler Bericht der FFH-Arten, Stand: Oktober 2007. Anhang II, FFH-Code: 1096 (In German). Witkowski A. 1996a. Distribution of the river lamprey Lampetra fluviatilis (Linnaeus, 1758) in inland waters of Poland and reasons for the species decline. Bulletin Lampetra 2, 77-82. Witkowski A. 1996b. Ukrainian brook lamprey, Eudontomyzon mariae (Berg, 1931) in Poland: its distribution and present status. Bulletin Lampetra 2, 69-76. Witkowski A. & Jesior M. 2000. Fecundity of river lamprey Lampetra fluviatilis (L.) in Drweca river (Vistula basin, Northern Poland). Archives of Polish Fisheries 8, 225-232. Witkowski A. & Kotusz J. 1998a. Occurrence of the brook lamprey, Lampetra planeri (Bloch, 1784) in rivers of Polish Silesia (SW of Poland). Bulletin Lampetra 3, 73-79. Witkowski A. & Kotusz J. 1998b. The lampreys (Petromyzontidae) in the ichthyological collection of the Museum of Natural History, Wroclaw University, Poland. Bulletin Lampetra 3, 65-71.

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Witkowski A., Kotusz J. & Przybylski M. 2009. The degree of threat to the freshwater ichthyofauna of Poland: Red list of fishes and lampreys – situation in 2009. Chronmy Przyrode Ojczyzysta 65, 33-52. Witkowski A. & Kuszewski J. 1995. Characteristics of the population of Lampetra fluviatilis (L.) entering the Drweca and Grabowa rivers (North Poland). Acta Ichthyologica et Piscatoria 25, 49-56. Wolfram G. & Mikschi E 2007. The red list of fishes (Pisces) in Austria. In: Zulka, K.P. (ed.): Red List of Threatened Animals of Austria, Part 2. Green Series Ministry of Life. Vol. 14/2. Pp. 61-198. Wien, Köln, Weimar: Bohlau-Verlag (In German). Wolter C., Arlinghaus R., Grosch U. A. & Vilinskas A. 2003. Fishes and fisheries in Berlin. Zeitschrift fuer Fischkunde, Supplementum 2, 1-156 (In German). Wolter C., Arlinghaus R., Grosch U. A. & Vilinskas A. 2005. The red list and fish lists of fishes and lampreys (Pisces et Cyclostomata) in the Berlin region. In: Der Lamdesbeauftragte fuer Naturschutz und Landschaftspflege / Senatsverwaltung fuer Stadtentwicklung (Hrsg.): Rote Listen der gefahrdeten Pflanzen und Tiere von Berlin. CD-ROM. Accessed on the internet at http://www.stadtentwicklung.berlin.de/natur_gruen/ naturschutz/downloads/artenschutz/rotelisten/13_fische_print.pdf on 16 November 2014 (In German). WWF. 2002. The ecological effects of mining spills in the Tisza river system in 2000. Vienna: World Wildlife Fund. Zitnan R. 1985. Our protected and endangered fishes. Polovnictvo a Rybarstvo 37, 25 (In Czech). Zontag M. 2000. Return of fish of the genus Gymnocephalus and lampreys. Polovnictvo a Rybarstvo 52, 34-35 (In Czech).

CHAPTER SIXTEEN DISTRIBUTION OF ARCTIC AND PACIFIC LAMPREYS IN THE NORTH PACIFIC ALEXEI ORLOV AND ALEXEI BAITALIUK

Introduction The most common and abundant parasitic cyclostomes in the North Pacific are the Arctic lamprey Lethenteron camtschaticum (Tilesius, 1811) and the Pacific lamprey Entosphenus tridentatus (Richardson, 1836) lampreys (Parin 2001; Parin et al. 2014). The Arctic lamprey is an anadromous parasitic lamprey that is widely distributed in the Arctic and the North Pacific. Its range covers waters of the Arctic seas from Varanger fjord (the Barents Sea) to the Beaufort Sea. In the North Pacific, it includes areas from the Bering Strait to the southern Korean Peninsula (the Sea of Japan), as well as from the central part of Honshu Island, along the Asian coastline to the Kenai Peninsula in the Gulf of Alaska and south along the coastline of the United States (Mecklenburg et al. 2002; Fedorov et al. 2003; Renaud 2011). This species is prey for a variety of species including sea gulls Larus, burbot Lota lota, pike Esox lucius, and nelma Stenodus leucichthys. On the other hand, it can be considered a major predator of the Pacific salmon (Oncorhynchus spp.) both at sea and in freshwater (Birman 1950; Roslyy & Novomodnyy 1996; Novomodnyy & Belyaev 2002; Bugaev & Shevlyakov 2005, 2007; Shevlyakov & Parensky 2010, 2011). This lamprey is also a parasite of the ciscoes Coregonus spp. and Prosopium spp., as well as threespine stickleback Gasterosteus aculeatus, rainbow smelt Osmerus mordax dentex, and Saffron cod Eleginus gracilis (Nikol’sky 1956; Horne-Brine 2007). In addition, this lamprey is important in maintaining the natural infestation of salmons with nematodes as it is an intermediate and reservoir host of the parasites and serves as the main vector for juvenile, resident, and migratory salmons (Butorina 1988). Some researchers discount the damage to the Pacific salmon incurred by Arctic lamprey because they

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either think that there is no damage (Myagkov 1983) or consider it insignificant (Gritsenko 1968). The Pacific lamprey is widespread in the North Pacific from the North Hokkaido (Japan) and South California (USA) in the south and up to northern part of the Bering Sea in the north (Scott & Crossman 1973; Ruiz-Campos & Gonzalez-Guzman 1996; Fukutomi et al. 2002). The Pacific lamprey is considered the most numerous species of parasitic lamprey of the west coast of Canada (Richards et al. 1982). At different stages of its life cycle, it serves as food for various aquatic animals from crayfish up to piscivorous birds and marine mammals (Hart 1973; Scott & Crossman 1973; Beamish 1980), and also is a serious parasitic threat to other fish in the North Pacific (Richards et al. 1982). Data on the trophic phase of Arctic and Pacific lampreys are very scarce (Nikol’sky 1956; Novikov 1963; Abakumov 1964; Prokhorov & Grachev 1965; Beamish 1980; Shuntov & Bocharov 2003, 2004, 2005, 2006; Murphy et al. 2003; Sviridov 2006; Orlov et al. 2007; Sviridov et al. 2007; Renaud 2011; Murauskas et al. 2013; Siwicke 2014). While the distribution of these species in the North Pacific was recently published (Orlov et al. 2008a, 2014), comparative analysis of the distributions was not performed. Such analysis would facilitate an identification of the composition of hosts for each lamprey species and an evaluation of their role in the ecosystems of the North Pacific Ocean. The aim of this chapter is to review and compare the long-term data on spatial and vertical distributions of Arctic and Pacific lampreys in the North Pacific and to determine the composition of hosts for each lamprey species.

Material and Methods The data used for this analysis came mostly from trawl surveys by bottom and mid-water trawls in various regions of the North Pacific carried out during 1975-2009 by researchers at the Pacific Scientific Research Fisheries Center (TINRO-Center, Vladivostok, Russia) and Alaska Fisheries Science Center (AFSC, Seattle, USA). The material obtained included only those catches in which Arctic or Pacific lampreys were recorded (Orlov et al. 2008a, 2014). In total, data from 469 catches of Arctic lamprey in bottom and mid-water trawls (all with indication of capture depth and depth of sea floor) and 3832 catches of Pacific lamprey (3818 with depths records) were analyzed. All catches were considered to be: 1) on the bottom, if the depth of location and layer of trawling coincided, or 2) pelagic, if the depths of location and layer of trawling differed by 10 m and more. Thus, the numbers of bottom and pelagic

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catches for Arctic lamprey were 40 and 429, and for Pacific lamprey they were 700 and 3118, respectively. Maps featuring the spatial distribution of the species were constructed based on the software SURFER 8 (Golden Software, Inc.; 2005).

Distribution and relative abundance The Arctic lamprey was commonly found in the Sea of Japan, Sea of Okhotsk, and the Bering Sea. Only solitary specimens were registered in the Pacific waters near Hokkaido Island, the Kuril Islands, and Eastern Kamchatka. Its maximum concentrations were observed in the central Sea of Japan to southeastern Peter the Great Bay, as well as in the northwestern Sea of Okhotsk to the east of northern Sakhalin and in the northeastern Bering Sea (Fig. 16-1A). In the majority of other regions, the catches of Arctic lamprey were insignificant. These were results are comparable to those obtained earlier (Shuntov & Bocharov 2003, 2004, 2005, 2006; Sviridov 2006, Sviridov et al. 2007). Thus, these studies showed that large concentrations of the Arctic lamprey occur in the Sea of Okhotsk (to the east of northern Sakhalin), near the continental coast of the northwestern Sea of Japan, near southwestern Sakhalin, and in the northwestern and central parts of the Bering Sea. It was pointed out in the earlier publications as well that this species was almost totally absent from the Pacific waters of the Kuril Islands and the eastern coast of Kamchatka. Because the earlier publications were limited to the northwestern Pacific, there is no information on the distribution outside the Russian waters in the northeastern Pacific. The Pacific lamprey is most abundant in the Bering Sea, occurring practically everywhere, except for the limited area in the central southern part (Fig. 16-1B). In the south, this species occurs down to central Honshu. Within Russian waters, the largest catches were recorded in the Bering Sea off the Navarin Cape and in the central part of the Koryak coast. In the eastern Bering Sea, it is most abundant off the eastern Aleutian Islands but rare in the shallower part of this area. Off the US and Canada west coast, it is caught in greatest numbers from southern Vancouver to San Francisco (we have no catch data between northern Vancouver and the Gulf of Alaska.

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Figure 16-1. Number of specimens per trawl in the North Pacific for Arctic lamprey(A) and Pacific lamprey (B).

The high abundance of Pacific lamprey in the Bering Sea in the Navarin Cape vicinity and in the central part of the Koryak coast is similar to previous data on the locations of maximum concentration (Shuntov &

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Bocharov 2005; Sviridov 2006). The large catches of the Pacific lamprey in the specified areas most likely were caused by high abundance of its hosts, primarily, the walleye pollock Theragra chalcogramma and Greenland halibut Reinhardtius hippoglossoides (Shuntov 1965; Fadeev 1986, 2005). The biomass of the most common Pacific lamprey hosts (walleye pollock, Pacific cod Gadus macrocephalus, Pacific herring Clupea pallasii, Pacific halibut Hippoglossus stenolepis, Greenland halibut, Kamchatka Atheresthes evermanni and arrowtooth Atheresthes stomias flounders) in the eastern Bering Sea was about 4.2 million tons for 2006 (Lauth & Acuna 2007). Thus, the main concentrations of these species were related to the continental slope, which may explain the increased number of lamprey in this area. The shallow water areas where Pacific lamprey were rare were characterized by a high fish biomass (about 5 million tons for 2006), dominated primarily by the abundance of three flatfish species (yellowfin sole Limanda aspera, rock sole Lepidopsetta bilineata and Alaska plaice Pleuronectes quadrituberculatus) but no attacks by lamprey have been recorded on these species. Pacific herring was the only common lamprey prey occurring in the shallow water area of the Bering Sea. However, the abundance was low (23 thousand tons for 2006) and they were distributed mostly between the St. Lawrence, St. Matthew, and Nunivak Islands (Lauth & Acuna 2007), where occasional catches of the Pacific lamprey were recorded. The largest catches of the Pacific lamprey along the west coast of North America may be related to the high abundance of the North Pacific hake (Ermakov 1986), which is an important host species in this area (Beamish 1980). Catches of the Pacific lamprey occurred very rarely over much of the area off the Aleutian Islands. Despite the rather high abundance of Pacific lamprey hosts (walleye pollock, Pacific cod, and Pacific halibut), whose biomass was estimated for 2002 at a value of about 630 thousand tons (Zender 2004), The probable reasons for the low catches of lamprey may be the remoteness of the islands from the spawning grounds of Pacific lamprey and the connection of basic aggregations of hosts to a narrow coastal strip of poorly developed shelf (Hart 1973; Scott & Crossman 1973; Beamish 1980). We cannot address the distribution of Pacific lamprey in British Columbia waters, as we had no data from Canadian trawl surveys. However Wade and Beamish (Chapter 17 of this book) report on the occurrence in the Strait of Georgia. The rare records of the Pacific lamprey in the Gulf of Alaska, both pelagic and on the bottom, are difficult to explain, as within that area regular trawl surveys are conducted and there

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is a large-scale trawl fishery. The number of common hosts in the Gulf of Alaska (walleye pollock, cod, and Pacific halibut) was estimated at about 3.5 million tons in a 1996 survey (Martin 1997). The densest aggregations of walleye pollock, cod and Pacific halibut were recorded off southwestern Kodiak Island. This corresponds to the distribution pattern of Pacific lamprey maximum catches in the Gulf of Alaska. However, there is a lack of correlation between the number of host species in this area and the number of Pacific lamprey catches. Probably, this is related to the small number of rivers running into the Gulf of Alaska and to the flow regulation of many rivers on the US and Canada west coast by construction of hydropower dams (Beamish & Northcote 1989; Mesa 2002; Moser et al. 2002; Robinson et al. 2002; Moser & Close 2003; Hamilton et al. 2005). This might limit the opportunity for normal reproduction and maintaining of high abundance of the Pacific lamprey in the Gulf of Alaska and adjacent areas.

Seasonal changes in spatial distribution Our data on seasonal patterns in the spatial distribution of Arctic lamprey can be considered as representative mostly for summer and autumn, as sampling in spring and winter was minimal. In the spring, this species was most frequently caught in the central Sea of Japan (Fig. 162A). Solitary specimens were registered in the Sea of Okhotsk near southwestern Kamchatka and in the southwestern Bering Sea, i.e., in the waters that were not covered with ice. In the summer, the Arctic lamprey occurrence was widespread. It was found everywhere in the Sea of Japan, Sea of Okhotsk, and the Bering Sea (Fig. 16-2B) except for deep-water basins. In this period, they were almost totally absent in the northwestern Sea of Okhotsk and the northern Bering Sea; but, small concentrations were found in the coastal waters of the western Bering Sea from Cape Olyutorsky to Cape Navarin. By autumn, Arctic lamprey abundance was low in the northern Sea of Japan and near eastern Sakhalin and western Kamchatka (Fig. 16-2C). However, an increased number was registered in the northwestern Sea of Okhotsk and the coastal waters of the northern and northwestern Bering Sea from Cape Olyutorsky to St. Matthew Island. In December, solitary specimens were found only near southeastern Kamchatka and the central Koryak shelf in the western Bering Sea (Fig. 16-2D), which may be due to the insufficient observations due to bad weather. Data obtained in January-March are absent, because the area was covered with ice.

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Figure 16-2. Capture sites of the Arctic lamprey in the North Pacific during spring (A), summer (B), autumn (C) and winter (D).

Maps featuring its quantitative distribution of the Arctic lamprey in different seasons of the year are available only for the northwestern Sea of Japan and the western Bering Sea (Shuntov & Bocharov 2004, 2006). Generally, the abundance of this species in the Sea of Japan increases from the spring to summer and decreases by autumn. In the Bering Sea, the abundance is greatest in the summer-autumn period. Data on the distribution of Arctic lamprey in the winter period have not been available until recently. The low number of lampreys caught in spring is a result of inability to sample due to ice. The transition from the spring to summer is accompanied by an increase in the catches of Arctic lamprey, which occurs as the ice melts and the juvenile transformed lampreys move from rivers into the sea (during the end of May-July in Kamchatka) (Renaud 2011). From the summer to autumn, the Arctic lamprey redistribute as noted earlier by Sviridov et al. (2007) as they disperse from areas of densest concentration. Thus, the catches in the northwestern Sea of Japan and near western Kamchatka become lower and increase in the northwestern Sea of Okhotsk. This is associated with the cessation of feeding and movements to spawning sites. The lampreys move to rivers in Japan in October (Renaud 2011) and occur in the lower reaches of the Amur River in the second half

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of August. The spawning migration peaks from the end of September to the first third of October (Bogaevsky 1949). Similar behavior of Arctic lamprey is observed in the rivers of the White Sea Basin, where they form concentrations in the river mouths areas during the second half of the summer. Here, they feed intensively until autumn and enter the rivers from the end of September-October (Gudoshnikov & Krykhtin 1965). At the same time, the number of lamprey caught in the northern part of the Bering Sea during autumn is significantly higher compared to summer. This suggests that the metamorphosis of lamprey and migration to the sea from the Yukon River takes place in August-November (Roberge et al. 2002). Adult specimens move into the Yukon River from the end of November to the end of April (Renaud 2011). An extremely low number of Arctic lampreys were caught in December. However, bad weather makes it difficult to study the freshwater migration of mature specimens. Seasonal distribution changes in Pacific lamprey were also recorded in our study. During spring solitary catches of Pacific lamprey occur off Paramushir and Kodiak Islands (Fig. 16-3A). Largest numbers occurred in the Bering Sea from Capes Olyutorsky and Navarin to the eastern Aleutian Islands, and also in waters of US and Canada south of Vancouver Island. In summer, this species was widely distributed in the North Pacific (Fig. 16-3B). The southern border of its range in Asian waters appeared near the southern Kuril Islands. Abundance of Pacific lamprey in the Bering Sea considerably increased, and its records became most frequent along the coast between Cape Olyutorsky and Cape Navarin and farther along the continental slope edge to the eastern Aleutian Islands. In contrast, spring and summer distributions off the US and Canada did not differ. In autumn (Fig. 16-3C), this species most frequently occurred in the Bering Sea and its abundance in the open part of the Sea increased considerably. The southern edge of the range shifted to central Honshu, occurrence off southwestern Kamchatka somewhat increased, and some captures were recorded in the eastern Bering Sea between St. Matthew and Nunivak Islands. As in spring and summer, Pacific lamprey occurred in greatest numbers south of Vancouver Island for tows made off the North American coast. In winter most records were from the open part of the Bering Sea (Fig. 16-3D) that is free of ice in this period. Otherwise, occasional Pacific lamprey records were registered in the high seas east of Kamchatka and south of the Gulf of Alaska, as well as in coastal waters of Honshu.

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Figure 16-3. Capture sites of the Pacific lamprey in the North Pacific during spring (A), summer (B), autumn (C) and winter (D).

Maps of the quantitative distribution of Pacific lamprey in different seasons of the year are available only for the Russian waters of the northwestern Pacific Ocean (waters off Kuril Islands and Kamchatka) and the western Bering Sea (Shuntov & Bocharov 2005, 2006). Generally, these maps demonstrate similar seasonal trends in Pacific lamprey distribution with the areas mentioned. However, they were constructed based on GIS technology with a 1º grid, and therefore reflected only the general behaviour of Pacific lamprey distribution. Moreover, the data are combined for mid-water trawls in epi- and mesopelagic depths so that it is not possible to evaluate distribution near the bottom. Finally, the specified maps were confined to the limits of the Russian waters in the northwestern Pacific and did not give any information concerning distribution of Pacific lamprey in the northeastern part of the ocean. Despite the limited amount of information, our data provide new insight into seasonal changes of Pacific lamprey spatial distribution within the entire North Pacific.

Long-term changes in spatial distribution Before the 1990s, Arctic lamprey was most often found in the northern Sea of Japan and the western Bering Sea (Fig. 16-4A). In the subsequent ten years, the number of captures in the Sea of Japan and the central Bering

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Figure 16-4 (previous page). Capture sites of the Arctic lamprey in the North Pacific before 1990 (A), in 1990-1999 (B) and after 2000 (C).

Sea became significantly lower, in contrast to the Sea of Okhotsk, where catches were numerous, especially near western Kamchatka (Fig. 16-4B). In the 2000s, this species was not caught in the Sea of Japan. Its abundance considerably decreased in the Sea of Okhotsk and in the western Bering Sea. However, large concentrations were detected in the eastern Bering Sea (Fig. 16-4C). The main reason for the changes in spatial distribution of Arctic lamprey in the North Pacific is probably due to sampling changes. A reduced number of investigations were performed in the Sea of Japan during the 1990s and almost none in the 2000s. This occurred because scientific expeditions to Russian waters were eliminated due to the catastrophic decrease in the abundance of Japanese sardine Sardinops melanostictus (Fadeev 2005), which was the main object of such expeditions in the early 1990s. In the 1980s, there were regular cruises to estimate stock sizes of walleye pollock in the central Bering Sea, where this species was abundant (Fadeev 1986, 2005). Consequently, the greater effort influenced the numerous captures of Arctic lampreys in this region. In the subsequent years, almost no investigations were carried out in the central Bering Sea. In the 2000s large lamprey concentrations were found in the eastern Bering Sea, because this period was marked by trawl surveys supported by the BASIS program (Bering Aleutian Salmon International Survey) under the aegis of the North Pacific Marine Science Organization (PICES) (Helle et al. 2007). Despite the variation in fishing effort, there are the data (E.I. Barabanshchikov personal communication) to indicate that young and adult Arctic lamprey disappeared from catches in southern Primorye during surveys targeting Pacific salmon smolts in recent years. There is also information that Arctic lamprey abundance in the Amur River recently decreased dramatically, due in part to a long-term drought and a sharp rise in Amur pike Esox reicherti numbers (G.V. Novomodnyy personal communication). This observation is supported by the recreational capture in winter of some Amur pike that had stomachs full of Arctic lampreys. Fishermen also reported numerous hoopnet captures of Arctic lampreys with deep wounds from teeth (most probably of Amur pike). These facts and higher occurrence of Arctic lamprey in the eastern Bering Sea might be associated with climatic changes that caused a northward shift in its distribution. Thus, long-term changes in Arctic lamprey catch distribution in the North Pacific were likely the result of changing research patterns, but also may be associated with a climate shift.

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Figure 16-5 (previous page). Capture sites of the Pacific lamprey in the North Pacific before 1990 (A), in 1990-1999 (B) and after 2000 (C).

Before the 1990s, records of Pacific lamprey occurred exclusively in two areas – off the US and Canada west coast and in the Bering Sea with solitary captures off the southern Kuril Islands, central Honshu, and Kodiak Island (Fig. 16-5A). During the 1990s, the number of records in the Bering Sea considerably increased, especially along the Koryak coast. Pacific lamprey appeared in the southwestern Sea of Okhotsk, and the number of captures in the Gulf of Alaska increased (Fig. 16-5B). In the new millennium, the range of this species has apparently extended into the waters of the Gulf of Alaska. It is now recorded off the eastern Sakhalin and abundance in waters of the eastern Bering Sea continental slope from Navarin Cape to eastern Aleutian Islands and off the coasts of US and Canada has increased as well (Fig. 16-5C). Long-term changes in Pacific lamprey abundance are poorly understood. Only recently has long-term data on the number of spawners migrating to Columbia River and on trawl catch rates in the North Pacific been analyzed (Murauskas et al. 2013). The former indicate that Pacific lamprey spawners were more abundant in late 1990s compared to the 2000s. The latter indicate the existence of peaks, with maximum catches in the middle of the 1980s, 1990s, and 2000s. Presently, abundance of Pacific lamprey is probably rising. Information from the 2014 Pacific salmon fishing season off British Columbia may support this idea in that sockeye salmon Oncorhynchus nerka in many areas bear a greater number of lamprey wounds (Pynn 2014).

Vertical distribution Historic data on the vertical distribution of the Arctic lamprey in the North Pacific are very limited (Fedorov 2000; Sheiko & Fedorov 2000; Mecklenburg et al. 2002; Fedorov et al. 2003). It is noted in all these publications that Arctic lamprey inhabits the upper 50-m layer. Our data radically transform the established views on the vertical distribution of this species in the sea. Arctic lamprey occurred higher in the water column than Pacific lamprey. The majority of the Arctic lamprey were caught at a considerable distance from the bottom (Fig. 16-6A), which is evidence that this species or its hosts or both, is a typical dweller of mid-waters. It was found in the mid-water trawls from the surface to 1000 m. In addition, 82.1% of all the lampreys were caught in the upper 100-m layer (Fig. 16-8A). Although the occurrence of this species decreased with depth, the catches at depths of 0-

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400 m were stable. Furthermore, 90.2% of all the lampreys were obtained from depths of less than 400 m (Fig. 16-9A). The maximum number of Arctic lampreys was also caught within this depth range.

Figure 16-6. Capture sites of the Arctic (A) and Pacific (B) lampreys in the water column of the North Pacific.

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Arctic lamprey was less frequent near the bottom. When caught near the bottom, they were most often found near eastern Sakhalin and in the western Bering Sea at depths from 23 to 710 m. (from Cape Olyutorsky to Navarin Cape) (Fig. 16-7A).

Figure 16-7. Capture sites of the Arctic (A) and Pacific (B) lampreys near the bottom in the North Pacific.

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The Pacific lamprey occurred in the catches of bottom trawls at depths of 16-1193 m. About 81% of the individuals were caught at depths of less than 300 m (Fig. 16-9B). The number of captures from depths exceeding 200 m considerably decreased as the depth increased. On the bottom, the Pacific lamprey occurred mostly in the Bering Sea along the continental slope from the Africa Cape to the east part of the Aleutian Archipelago, and along the west coast of North America south from Vancouver Island (Fig. 16-7B). The overwhelming majority of these catches were related to the shelf and continental slope waters. The Pacific lamprey was rather widespread in the pelagic zone (Fig. 16-6B). The numerous catches of this species at a sufficient distance from coasts (e.g., in the central part of the Bering Sea and off the Kamchatka coast), corroborated the conclusions of Beamish (1980) on its ability to migrate long distances to open waters. At the same time, our data indicated more frequent occurrence of the Pacific lamprey in the eastern part of the Sea of Okhotsk off the southwest coast of Kamchatka than indicated by former records (Sviridov 2006). In the pelagic zone, Pacific lamprey were caught by trawls at depths from 0 to 1485 m, and about 83% of all the catches occurred at depths of less than 200 m (Fig. 16-8B). The average catch size and frequency of occurrence of Pacific lamprey decreased with an increase in depth. Nevertheless, a significant number of individuals (about 8%) was recorded in the mesopelagic at a depth of 400-500 m, which corroborated previously-published records of this species in the mesopelagic Bering Sea (Balanov & Il’insky 1992; Balanov & Radchenko 1995). Little was known concerning the vertical distribution of the Pacific lamprey. There is an opinion (Abakumov 1964) that the Pacific lamprey inhabit greater depths of 300-400 m and deeper. It is believed that the Pacific lamprey can occur at depths from 0 to 1100 m (Fedorov 2000; Sheiko & Fedorov 2000), and catches at the surface often occur in the Pacific waters off the Kuril Islands (Ivanov 1998; Fedorov & Parin 1998). Later Prokhorov & Grachev (1965) showed that it can parasitize herring at a depth of about 5 m. A range of 200-1000 m was considered to be the preferred depths (Fedorov 2000). Our data considerably change the existing view about Pacific lamprey vertical distribution during its marine phase of life.

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Figure 16-8. Vertical distributions of the Arctic (A) and Pacific (B) lampreys in the water column of the North Pacific.

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Figure 16-9. Vertical distributions of the Arctic (A) and Pacific (B) lampreys near the bottom in the North Pacific.

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Conclusion The comparison of spatial distributions of Arctic and Pacific lampreys identified the Bering Sea as an area where their ranges overlapped. The Arctic lamprey is rare in the northeastern Pacific off the Aleutian Islands, Gulf of Alaska, and coasts of US and Canada. The Pacific lamprey is not found in the Sea of Japan, is rare in the Sea of Okhotsk and most frequently occurs off the southwestern Kamchatka). It was most frequently caught in Pacific waters off the Kuril Islands and eastern Kamchatka. Both species inhabit almost the entire Bering Sea area but their distributions differ slightly. The Pacific lamprey is least abundant in shelf waters of the northern and eastern Bering Sea east of the Navarin Cape, where it is replaced by the Arctic lamprey. In contrast, the Arctic lamprey is absent along the continental slope break that separates the eastern Bering Sea and the deep-water Aleutian Basin. In the western Bering Sea, the distribution of both species is quite similar, with high concentrations southeast of Navarin Cape and in the central part of Koryak shelf. The Arctic lamprey also is abundant in the central Bering Sea, while the Pacific lamprey is abundant in southwestern Bristol Bay. It is believed that the Arctic lamprey occurs closer to coasts than the Pacific lamprey that inhabits waters farther offshore (Murphy et al., 2003). Recent studies, however, do not confirm this conclusion (Orlov et al. 2008ɚ, 2014). In the northwestern Bering Sea both species co-occur. However, their different vertical distributions probably decrease feeding competition; 82.1% of Arctic lamprey captures were recorded within the upper 100-m while only 51.3% of Pacific lamprey were caught at these depths (Orlov et al. 2008a, 2014). The extremely low occurrence of the Arctic lamprey near the bottom and an increased abundance in the upper 100-m layer, suggests that main host species of this lamprey during the marine period are Pacific salmon. Recent research of Siwicke (2014) confirmed that the main host fishes of this species in the North Pacific are Pacific salmon and Pacific herring. The considerably deeper distribution of Pacific lamprey in the North Pacific and its closer affinity to the bottom indicates that important hosts are demersal fishes inhabiting depths > 100 m and include walleye pollock, Pacific cod, Pacific herring, Pacific halibut, Greenland halibut, Kamchatka and arrowtooth flounders, rockfishes Sebastes spp., etc. (Beamish 1980; Orlov et al. 2008b; Siwicke 2014).

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Acknowledgments The authors are grateful to their colleagues Dr. Vadim Savinykh, Dr. Andrei Vinnikov, and Dr. Evgeny Barabanshchikov (TINRO-Center, Vladivostok, Russia), German Novomodnyy (Khabarovsk Branch of TINRO-Center, Khabarovsk, Russia), and Dmitry Pelenev (VNIRO, Moscow, Russia) for valuable assistance in preparation of this chapter. Special thanks to Alaska Fisheries Science Center for availability of bottom trawl survey data on their website. Authors also acknowledge valuable comments of Dr. Mary Moser, Dr. Kevin Siwicke and Dr. Richard Beamish on the early draft of the chapter that allowed for its considerable improvement.

References Abakumov V.A. 1964. About sea period of life of Pacific lamprey – Enthosphenus tridentatus (Richardson). Trudy VNIRO 49, 253–256 (In Russian). Balanov A.A. & Il’insky E.N. 1992. Species composition and biomass of mesopelagic fishes in Okhotsk and Bering seas. Voprosy Ikhtiologii 32, 56–63 (In Russian). Balanov A.A. & Radchenko V.I. 1995. Composition and distribution of fishes in meso- and bathypelagial of the Bering and Okhotsk seas. In Kotenev B.N., Sapozhnikov V.V. (eds.): Complex Study of the Bering Sea Ecosystem. Pp. 335-343. Moscow: VNIRO (In Russian). Beamish R.J. 1980. Adult biology of the river lamprey (Lampetra ayresi) and Pacific lamprey (Lampetra tridentata) from the Pacific coast of Canada. Canadian Journal of Fisheries and Aquatic Science 37, 19061923. Beamish R.J. & Northcote T.G. 1989. Extinction of a population of anadromous parasitic lamprey, Lampetra tridentata, upstream of an impassable dam. Canadian Journal of Fisheries and Aquatic Science 46, 420–425. Birman I.B. 1950. About parasitism of Arctic lamprey on salmons of the genus Oncorhynchus. Izvestiya TINRO 32, 158-160 (In Russian). Bogaevskii V.T. 1949. On possibilities of commercial fishery of lamprey in Amur region. Rybnoye Khozyaistvo 7, 22-24 (In Russian). Bugaev A.V. & Shevlyakov E.A. 2005. Traumatization of Pacific salmons of the genus Oncorhynchus spp. by some predatory species based on data of driftnet catches withIn Russian EEZ in 2004. Izvestiya TINRO 142, 46-63 (In Russian).

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Bugaev A.V. & Shevlyakov E.A. 2007. Wounding of Pacific salmon by predators in gillnet catches in the Russian economic zone in 2004. North Pacific Anadromous Fish Commission Bulletin 4, 145-154. Butorina T.E. 1988. About the role of lampreys in the life cycle of nematods of salmonid fishes in Kamchatka. Biologiya Morya 4, 66-67 (In Russian). Ermakov Yu.K. 1986. Hakes. In Vinogradov M.E. et al. (eds.): Biological Resources of the Pacific Ocean. Pp. 221-228. Moscow: Nauka (In Russian). Fadeev N.S. 1986. The walleye pollock. In Vinogradov M.E. et al. (eds.): Biological Resources of the Pacific Ocean. Pp. 187-201. Moscow: Nauka (In Russian). Fadeev N.S. 2005. Guide to the Biology and Fisheries of Fishes of the North Pacific. Vladivostok: TINRO-Center (In Russian). Fedorov V.V. 2000. Species composition, distribution and habitation depths of species of fish-like animals and fishes of the northern Kuril Islands and adjacent areas of the Okhotsk and Bering seas. In Kotenev B.N. (ed.): Commercial-Biological Research of Fishes in the Pacific Waters off the Kuril Islands and Adjacent Areas of the Okhotsk and Bering Seas in 1992-1998. Pp. 7-41. Moscow: VNIRO (In Russian). Fedorov V.V. & Parin N.V. 1998. Pelagic and Benthopelagic Fishes of the Pacific Waters of Russia. Moscow: VNIRO (In Russian). Fedorov V.V., Chereshnev I.A., Nazarkin M.V., Shestakov A.V. & Volobuev V.V. 2003. Catalogue of Marine and Freshwater Fishes of the Northern Sea of Okhotsk. Vladivostok: Dal’nauka (In Russian). Fukutomi N., Nakamura T., Doi T., Takeda K. & Oda N. 2002. Records of Entosphenus tridentatus from Naka River system, central Japan: physical characteristics of possible spawning redds and spawning behavior in the aquarium. Japanese Journal of Ichthyology 49, 53–58. Gritsenko O.F. 1968. To the question about ecological parellelism between lampreys and salmons. Izvestiya TINRO 65, 157-169 (In Russian). Gudoshnikov Yu.A. & Krykhtin M.L. 1965. Fishery of Arctic lamprey in the Amur River. Rybnoye Khozyaistvo 7, 47-48 (In Russian). Hamilton J.B., Curtis G.L., Snedaker S.M., & White D.K. 2005. Distribution of anadromous fishes in the upper Klamath River watershed prior to hydropower dams - a synthesis of the historical evidence. Fisheries 30, 10–20. Hart J.L. 1973. Pacific fishes of Canada. Bulletin of Fisheries Research Board of Canada 180, 1-740. Helle J., Farley E., Murphy J., Feldmann A., Cieciel K., Moss J., Eisner L., Pohl J. & Courtney M. 2007. The Bering-Aleutian Salmon

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International Survey (BASIS). AFSC Quarterly Report JanuaryFebruary-March, 1-5. Horne-Brine M. 2007. Yukon River lamprey fishery. Oncorhynchus 27, 1, 3-4. Ivanov O.A. 1998. The epipelagic community of fishes and cephalopods of Kuril waters of the Pacific in 1986-1995. Izvestiya TINRO 124, 3-54 (In Russian). Lauth R.R. & Acuna E. 2007. Results of the 2006 Eastern Bering Sea ɫontinental shelf bottom trawl survey of groundfish and invertebrate resources. U.S. Department of Commerce, NOAA Technical Memorandum. NMFS–AFSC–176, 1-187. Martin M.H. 1997. Data Report: 1996 Gulf of Alaska bottom trawl survey. U.S. Department of Commerce, NOAA Technical Memorandum. NMFS–AFSC–82, 1-235. Mecklenburg C.W., Mecklenburg T.A. & Thorsteinson L.K. 2002. Fishes of Alaska. Bethesda: American Fisheries Society. Mesa M.G. 2002. Annual physiological profiles of Pacific lamprey: implications for migrations past dams. In Moser. M., Bayer J. & MacKinlay D. (eds.): The Biology of Lamprey. Proceedings of International Congress on the Biology of Fish. Pp. 17-20. Vancouver: American Fisheries Society, Physiology Section. Moser M.L., Cavender W.P., Ogden D.A. & Peery C. 2002. Effects of light on migrating adult Pacific lamprey. In Moser. M., Bayer J. & MacKinlay D. (eds.): The Biology of Lamprey. Proceedings of International Congress on the Biology of Fish Pp. 37-40. Vancouver: American Fisheries Society, Physiology Section. Moser M.L. & Close D.A. 2003. Assessing Pacific lamprey status in the Columbia River basin. Northwest Science 77, 116–125. Murauskas J.G., Orlov A.M. & Siwicke K.A. 2013. Relationships between the abundance of Pacific lamprey in the Columbia River and their common hosts in marine environment. Transactions of the American Fisheries Society 142, 143-155. Murphy J., Davis N., Ivanov O., Rohr M., Elmajatii S. & Barber W. 2003. Cruise report of the 2002 F/V Northwest Explorer BASIS survey in the Bering Sea, September-October. NPAFC Doc. 676. Rev. 1. Vancouver: North Pacific Anadromous Fish Commission. Myagkov N. 1983. Far Eastern lampreys. Rybovodstvo I Rybolovstvo 11, 10 (In Russian). Nikol’sky G.V. 1956. Some data on sea period of life of Arctic lamprey Lampetra japonica (Martens). Zoologicheskii Zhurnal 35, 588-591 (In Russian).

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Novikov N.P. 1963. Events of Pacific lamprey Entosphenus tridentatus (Gairdner) attacks of halibuts and other fishes of the Bering Sea. Voprosy Ikhtiologii 3, 567–569 (In Russian). Novomodnyy G.V. & Belyaev V.A. 2002. Predation by lamprey smolts Lampetra japonica as a main cause of Amur chum salmon and pink salmon mortality in the early sea period of life. NPAFC Technical Report 4, 81-82. Orlov A.M., Vinnikov A.V. & Pelenev D.V. 2007. Methodic of the study of sea period of life in parasitic anadromous lampreys by the example of Pacific lamprey Lampetra tridentata (Gairdner, 1836) fam. Petromyzontidae. Voprosy Rybolovstva 8, 287–312 (In Russian). Orlov A.M., Savinykh V.F. & Pelenev D.V. 2008a. Features of spatial distribution and size composition of Pacific lamprey Lampetra tridentata in the North Pacific. Biologiya Morya 34, 324-335 (In Russian). Orlov A.M., Pelenev D.V. & Vinnikov A.V. 2008b. Pacific lamprey and stocks of commercial fishes in Russian waters of the Far East. Rybnoye Khozyaistvo 2, 60-65 (In Russian). Orlov A.M., Baitaliuk A.A. & Pelenev D.V. 2014. Features of spatial distribution and size composition of Arctic lamprey Lethenteron camtschaticum in the North Pacific. Okeanologiya 54, 200-215 (In Russian). Parin N.V. 2001. An annotated catalog of fishlike vertebrates and fishes of the seas of Russia and adjacent countries. Pt. 1. Orders Myxiniformes – Gasterosteiformes. Journal of Ichthyology 41, S51-S131. Parin N.V., Evseenko S.A. & Vasil’eva E.D. 2014. Fishes of Russian Seas: Annotated Catalogue. Moscow: KMK Scientific Press. Prokhorov G.V. & Grachev L.E. 1965. About record of Pacific lamprey Enthosphenus tridentatus (Gairdner) in the western Bering Sea. Voprosy Ikhtiologii 5, 723–726 (In Russian). Pynn L. 2014. Parasitic lampreys feed on bumper sockeye run. Eel-like species has targeted large schools of Fraser River salmon in the past. The Vancouver Sun. August 30, 2014, http://www.vancouversun.com/Parasitic+lampreys+feed+bumper+sock eye/10161652/story.html. Renaud C.B. 2011. Lampreys of the world. An annotated and illustrated catalogue of lamprey species known to date. Rome: FAO. Richards J.E., Beamish R.J. & Beamish F.W.H. 1982. Descriptions and keys for ammocoetes of lampreys from British Columbia, Canada. Canadian Journal of Fisheries and Aquatic Science 39, P. 1484–1495.

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Roberge M., Hume J.M.B., Minns C.K. & Slaney T. 2002. Life history characteristics of freshwater fishes occurring in British Columbia and the Yukon, with major emphasis on stream habitat characteristics. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2611, 1-262. Robinson T.C., Bayer J.M. & Seelye J.G. 2002. Upstream migration of Pacific lamprey in the John Day River: behavior, timing, and habitat use. In Moser. M., Bayer J. & MacKinlay D. (eds.): The Biology of Lamprey. Proceedings of International Congress on the Biology of Fish Pp. 69-72. Vancouver: American Fisheries Society, Physiology Section. Roslyy Yu.S. & Novomodnyy G.V. 1996. Elimination of salmons’ young of the genus Oncorhynchus in the Amur river by Arctic lamprey Lampetra japonica and other predatory fishes during early sea life period. Voprosy Ikhtiologii 36, 50-54 (In Russian). Ruiz-Campos G. & Gonzalez-Guzman S. 1996. First freshwater record of Pacific lamprey, Lampetra tridentata, from Baja California, Mexico. California Fish and Game 82, 144–146. Scott W.B. & Crossman E.J. 1973. Freshwater fishes of Canada. Bulletin of Fisheries Research Board of Canada 184, 1–966. Sheiko B.A. & Fedorov V.V. 2000. Class Cephalaspidomorphi – Lampreys. Class Chondrichthyes – Cartilaginous Fishes. Class Holocephali – Chimaeras. Class Osteichthyes – Bony Fishes. In Moiseev R.S., Tokranov A.M. (eds.): Catalogue of Vertebrates of Kamchatka and Adjacent Waters. Pp. 1-69. PetropavlovskKamchatskii: Kamchatskii Pechatnyi Dvor (In Russian). Shevlyakov V.A. & Parensky V.A. 2010. Traumatization of Pacific salmons by lampreys in Kamchatka River. Biologiya Morya 36, 390394 (In Russian). Shevlyakov V.A. & Parensky V.A. 2011. Traumatization of salmons in Kamchatka River by predators and ectoparasites. Vestnik SVNTs DVO RAN 3, 59-69 (In Russian). Shuntov V.P. 1965. Distribution of Greenland halibut and Kamchatka flounder in the North Pacific. Trudy VNIRO 58 / Izvestiya TINRO 53, 155–163 (In Russian). Shuntov V.P. & Bocharov L.N. (eds.). 2003. Atlas of quantitative distribution of nekton in the Sea of Okhotsk. Maps. Vol. 1. Moscow: Natsional’nyie Rybnyie Resursy (In Russian). Shuntov V.P. & Bocharov L.N. (eds.). 2004. Atlas of quantitative distribution of nekton in the northwestern Sea of Japan. Maps. Vol. 2. Moscow: Natsional’nyie Rybnyie Resursy (In Russian).

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Shuntov V.P. & Bocharov L.N. (eds.). 2005. Atlas of quantitative distribution of nekton in the northwestern Pacific Ocean. Maps. Vol. 3. Moscow: Natsional’nyie Rybnyie Resursy (In Russian). Shuntov V.P. & Bocharov L.N. (eds.). 2006. Atlas of quantitative distribution of nekton in the western Bering Sea. Maps. Vol. 4. Moscow: Natsional’nyie Rybnyie Resursy. (In Russian). Siwicke K.A. 2014. Relationships Between Anadromous Lampreys and Their Host Fishes in the Eastern Bering Sea. Ph.D. Thesis. University of Alaska Fairbanks. Sviridov V.V. 2006. Spatio-temporal variability of distribution of main predatory fishes and fish-like animals – consumers of Pacific salmons in Far Eastern seas. Implementation Bulletin of “Conception of Far Eastern Basin Program of Pacific Salmon Research” 1, 266–276 (In Russian). Sviridov V.V., Glebov I.I., Starovoytov A.N., Sviridova A.V., Zuev M.A., Kulik V.V. & Ocheretyanny M.A. 2007. Wounding of Pacific salmon in relation to spatio-temporal variation in distribution patterns of important predatory fishes in the Russian economic zone. NPAFC Bulletin 4, 133-144. Zender H.H., Jr. 2004. Data report: 2002 Aleutian Islands bottom trawl survey. U.S. Department of Commerce, NOAA Technical Memorandum NMFS–AFSC–143, 1-258.

CHAPTER SEVENTEEN TRENDS IN THE CATCHES OF RIVER AND PACIFIC LAMPREYS IN THE STRAIT OF GEORGIA JOY WADE AND RICHARD BEAMISH

Introduction Pacific lamprey (Entosphenus tridentatus) and river lamprey (Lampetra ayresii) are anadromous fishes that enter and feed in the Strait of Georgia British Columbia, Canada. The Strait of Georgia is the body of water between Vancouver Island and British Columbia mainland that has been an area of study of juvenile Pacific salmon (Oncorhynchus spp.) survival (Beamish et al. 1998, 2012) Because of the recent interest in understanding factors affecting Pacific lamprey abundances in the Columbia River (Murauskas et al. 2013), we use incidental catches of lampreys from studies focused on juvenile salmon in the Strait of Georgia to improve our understanding of marine survival. Specifically, it is hypothesized that population abundance of Pacific lamprey and river lamprey is regulated by prey availability which in turn is highly influenced by environmental conditions as has been found for Pacific salmon (Ruggerone & Goetz 2004; Duffy & Beauchamp 2011; Beamish et al. 2010; Swain et al. 1991 ). It is difficult to get information on Pacific lamprey and river lamprey during their marine life as trawl nets are designed to catch juvenile salmon and not to retain lamprey, as well, some investigators are reluctant to handle the ones that are retained. The intent of this paper is to use information collected through the study of other species such as Pacific salmon (O. spp.), Pacific herring (Clupea pallasii) and groundfish, to help understand the early marine survival of Pacific and river lamprey within the Strait of Georgia.

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Pacific lamprey In British Columbia, Pacific lamprey are considered common and have been found in most large freshwater rivers as well as small rivers which empty into large rivers (R. Beamish, personal observations). Beamish (1980) notes that Pacific lamprey are widespread in British Columbia and have a greater distribution than previously thought as they have been observed in all the commercially important fishing areas off the west coast of Canada. Globally, they are found from the Sea of Japan to the Bering Sea to the eastern North Pacific Ocean south to Mexico (Mecklenburg et al. 2002; Renaud 2011). One of the sources of Pacific lamprey that enter the Strait of Georgia is the Nicola River, a major tributary of the Thompson River, British Columbia. Pacific lamprey from the Nicola River spend approximately 4 or 5 years as ammocoetes with young adults migrating downstream beginning in September (Beamish & Levings 1991). Ammocoetes and young adults sampled from the Fraser River were aged using statoliths (Beamish & Levings 1991). The oldest ammocoetes were age 6, recently metamorphosed lamprey ranged in age from 4 to 8 years (Beamish & Levings 1991). Ammocoete ages were also determined by Beamish and Northcote (1989) from data collected before and after a dam was constructed on the outlet of Elsie Lake, British Columbia. It was possible to estimate the age of Pacific lamprey ammocoetes to be approximately 7 years because lamprey spawning was prevented after the construction of the dam. (Beamish & Northcote 1989). The average length of young adult Pacific lamprey collected from the Fraser River in the spring of 1985 was 12.1 cm; 10.6 cm from the period March to May 1986 and; 12.3 cm from early April to early May 1987 (Beamish & Levings 1991). The time from metamorphosis to sea water entry has been reported to take up to one year (Beamish & Levings 1991) however, recently metamorphosed individuals may begin feeding in freshwater or in salt water by mid-October (Beamish 1980). Feeding in freshwater is most likely temporary as it has not been possible to keep metamorphosed anadromous Pacific lamprey in the laboratory in freshwater for their entire adult life span (Clark & Beamish 1988). Reports of freshwater feeding are for a short period of time after metamorphosis (Beamish & Northcote 1989) or in one case, a new species (Beamish 1982). Pacific lamprey from the Fraser River enter the Strait of Georgia over a protracted period of time, from March until the end of July (Beamish & Levings 1991). They return to freshwater either in the spring or fall and begin their upstream migration (Beamish 1980). Those lamprey populations that return in the spring tend to migrate farther upstream than

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fall returning fish, however, both spawn between April and July the following year (Beamish 1980). The Pacific lamprey population in the US Pacific Northwest has been reported to be in decline in recent years (Luzier et al. 2011; Murauskas et al. 2013; Mayfield et al. 2014). In 2003, the US Fish and Wildlife Service petitioned to list Pacific lamprey, among other lamprey species, as threatened or endangered under the Endangered Species Act of 1973 (Hayes et al. 2013). The petition was denied, in part, because of a lack of specific population information such as distribution, abundance and population structure (Klamath-Siskiyou Wildlife center and ten other conservation organizations, 2003). As a result of this determination, a range-wide conservation initiative was undertaken (Luzier et al. 2011), and an assessment was performed which found that Pacific lamprey populations have declined and many are at risk of extirpation (Hayes et al. 2013). River lamprey River lamprey are distributed from the Sacramento River in California north to Juneau, Alaska (Scott & Crossman 1973; Renaud 2011). In British Columbia, river lamprey have most frequently been reported from larger rivers such as the Fraser River (Beamish 1980; Beamish & Northcote 1989; Beamish & Neville 1995) where it has been shown to be the dominant organism by weight in the sediments of the 160 km section of the river from Hope, British Columbia to the mouth of the Fraser River (Beamish & Youson 1987). Beamish (2010) also reports samples of river lamprey from the Nass River, Knight Inlet (Klinaklini River) and Puget Sound. It is now known that some river lamprey in Puget Sound originate from several rivers flowing into the sound (Hayes et al. 2013) indicating that they also occur in smaller rivers. Metamorphosis begins in July but river lamprey do not enter the Strait of Georgia until the following year, from May to July (Beamish 1980; Beamish & Youson 1987). Metamorphosis is not complete until the oesophagus is open in the spring of the year following the onset of metamorphosis which delays salt water entry. Once the oesophagus opens, the lamprey can osmoregulate in salt water (Beamish & Youson 1987). They return to freshwater from September until late winter with spawning occurring in freshwater from April to June (Beamish 1980). The lifespan from metamorphosis to death of a river lamprey is approximately two years (Beamish 1980).

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Based on the results of a survey conducted in 1975, river lamprey abundance in the Strait of Georgia was estimated at 667,000 (Beamish & Williams 1976). Although the major prey of river lamprey entering the Strait of Georgia is Pacific herring, Pacific salmon remain an important component of the diet (Beamish & Neville 1995). In efforts to understand the potential causes of the marine mortality of salmon, Beamish and Neville (1995) estimated that river lamprey from the Fraser River killed a minimum of 20 million juvenile Chinook salmon (O. tshawytscha) and 2 million juvenile coho salmon (O. kistuch) in 1990 and; 18 million juvenile Chinook salmon and 10 million coho salmon in 1991. In 1991 alone, this equated to 65% and 25% of the total Canadian hatchery production of coho and Chinook salmon, respectively (Beamish & Neville 1995).

Methods Temperature data Temperature data have been compiled from 1969 to 2011 from the central Strait of Georgia, British Columbia. Oceanographic data including sea level height, sea surface temperature and salinity are taken at lighthouses in the Strait of Georgia and managed by the Department of Fisheries and Oceans Canada’s Institute for Ocean Sciences. Methodology for daily sea surface temperature and salinity have remained unchanged since the beginning of the time series and are described in Fissel et al. (1991). Trawl catches Lampreys were captured in trawls that were fished using the Government of Canada research vessel, W.E. Ricker. Standardized trawl surveys were performed as described in Beamish et al. (2000). Standardized trawl surveys were used to study the ocean life of juvenile Pacific salmon in the Strait of Georgia (Beamish et al 2000). A model 250/350/14 trawl (Cantrawl Pacific Ltd., Richmond, BC) was fished. The front end was 54m long with large meshes (ranging < 2 m to > 3.8 m wide). The intermediate section of the net contained mesh ranging from 1.6 m to 20 cm; the cod end meshes were 10 cm with a 1 cm liner in the last 7.6 m. A fixed survey design using track lines was used for these juvenile salmon surveys in the Strait of Georgia (Fig. 17-1) (Beamish et al. 2000). The survey area was 5,899 km2 and encompassed approximately 93% of the total area of the Strait of Georgia (Beamish et al. 2000). Surveys were

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normally conducted in July and September. Most sets were in the top 45m, and the proportion of deeper sets was consistent among surveys.

Figure 17-1. Standard track lines (bold) for trawl surveys in the Strait of Georgia. Sets were evenly spaced along these lines.

Catches of lampreys were standardized to 30 minute sets and summed for each depth strata. After 2011 the research cruises were staffed differently than had been done in previous years. Thus our data on catches from the trawl survey terminate after 2011 except for some specific reports where we are confident of the identifications. Catch data by depth strata are presented to demonstrate the depths over which lamprey have been captured in the Strait of Georgia. The depth data for river lamprey were only available for July and September 1997 to 2002 and July 2004. Catch per unit effort (CPUE) was calculated as the number of fish captured per set. CPUE for river lamprey was calculated for 1998 to 2011 with the exclusion of 2003 as only the September trawl data were available. It is probable that the lamprey catches, and subsequently CPUE, are low because the survey methods and net were not designed for the capture of lamprey.

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A species distribution survey provided relative abundance estimates of Pacific hake (Merluccius productus) and walleye pollock (Gadus chalcogrammus). These research surveys were in addition to the July and September surveys performed for salmonid research however, the same fishing methodologies applied. Catches of Pacific hake and walleye pollock include young-of-the-year, juvenile and mature fish at different depths. Sets were made at varying depths from the bottom to the surface throughout the Strait of Georgia. This allowed for the determination of species composition throughout the water column within a small area.

Results Temperature There was a warming trend from 1969 to 2003 followed by a cooling trend to 2011 (Fig. 17-2). The warming trend that was evident from the beginning of the time series in 1969 changed to a cooling trend in the early 2000’s. From 1969 to 2003 the average annual increase was 0.98oC at the surface and 0.94oC at 10m. From 2004 to 2011 there was a decrease in surface temperature of 0.63oC and a decrease of 1.25oC at 10m. Pacific lamprey Total catch of Pacific lamprey in the Strait of Georgia (1998-2011) from trawl surveys was highest in 1998 (n=28) and declined until 2005 (n=0) with catches increasing beginning in 2008 to 12 individuals in 2011 (Table 17-1). Pacific lamprey CPUE was highest in 1998 at 0.15 and lowest in 2005 and 2008 at 0 (Fig. 17-3). In the July 2013 survey in the Strait of Georgia an exceedingly large catch of Pacific lamprey (n=132) was landed off the central Strait of Georgia at a depth of 45 m (Table 17-2). In this same set, 464 walleye pollock were captured, many with lamprey scars (Fig. 17-4, centrefold, page iii). This many Pacific lamprey in one set was the largest ever recorded during these surveys.

Figure 17-2 (next page). Average annual temperature from the Strait of Georgia for surface and10m from 1969 to 2011 showing the warming trend to about 2003 followed by a cooling trend.

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Figure 17-3. Pacific lamprey CPUE showing a declining trend from 1998 to 2008 followed by an increasing trend after 2008.

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Table 17-1. Number of Pacific lamprey caught in trawl surveys (19982011). Year Catch 1998 28 1999 20 2000 15 2001 15 2002 10 2003 2 2004 1 2005 0 2006 2 2007 2 2008 0 2009 6 2010 7 2011 12 Table 17-1. Catch of Pacific lamprey off central Strait of Georgia in late June/ early July 2013. Date 27 June 30 June 2 July 2 July 3 July 4 July 4 July 4 July 5 July 6 July Total

Depth (m) 45 60 15 60 60 45 60 0 0 15

Catch 132 10 1 1 1 3 16 2 2 1 169

Pacific lamprey were captured throughout the water column, between the surface (0-15 m) and 500 m depth (Table 17-3). The greatest number of Pacific lamprey captured per set (CPUE) was 3.6 at 31-100 m depth followed by 2.4 at 101-500 m depth. The smallest CPUE was at the surface (1.3) and 16-30 m (2.2) depth.

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Table 17-3. Catch of Pacific lamprey by depth (1994 to 2002). Depth 0-15 m 16-30 m 31-100 m 101-500 m Total Average

Catch 78 20 93 47 238

Number of sets 60 9 26 20 115

CPUE 1.3 2.2 3.6 2.4 2.4

River lamprey Catches of river lamprey were higher in July (n=559) than in September (n=154) (Table 17-4). CPUE was lowest in 2005 at 0.13 and were the largest in 1999 at 1.75 (Fig. 17-5). Overall, there was a declining trend with a low CPUE from 2005 to 2011 ranging from 0.13 to 0.72 (Fig. 17-5). Table 17-4. Catch of river lamprey (1998-2011) (* only total catches available for these years). Year 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010* 2011* Total

271 16 37 64 68 103

Catch September 18 13 30 16 9 9 7 4 4 12 12 20

559

154

July 153 308 124 286 117

Total 171 321 154 302 126 9 278 20 41 76 80 123 59 74 1834

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Figure 17-5. River lamprey CPUE in the Strait of Georgia (1998-2011) showing a declining trend. There was no survey in July 2003.

The majority of river lamprey (98%) were caught in the top 30 m. The CPUE for river lamprey, 4.9, was highest at the surface (0-15 m), 1.2 at 16-30 m and 1.3 at 31-100m (Table 17-5). A total of 46 river lamprey were captured at depths greater than 30 m in a total of 33 sets for a combined CPUE of 1.4. Table 17-5. Catch of river lamprey by depth (1997 to 2002 July and September; July 2004). Depth

Catch

0-15 m 16-30 m 31-100 m 101-200 m Total Average

1942 23 35 11 2011

Number of sets 395 20 27 6 448

CPUE 4.9 1.2 1.3 1.8 2.3

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In the species distribution survey, the total catch of Pacific hake was 53,918 and 17,241 walleye pollock. CPUE of Pacific hake ranged from a low of 168 in October 2009 to a high of 2035 in September 2012 (Table 17-6). CPUE of walleye pollock ranged from a low of 19 in September 2012 to a high of 1707 in October 2013 (Table 17-6). CPUE was approximately 2.5 times higher for Pacific hake than walleye pollock over this time period. Table 17-6. Catch of Pacific hake and walleye pollock during species distribution surveys.

Date October 2009 July 2011 September 2011 September 2012 October 2013 March 2013 Total Average

Catch 1174 3929 4475 24427 4586 15327 53918

Pacific hake Number of sets 7 8 4 12 5 16 52

CPUE

Catch

168 491 1119 2035 917 958

212 320 1358 155 10245 4951 17241

948

Walleye pollock Number CPUE of sets 3 71 8 40 3 453 8 19 6 1707 14 354 42 441

Discussion Our study shows that there are trends in the catches of both Pacific lamprey and river lamprey in the Strait of Georgia. Despite the small catches, there is no indication of randomness in the catches. Pacific lamprey catches declined until there was a cooling trend in the Strait of Georgia which we propose resulted in an increase in the walleye pollock abundance, a major prey of Pacific lamprey in the Strait of Georgia. Although our study ends in 2011, we provide catch data from one cruise (2013) that shows that large numbers of Pacific lamprey are associated with schools of walleye pollock. Our species distribution surveys showed that Pacific hake were approximately 2.5 times more abundant than walleye pollock. An assessment in the early 1980s of the relative abundance of Pacific hake and walleye pollock showed that Pacific hake were approximately 16 times more abundant than walleye pollock (Thompson & McFarlane 1982). Thus, walleye pollock may have increased in abundance by about six times relative to Pacific hake abundance. We do not know the absolute abundance of walleye pollock, but it appears that there are more prey available for Pacific lamprey. It is

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not known when the abundance of walleye pollock started to increase, but it is possible that it was associated with the beginning of the cooling trend around 2004. An increasing trend in lamprey abundance about 2008 would be consistent with an increasing walleye pollock survival that started approximately 2004. Our observation of an increase in Pacific lamprey catch with increase in preferred prey is similar to the increase in Pacific lamprey catches along the west coast of North America in association with increases in Pacific hake abundances (Murauskas et al. 2013) except that the preferred prey for Pacific lamprey in the Strait of Georgia is walleye pollock and not Pacific hake. River lamprey catches were mostly in the surface waters as reported here and in Beamish (1980) and Beamish and Neville (1995). The dominant prey of Pacific lamprey are Pacific herring (Beamish & Neville 1995) with young-of-the-year Pacific herring found mostly found in the surface waters of the Strait of Georgia (Beamish et al 2012). Actively feeding river lamprey in schools of Pacific herring is commonly observed in the Strait of Georgia (Beamish 1980).

Figure 17-6. Average CPUE (by weight) for age-0 Pacific herring (1991-2011) in the Strait of Georgia showing a declining trend beginning about 1998.

The relative abundance of young-of-the-year Pacific herring have been determined by the Department of Fisheries and Oceans Canada’s Strait of Georgia juvenile herring and nearshore ecosystem survey from 1991 to 2011 (Jennifer Boldt, personal communication). The average CPUE, by

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weight, for young-of-the-year Pacific herring follows a distinct pattern of alternating highs and lows with a declining trend beginning in 1998 (Fig. 17-6). The declining trend in CPUE of river lamprey is consistent with the declining trend in CPUE of young-of-the-year Pacific herring. The declining trend in the survival of young-of-the-year Pacific herring remains to be explained. The alternating pattern of an increased and decreased survival also is not understood. The abundance of adult Pacific herring in the Strait of Georgia is increasing (DFO 2015) and if accurate monitoring of feeding river lamprey could occur, it would be most interesting to see if their abundance increases. Murauskas et al. (2013) found a correlation between the abundance of returning adult Pacific lamprey and prey in the commercial fisheries off the coast in the United States (US) Pacific Northwest. In contrast, Siwicke (2014) found that there were no significant positive correlations between CPUE of any of the 10 potential hosts and Pacific lamprey examined in trawl studies conducted in the Bering Sea area. However, Pacific cod (Gadus macrocephalus) and Greenland halibut (Reinhardtius hippoglossoides) had the greatest positive correlation coefficients although still not significant (Siwicke 2014). Abundances of feeding juvenile lampreys could be related to the number of ammocoetes and to predation on the metamorphosed juveniles when they are in the ocean. Our analysis does not include predation effects but focuses on the changes in the abundances of the major prey of Pacific lamprey and Pacific herring for river lamprey. We know that river lamprey ammocoetes are extremely abundant in the lower Fraser River (Beamish & Youson 1987) and we also know that Pacific lamprey ammocoetes are common to most rivers around the Strait of Georgia (R. Beamish, personal observations). Thus, although ammocoete abundance and predation within the Strait of Georgia can influence the abundance of feeding juveniles, we suggest that the abundances of river lamprey and Pacific lamprey in the Strait of Georgia is closely related to the abundances of their preferred prey.

Acknowledgements We would like to thank Rusty Sweeting, Chrys Neville and Lana Fitzpatrick for the collection of samples.

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References Beamish R. J. 1980. Adult biology of the river lamprey (Lampetra ayresi) and the Pacific lamprey (Lampetra tridentata) from the Pacific coast of Canada. Canadian Journal of Fisheries and Aquatic Sciences 37, 1906-1923. Beamish R.J. 1982. Lampetra macrostoma, a new species of freshwater parasitic lamprey from the west coast of Canada. Canadian Journal of Fisheries and Aquatic Sciences 39, 277-287. Beamish R.J. 2010. Use of gill pore papillae in the taxonomy of lampreys. Copeia 2010, 618-628. Beamish R.J., & Levings C.D. 1991. Abundance and freshwater migrations of the anadromous parasitic lamprey, Lampetra tridentata, in a tributary of the Fraser River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 48, 1250-1263. Beamish R.J., Noakes D., McFarlane G., Pinnix W., Sweeting R., King J. & Folkes M. 1998. Trends in coho marine survival in relation to the regime concept. Canadian Stock Assessment Secretariat Research Document 98, 1-171. Beamish R.J. and Northcote T.G. 1989. Extinction of a population of anadromous parasitic lamprey, Lampetra tridentata, upstream of an impassable dam. Canadian Journal of Fisheries and Aquatic Sciences 46, 420-425. Beamish R.J. & Youson J.H. 1987. Life history and abundance of young adult Lampetra ayresi in the Fraser River and their possible impact on salmon and herring stocks in the Strait of Georgia. Canadian Journal of Fisheries and Aquatic Sciences 44, 525-537. Beamish R.J. & Neville C-E. M. 1995. Pacific salmon and Pacific herring mortalities in the Fraser River plume caused by river lamprey (Lampetra ayresi). Canadian Journal of Fisheries and Aquatic Sciences 52, 644-650. Beamish R.J. & Williams N.E. 1976. A preliminary report on the effects of river lamprey (Lampetra ayresi) predation on salmon and herring stocks. Fisheries and Marine Service Technical Report 611, 1-26. Beamish R.J., McCaughran D., King J.R., Sweeting R.M. & McFarlane G.A. 2000. Estimating the abundance of juvenile coho salmon in the Strait of Georgia by means of surface trawls. North American Journal of Fisheries Management 20, 369-375. Beamish R.J., Neville C., Sweeting R. & Lange K. 2012. A synchronous failure of juvenile Pacific salmon and herring production in the Strait of Georgia in 2007 and the poor return of sockeye salmon to the Fraser

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River in 2009. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 4, 403-414. Beamish R.J. Sweeting R.M., Lange K.L, Noakes D.J., Preikshot D. & Neville C.M. 2010. Early marine survival of coho salmon in the Strait of Georgia declines to very low levels. Marine and Coastal Fisheries: Dynamics, Management and Ecosystem Science 2, 424-439. Clarke W.C. & Beamish R.J. 1988. Response of recently metamorphosed anadromous parasitic lamprey (Lampetra tridentata) to confinement in fresh water. Canadian Journal of Fisheries and Aquatic Sciences 45, 42-47. Duffy E.J. & Beauchamp D.A. 2011. Rapid growth in the early marine period improves the marine survival of Chinook salmon (Oncorhynchus tshawytscha) in Puget Sound, Washington. Canadian Journal of Fisheries and Aquatic Sciences 68, 232-240. DFO. 2015. Stock assessment and management advice for British Columbia Pacific Herring: 2014 status and 2015 forecast. DFO Canadian Science Advisory Secretariat Science Advisory Report 2014/060, 1-21. Fissel D.B., Birch, J.R. & Chave R.A.J. 1991. Measurements of temperature, salinity and sound velocity at the Nanoose Bay Naval Underwater Weapons Test Range, 1967-1984: updated March 1991 to include 1985-1989, Appendix 4. Sidney, B.C.: Arctic Sciences Ltd. Hayes M.C., Hays R., Rubin S.P., Chase D.M., Hallock M., Cook-Tabor C., Luzier C.W. & Moser, M.L. 2013. Distribution of Pacific lamprey Entosphenus tridentatus in watersheds of Puget Sound based on smolt monitoring dHata. Northwest Science 87, 95-105. Klamath-Siskiyou Wildlands Center and 10 other conservation organizations. 2003. A petition for rules to list: Pacific lamprey (Lampetra tridentata); river lamprey (Lampetra ayresii); western brook lamprey (Lampetra richardsoni) and Kern brook lamprey (Lampetra hubbsi) as threatened or endangered under the Endangered Species Act. Ashland, Oregon: Klamath-Siskiyou Wildlands Center. Luzier C.W., Schaller H.A., Brostrom J.K., Cook-Tabor C., Goodman D.H., Nelle R.D., Ostrand K. & Streif, B. 2011. Pacific lamprey (Entosphenus tridentatus) assessment and template for conservation measures. Portland, Oregon: U.S. Fish and Wildlife Service. Mayfield M.P., Schultz L.D., Wyss L.A., Clemens B.J. & Schreck C.B. 2014. Spawning patterns of Pacific lamprey in tributaries to the Willamette River, Oregon, USA. Transactions of the American Fisheries Society 143, 1544-1554.

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Mecklenburg C.W., Mechlenburg T.A. & Thorsteinson L.K. 2002. Fishes of Alaska. Bethesda: American Fisheries Society. Murauskas J.G., Orlov A.M. & Siwicke K.A. 2013. Relationships between the abundance of Pacific lamprey in the Columbia River and their common hosts in the marine environment. Transactions of the American Fisheries Society 142, 143-155. Renaud C.B. 2011. Lampreys of the world. An annotated and illustrated catalogue of lamprey species known to date. Rome: FAO. Ruggerone G.T. & Goetz F.A. 2004. Survival of Puget Sound Chinook salmon (Oncorhynchus tshawytscha) in response to climate-induced competition with pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 61, 1756-1770. Scott W.B. & Crossmann E.J. 1973. Freshwater Fishes of Canada. Fisheries Research Board of Canada Bulletin 184 966pp. Siwicke K.A. 2014. Relationships between anadromous lampreys and their host fishes in the eastern Bering Sea. M.S. Thesis. University of Alaska Fairbanks. Swain D.P., Riddell B.E. & Murray C.B. 1991. Morphological differences between hatchery and wild populations of coho salmon (Oncorhynchus kistuch): environmental versus genetic origin. Canadian Journal of Fisheries and Aquatic Sciences 48, 1783-1791. Thompson M. & McFarlane G.A. 1982. Distribution and abundance of Pacific hake and walleye pollock in the Strait of Georgia, March 24May 2, 1981. Canadian Manuscript Report of Fisheries and Aquatic Sciences 1661, 1-79.

CHAPTER EIGHTEEN TRENDS OF PACIFIC LAMPREY POPULATIONS ACROSS A BROAD GEOGRAPHIC RANGE IN THE NORTH PACIFIC OCEAN, 1939-2014 JOSHUA MURAUSKAS, LUKE SCHULTZ AND ALEXEI ORLOV

Background and management interest The Pacific lamprey Entosphenus tridentatus is a parasitic anadromous lamprey (Petromyzontidae) found along coastal regions of North America and Asia. The reported latitudinal range (> 50°) of Pacific lamprey is greater than any other lamprey in the world, with observations ranging from Alaska to Mexico in the eastern Pacific Ocean, and from Russia to Japan in the western Pacific Ocean (Link et al. 2001; Renaud 2008; Orlov et al. 2009). Pacific lamprey reside in freshwater as filter feeding larvae for several years, followed by metamorphosis and migration to marine environments where they feed on other fishes until maturity (Clemens et al. 2010). Research suggests that they lack home stream fidelity, instead relying on larval pheromones to select spawning locations, similar to other lampreys (Lin et al. 2008; Spice et al. 2012; Hess et al. 2014). The primary distribution of Pacific lamprey is thought to be along the Pacific coast of North America (Renaud 2011; Spice et al. 2012), but it is also encountered in coastal Russia (Orlov et al. 2008), Mexico (Renaud 2008), and Japan (Yamazaki et al. 2005). Regional Pacific lamprey fisheries have existed for centuries. Native American Tribes in the Columbia River Basin (U.S. Pacific Northwest) have ongoing traditions of harvesting lampreys for consumption, medicinal, and ceremonial purposes (Close et al. 2002). Other historic uses of lamprey include vitamin oil, export to Europe for human consumption, fishing and trapping bait, and fishmeal for aquaculture, livestock and

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poultry (Renaud 2008). Appreciable fishing of adult lampreys in the Columbia River Basin occurred through at least the 1940s where harvest numbers sometimes exceeded 500,000 adults at Willamette Falls, Oregon (Fig. 18-1; Ward 2001). Current harvest numbers are only a fraction of historical records, concurrent with a reduction in Pacific lamprey abundance since the mid-1900s (Murauskas et al. 2013, Baker et al. 2015). Nonetheless, some tribes consider harvest of Pacific lamprey an important component of their cultural heritage (CRITFC 2011).

Figure 18-1. This photo was taken at Willamette Falls, Oregon in 1913 and illustrates the historical abundance of Pacific lamprey at this traditional harvest location (photo provided by Kathryn Kostow, Oregon Department of Fish and Wildlife).

Substantial conservation measures to protect Pacific lamprey have been implemented in recent years, predominantly in the Columbia River Basin (Close et al. 2002; CRITFC 2011). For example, more than $50M has been allocated to improve passage at federal hydroelectric projects alone (USACE 2009). Additional research continues to develop monitoring techniques for juveniles (Mueller et al. 2006; Mesa et al. 2012), implement adult translocation programs (Ward et al. 2012), and plan artificial propagation programs to supplement wild populations (CRITFC 2011). Despite substantial efforts to conserve Pacific lamprey in the freshwater environment, survival in the marine environment has received little attention. Considering that adult abundance has been related to availability of hosts in the marine environment, additional information

Trends of Pacific Lamprey Populations, 1939-2014

75

on population trends throughout the Pacific Ocean is needed to better identify limiting factors for the species and aid in its conservation (Murauskas et al. 2013). Given the scientific uncertainty surrounding the perceived reduction in abundance of Pacific lamprey, it is evident that better accounting for adult abundance would inform population trends within a broader context. Although long-term datasets for Pacific lamprey are less complete than many other fishes, adult Pacific lamprey are monitored in some river basins on the Pacific Coast of North America. Further, researchers started monitoring the abundance of adult Pacific lamprey in ocean trawls during the late 1900s, largely to account for lamprey-caused mortalities incurred to commercially valuable marine fishes (Orlov et al. 2008, 2009; Shevlyakov & Parensky 2010). Despite limitations, these data provide an opportunity to examine the marine ecology of Pacific lamprey. We present these indices to examine annual patterns in abundance of Pacific lamprey across a range of habitats. Specifically, discordant trends in Pacific lamprey abundance across varying locations might suggest that localized conditions drive abundance and that some degree of natal stream fidelity exists, whereas similar trends in abundance across broad expanses would refute this hypothesis. This information may improve the understanding of Pacific lamprey population dynamics and can be used to develop additional research questions to inform conservation needs.

Records of abundance Enumeration of adult Pacific lamprey has been relatively uncommon throughout its entire range. This is likely a result of its negligible commercial value and the reputation of parasitic lampreys for negatively impacting commercially-important fisheries (Beamish & Levings 1991), difficulties associated with interpreting spawning survey information (Moser et al. 2007, Mayfield et al. 2014), and a negative perception due to it being associated with invasive sea lamprey Petromyzon marinus in the Laurentian Great Lakes (Clemens et al. 2010). Despite the lack of targeted survey information (e.g., Chase et al. 2009), the distribution of adult Pacific lamprey in the ocean overlaps many commercially-valuable fishes (Orlov et al. 2008), and its distribution in freshwater during spawning and early rearing overlaps with many routinely-monitored Pacific salmon populations (Beamish 1980; Nehlsen 1997). We identified seven datasets spanning roughly 20° of latitude that include abundance metrics of marine or spawning phase Pacific lamprey (Table 18-1). These data include counts in fish ladders in three different river basins, trawl surveys in both

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the Western and Eastern Pacific Ocean, fishwheel counts from one river basin, and spawning ground surveys from an additional river basin. Although these measures of adult abundance have various limitations, these data represent some of the only available insight to population trends of Pacific lamprey throughout its distribution. Counts at Fish Ladders – Adult return sizes in rivers with hydroelectric projects can be measured directly by counting adults that ascend fish ladders. Count stations generally consist of a confinement structure in the ladder where fish are forced to swim past a viewing window, and fishes are enumerated by a counter or recorded in video archives for later counting. Although Pacific lamprey dam counts can be biased (e.g., when nighttime passage is not monitored), they represent the longest time series of abundance at many locations and are often considered acceptable indicators of population trends (Kostow 2002; Clabough et al. 2012; Murauskas et al. 2013). Pacific lamprey records were available from three unique river systems in the Western U.S. that represent a long time series in the Columbia, Umpqua, and Rogue rivers (Fig. 18-2). The Columbia River Basin (46° 14’ N) spans more than 640,000 km2, with is headwaters in western Canada and is the fourth largest river in the U.S. when it empties into the Pacific Ocean on the Oregon-Washington border. Intense fishing pressure in the 1870s initiated a substantial decline in the abundance of Pacific salmon and steelhead, and declines were later exacerbated by impacts to freshwater habitats as a result of agriculture, ranching, mining, timber harvest, and urbanization practices. The construction of several mainstem hydroelectric projects beginning in the 1930s further altered migratory pathways and significantly reduced access to spawning and rearing habitat for anadromous fishes, consequently reducing their abundance (McClure et al. 2003). Counts of Pacific lamprey have been collected at Bonneville Dam (river km 233) since 1939 and represent the longest time series of abundance throughout its range (though a data gap exists between 1970 and 1997; Fig. 18-3). The Umpqua River Basin (43° 40’N) spans nearly 13,000 km2 in the central coast of Oregon, U.S., and the basin is moderately developed for commercial timber harvest and agriculture (Benke et al. 2011). Winchester Dam (river km 190), the lowest dam the basin, was constructed on the North Fork Umpqua River in 1907 and is the only identified location with a continuous record of adult Pacific lamprey passage since 1965 (Lampman 2011). Finally, the Rogue River Basin (42° 25’ N) drains over 13,000 km2 west of the Cascade Mountains in Oregon, U.S. (Benke & Cushing 2011), and has similar development patterns as the Umpqua River. Gold Ray

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77

Dam (river km 202) was constructed in the early 1900s, and later outfitted with a fish ladder and counting station. Counts of adult Pacific lamprey ascending the fish ladder were recorded from 1993 until 2010, when the dam was removed concomitantly with two smaller dams upstream and downstream of Gold Ray Dam (personal communication, Kathryn Kostow, Oregon Department of Fish and Wildlife).

Figure 18-2. Locations of surveys that provide indices of adult Pacific Lamprey abundance throughout their range in the Pacific Ocean.

Trawl surveys – Deep water trawls are commonly used to monitor groundfish and Pacific salmon abundance in the northern Pacific Ocean (Weinberg et al. 1994; Orlov et al. 2008). These surveys are often designed to be consistent across years and can be used to expand catch into estimates of abundance. Although gear efficiency with trawls is difficult to quantify (Beamish et al. 2000), adult lampreys are regularly encountered in surveys throughout the North Pacific Ocean and provide valuable insight to its marine phase. Trawl survey data collected off the coast of Russia in the Western Pacific Ocean (1977-2005) and off the coast of Alaska, U.S. in the Eastern Pacific Ocean (2002-2012) have been used to examine trends in abundance of lampreys (Orlov et al. 2008; Siwicke 2014; Fig. 18-2). In both surveys, bottom and variable-depth

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trawls were used and catch per unit effort was standardized to a mass per unit of area swept by the trawl (e.g., kg/ha). The reported measure of Pacific lamprey catch per unit effort across survey years is used here as an index of annual abundance. Fish wheels – Fish wheels have been used for research and monitoring of Pacific salmon for several decades (Meehan 1961). We used fishwheel data from the free-flowing Nass River (54° 58’ N) – a sparsely populated system that drains over 20,000 km2 in British Columbia and hosts abundant runs of wild Pacific salmon and Pacific lamprey (Benke & Cushing 2011). Considerable numbers of Pacific lamprey are encountered each year in fish wheels used by the indigenous Nisg’a Nation’s fish department, representing a time series extending more than 20 years (i.e., 1994-2012). Although rigorous estimates based on mark-recapture events do not include Pacific lamprey, the number of lampreys captured per day per fish wheel is recorded. These data were used as an index of annual adult returns in the Nass River. Spawning ground surveys – The abundance of adult anadromous fishes is commonly estimated by visual surveys of gravel nests (redds) in spawning tributaries (Gallaher et al. 2007). Redd surveys are typically used to monitor spawning escapement of Pacific salmon populations, but have recently been used to monitor Pacific lamprey populations in some locations (Luzier et al. 2011; Mayfield et al. 2014). While challenges in redd surveys, such as observer efficiency and assumptions about the number of fish per redd and proper identification of redds also apply to Pacific lamprey evaluations, they represent an opportunity to track abundance in systems without other means of quantifying return size (e.g., dam counts). The Chehalis River (46° 27’ N) has a drainage area of 5,709 km2 in western Washington State, U.S. While the mainstem river is unobstructed by dams, the area is modified by agriculture, municipal, and industrial uses (Fresh et al. 2003). Annual spawning ground surveys were conducted to monitor steelhead Oncorhynchus mykiss populations and Pacific lamprey redds between 2005 and 2010 (Luzier et al. 2011). Total Pacific lamprey redd counts for each year are used as an index of spawner abundance.

79

57,928 32,693 45,110 26,203 47,129 40,986 42,603 49,911

1950

1951

1952

1953

1954

1955

1956

74,825

1949

36,488

1946

94,326

36,209

1945

143,815

51,096

1944

1948

52,361

1943

1947

64,954

1942

Columbia R.

1941

Chehalis R. 156,102

Nass R.

1940

Alaska 227,122

Russia

1939

Year

Umpqua R.

Rogue R.

Table 18-1. Records of Pacific lamprey abundance from various locations. Data from Russia and Alaska represent kg per hectare trawled (Orlov et al. 2008; Siwicke 2014) and data from the Nass River represent total lampreys per day per fishwheel. Data from the Chehalis, Columbia, Umpqua, and Rogue rivers represent direct counts of redds or adult lampreys.

Trends of Pacific Lamprey Populations, 1939-2014

80 Alaska

Nass R.

Chehalis R.

Columbia R.

2,996

0.00

1978

1,512

2,628

2,540

1.14

1,556

1975

1977

9,455

1974

1976

7,262

1973

27,297

17,896

29,175

379,509

1969

14,532

1972

109,029

1968

46,785

30,427

66,171

1967

37,566

1971

67,914

1966

Umpqua R.

1970

108,987

1965

1962 87,937

101,426

1961

104,337

364,805

1960

1964

177,898

1959

1963

98,419 215,083

1958

53,031

Russia

1957

Year

Chapter Eighteen Rogue R.

Russia

0.35

0.09

0.68

0.00

0.32

0.61

1.63

0.61

0.43

0.41

0.07

0.39

0.31

0.61

0.37

1.40

0.17

0.24

0.49

0.58

0.30

0.30

Year

1979

1980

1981

1982

1983

1984

1985

1986

1987

1988

1989

1990

1991

1992

1993

1994

1995

1996

1997

1998

1999

2000

Alaska

0.423

0.402

0.485

0.933

0.828

0.230

0.128

Nass R.

Chehalis R.

19,002

37,296

37,515

20,891

Columbia R.

Trends of Pacific Lamprey Populations, 1939-2014

35

26

144

15

80

54

428

472

879

472

1,129

660

1,171

1,857

2,726

13,463

1,034

1,591

7,080

877

1,665

1,874

Umpqua R.

960

523

705

710

2,370

732

155

346

Rogue R.

81

82

8.6

1.005

2.073

31,953

2014

29,224

18,315

6,234

8,622

14,562

19,313

38,938

26,664

61,780

117,029

100,476

27,947

Columbia R.

23,970

1.272

267

200

386

496

552

344

Chehalis R.

2013

1.170

2012

9.3

2011

0.462

2010

8.6

0.782

2009

0.426

0.53

2005

12.6

2008

0.87

2004

1.880

0.385

0.536

1.85

2003

18.4

0.401

Nass R.

0.695

0.64

2002

Alaska

2007

0.54

2001

2006

Russia

Year

Chapter Eighteen

1044

175

57

83

495

31

156

172

47

41

203

38

34

Umpqua R.

30

10

175

1

82

378

376

424

239

Rogue R.

Trends of Pacific Lamprey Populations, 1939-2014

83

Comparison of indices These observations of Pacific lamprey represent different life stages from freshwater and marine habitats. Adult Pacific lamprey are encountered in the ocean throughout the year (Orlov et al. 2008), enter estuarine habitats between January and March (Weitkamp et al. 2015), pass hydropower facilities between May and October, and hold in freshwater until the following spring to spawn (Clemens et al. 2010, Starcevich et al. 2013). Although length data from marine collections were not available, it was assumed that individuals collected from marine habitats represent a life stage roughly one year prior to adult returns enumerated at lower river fish wheels or ladders. Conversely, spawning surveys provide an index of abundance for the year after freshwater entry when most fish ladder counts are collected. To correct for this discrepancy, data were adjusted to best approximate the year that individual fish from that age class would have returned to freshwater (“run year”; i.e., we adjusted marine catches by adding a year to their collection, redd counts by subtracting a year from their counts). Metrics of abundance also varied greatly with each gear type or location which inhibited comparisons across systems. Therefore, data were standardized to graph trends across gears and locations at a similar scale. To do this, the values from each time series were scaled between 0 and 1. For each dataset, each individual datum (i.e., each year in each habitat) was divided by the maximum value in the dataset. Each time series therefore includes a maximum value of 1 (i.e., the year with the highest recorded abundance metric) and all locations have an identical y-axis scale to facilitate comparison (Fig. 18-3). Plots of these data were constructed to examine trends in abundance across years. In addition, only two of the datasets included continuous data from pre-1994, so separate plots were constructed that included data from post-1994, and each dataset (i.e., location) was scaled relative to the maximum datum from 1994-2014 as described above (Fig. 18-4). Several patterns were evident from an examination of trends in Pacific lamprey abundance across these systems. First, abundance of Pacific lamprey has declined by an order of magnitude (Columbia River) or two orders of magnitude (Umpqua River) from peak counts in the two river systems that have data from several decades. However, quantifying declines in abundance is difficult without knowing if abundance of Pacific lamprey during the 1960s was unusually high. The Umpqua River is the only location where a declining trend over time is clearly evident (Fig. 18-3). Secondly, similar trends of Pacific lamprey abundance since the

Chapter Eighteen

84

Russia

0.9 0.6 0.3 0.0

Alaska

0.9 0.6 0.3 0.0

Nass R

0.9 0.6 0.3

Chehalis R

0.0 0.9 0.6 0.3

Columbia R

0.9

Umpqua R

0.0

0.9

0.6 0.3 0.0

0.6 0.3

Rogue R

0.0 0.9 0.6 0.3 0.0 1930

1940

1950

1960

1970

1980

1990

2000

2010

Year

Figure 18-3. Trends in adult Pacific lamprey abundance from two locations in the Pacific Ocean (top two) and five river basins (bottom five). Data were standardized to facilitate comparisons. Linear trends are shown and confidence limits are shaded.

mid-1990s were apparent across diverse habitats and geographic locations. For example, data collected in Russia, the Nass River, and the Columbia River peaked in the early 2000s, followed by declines ranging from 71%

2020

Trends of Pacific Lamprey Populations, 1939-2014

85

to 93% (Fig. 18-4). This pattern was observed in the five most northerly locations, suggesting that broad-scale environmental conditions were conducive to Pacific lamprey abundance during the early 2000s. Finally, examination of the data indicated an interesting inter-annual pattern during multiple time series. In years with a relatively high abundance, there were generally relatively low indices in the preceding and following years (Fig. 18-5).

Figure 18-4. Trends in abundance of Pacific lamprey from Russia, the Nass River, and Columbia River display similar patterns between 1996 and present despite the difference in habitat and geographic locations.

Figure 18-5 (next page). Trends in Pacific lamprey abundance from various locations and time periods often show smaller peaks before and after a year of peak abundance (shown with shaded circles). Panels include 12-year periods from (A) Russia, (B) the Nass River, (C and D) the Columbia River, (E) the Umpqua River, and (F) the Rogue River.

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Trends of Pacific Lamprey Populations, 1939-2014

87

Conclusions Present-day abundance of Pacific lamprey in the seven areas reviewed appears to be highly variable and some populations exhibit similar temporal patterns across a broad geographic range and varying freshwater habitat conditions. The decrease in abundance from peaks observed in the mid-1900s in the Columbia and Umpqua rivers supports the perception that the abundance of Pacific lamprey has decreased in the U.S. (Luzier et al. 2011), though trends are otherwise inconclusive or increasing. Suggesting that Pacific lamprey are at risk of extinction (Close et al. 2002) therefore appears premature based on the limited historical context and available indices of abundance. A lack of continuous trend data in any system further complicates the ability to evaluate factors operating in the decline. For example, the severe reduction in numbers of Pacific lamprey returning to the Umpqua River parallels the completion of four Snake River dams that have been implicated as a major factor in Pacific salmon declines in the Columbia River (Kareiva et al. 2000), but additional data are not available to corroborate the hypothesis. The similarity among population trends in some instances supports the concept that abundance of adult Pacific lamprey is linked with conditions experienced during the marine phase of the life cycle (Murauskas et al. 2013; Siwicke 2014). Research on sea lamprey in the Great Lakes suggests that parasitic lampreys are well-mixed and driven by host abundance (Young et al. 1996; Howe et al. 2012). Regardless of the mechanism, these data support the hypothesis that conditions in the marine environment exert a strong influence on the abundance of Pacific lamprey and may negate variation in survival during residence in freshwater. Although there is convincing evidence that the marine environment is closely related to Pacific lamprey abundance, a mechanistic understanding of how ocean conditions influence population dynamics is lacking. In particular, it is not known whether ocean conditions function to effectively set a given marine survival rate or a given marine carrying capacity. These two contrasting hypotheses have important implications for Pacific lamprey conservation. If marine conditions specify a given carrying capacity, then freshwater conditions likely become largely irrelevant once enough juveniles are produced to reach the carrying capacity of the marine environment. Conversely, if marine conditions determine a given rate of survival, improved freshwater conditions could increase abundance of adults via higher juvenile production. However, it is plausible that survival in the ocean would exert a stronger relative influence on population

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dynamics as seen in other anadromous fishes in the Pacific Ocean (e.g., Ryding & Skalski 1999). The life history of Pacific lamprey presents several challenges to understanding mechanisms behind their population dynamics. Evidence that Pacific lamprey have diverse age structures (e.g., Kan 1975, Beamish & Levings 1991), lack natal stream fidelity (Spice et al. 2012), utilize multiple habitats with unique threats (Close et al. 2003), are able to withstand conditions known to cause mortality to other juvenile fishes (Colotelo et al. 2012), are long-lived (Potter 1980), and can survive multiple years without feeding (Whyte et al. 1993) suggests that they are opportunistic generalists that should be fairly resilient in the face of multiple threats (Clemens et al. 2013). Despite this, these data suggest abundance varies widely in all locations and identifying factors that influence population dynamics for Pacific lamprey may be inherently challenging. However, at least two studies have demonstrated a convincing link between host availability during the early parasitic phase and abundance of anadromous lampreys (Young et al. 1996; Murauskas et al. 2013). Furthermore, active research in freshwater systems has greatly expanded the understanding of dam passage (e.g., Keefer et al 2002), rearing habitat needs (Torgersen & Close 2004, Jolley et al. 2012, Schultz et al. 2014), monitoring approaches (Moser et al. 2007, Mayfield et al. 2014), and threats posed to outmigrants (Moser et al. 2014). Despite challenges, concerted research efforts into the ecology of Pacific lamprey throughout its range might better describe its entire life cycle and inform conservation of the species. Although several consistent trends were apparent among datasets, the two southernmost datasets were dissimilar enough to warrant discussion. The Rogue River experienced a small peak in adult returns during the mid1990s, while adult counts in the Umpqua River remained at less than 1% of the historical maximum for over twenty consecutive years. It is possible that large-scale climatic changes may influence spawning success in the freshwater environment associated with warming trends, as has been postulated for sea lamprey (Holmes 1990). This hypothesis is largely based on evidence from the wide variation in egg hatching success with increased temperature in multiple lamprey species (Smith & Mardsen 2009; Meeuwig et al. 2005). However, detecting these responses would be difficult because of the diversity in duration of freshwater residence may mask this occurrence (i.e., the 3-7 year larval phase; Potter 1980; Morkert et al. 1998), and spawning survey data suggest that the phenology of Pacific lamprey spawning changes with inter-annual water temperature patterns (Mayfield et al. 2014). Broader oceanographic patterns may also

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explain variable returns to river basins in southern Oregon. The convergence of the three primary marine currents along the Pacific Coast (i.e., the Alaska Current, the California Current, and the North Pacific Current) can occur in the vicinity of the mouth of these rivers (Hickey 1979), and might greatly influence migratory patterns and productivity, and their inter-annual variation. In addition, biomass of Pacific hake Merluccius productus, a host species whose abundance closely correlates with Pacific lamprey (Murauskas et al. 2013) and migrate extensively through the California Current System, has declined steadily since the late1980s due to exploitation of the fishery (Ressler et al. 2007). The spatial distribution of Pacific hake appears to have shifted northward in the last 25 years, so it is possible that these dynamics influence Pacific lamprey. The most recent survey information in California suggests that the distribution of Pacific lamprey has shifted northward on the coast, with no known populations currently south of Big Sur (36.24° N; Reid & Goodman 2015). The interpretation of Pacific lamprey abundance here assumes reliability in in the data provided, particularly when comparing data derived from different collection methods. These data do contain several limitations that we attempted to address in our analyses, and some of these limitations precluded strong inferences. However, we assumed that dam counts, fish wheels and redd surveys were acquired using similar annual effort for collection across all years. Despite these limitations, certain characteristics support that the apparent trends are valid. A wide range between minimum and maximum values and substantial inter-annual variation was evident in all indices of abundance. Signs of autocorrelation between subsequent years also support previous suggestions that Pacific lamprey may experience periodic population cycles (Murauskas et al. 2013). Collectively, it seems unlikely that these trends are inaccurate representations of Pacific lamprey abundance that coincidentally have a high degree of correlation, including unique trend characteristics. In conclusion, it is clear that abundance of Pacific lamprey throughout the locations examined has high temporal variability and some locations have experienced substantial declines in abundance. However, of the datasets spanning more than two decades, indiscernible or increasing patterns are also apparent. Thus, the notion that Pacific lamprey are experiencing a decline in abundance throughout their range is not supported by these data. It is also apparent that trends in the most recent decades show similar patterns in abundance across many regions despite very different anthropogenic and environmental conditions, suggesting that large-scale influences might be the contemporary driver of abundance over a vast geographic range (e.g., Russia, Nass and Columbia rivers; Fig.

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18-4). Given the increasing level of conservation interest in Pacific lamprey (Chase et al. 2009), better documentation of abundance throughout its range will be required to truly understand population dynamics. In particular, these data suggest that insight into the marine ecology is needed to comprehensively understand the life cycle and adult returns of Pacific lamprey. Given that the infrastructure is already in place to monitor the abundance of Pacific salmon and various groundfishes throughout the Pacific Ocean, a concerted effort to monitor lamprey observations would require a relatively small incremental increase in effort. Improved international coordination and survey designs might also eventually lead to more accurate conclusions on the effects of freshwater and marine environments on anadromous lampreys, therefore improving management strategies.

Acknowledgments We thank many friends and colleagues for providing valuable information on Pacific lamprey abundance. Kathryn Kostow (Oregon Department of Fish and Wildlife) helped to obtain dam counts from the Umpqua and Rogue rivers in Oregon. Curt Holt (Washington Department of Fish and Wildlife) and Carrie Cook-Tabor (US Fish and Wildlife Service) provided redd counts from the Chehalis River. Fishwheels on the Nass River are operated by the Nisga’a Fisheries Management Program. Trawl survey data were made available through the National Marine Fisheries Service and multiple research centers in Russia. Kevin Siwicke provided information on Alaskan trawl data and we thank Richard Alexander (LGL Limited) for bringing Pacific lamprey counts in Canada to our attention. Joy Wade of Fundy Aqua, Dick Beamish (retired), Beau Patterson of Douglas Public Utility District, and Steve Hemstrom of Chelan Public Utility District provided valuable suggestions to improve the presentation of these data. Charles Kiblinger of Anchor QEA assisted in mapping the sampling locations. Conversations with Carl Schreck and Steve Whitlock of the Oregon Cooperative Fish and Wildlife Research Unit greatly helped the focus the content of this work.

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CHAPTER NINETEEN OBSERVATIONS ON THE CATCH AND BIOLOGY OF PACIFIC HAGFISH (EPTATRETUS STOUTII) FROM AN EXPLORATORY FISHERY IN NORTHWEST MEXICO J. FERNANDO MÁRQUEZ–FARÍAS, RAÚL LARA–MENDOZA, OSCAR ZAMORA–GARCÍA AND EVLIN RAMÍREZ–FÉLIX

Introduction The Pacific hagfish (Eptatretus stoutii) and the dark hagfish (E. deani) occur in the North-Eastern Pacific. These two species in the Myxinidae family, are primitive fish that have a cartilaginous skeleton and lack eyes, jaws, scales and paired fins (Clark & Summers 2007). The Pacific hagfish is the most abundant species, supporting a fishery in the USA and Canada. It is distributed over the Eastern-Pacific coast, from southeastern Alaska to Punta San Pablo, Baja California (BC), Mexico. The preferable habitats are silt and clay bottoms with depths ranging from 16–966 m, a nearbottom salinity ranging from 31–32 ups and water temperatures 500 kg/set) were observed offshore of San Carlos and Punta Canoas. The variability of the catch is difficult to explain. No clear pattern of higher catch in a particular zone was observed (Fig. 19-7).

Chapter Nineteen

A

Trip 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Ship 1 8 10 10 11 8 12 10 12 11 10 9 14 12 2 14 14 14 14 12 8 10 8

Ship 2 7 8 10 10 6 14 2 12 6 10 8 9 10 14 1 7 6 6 12 14 11 10

Total 15 18 20 21 14 26 12 24 17 20 17 23 22 16 15 21 20 20 24 22 21 18

B

2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Trip

Ship 1 2320 2760 3310 2870 2560 3030 2340 2550 2600 2470 2200 2470 2680 410 2560 2510 2630 3100 3500 2780 3050 2600

Ship 2 2500 2530 2700 2470 1650 2780 620 2070 1350 3100 3000 3040 3100 3160 400 2300 850 1000 2700 2200 2350 2500

Total 4820 5290 6010 5340 4210 5810 2960 4620 3950 5570 5200 5510 5780 3570 2960 4810 3480 4100 6200 4980 5400 5100

C Trip 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Ship 1 290 276 331 261 320 253 234 213 236 247 244 176 223 205 183 179 188 221 292 348 305 325

Ship 2 357 316 270 247 275 199 310 173 225 310 375 338 310 226 400 329 142 167 225 157 214 250

Total 321 294 301 254 301 223 247 193 232 279 306 240 263 223 197 229 174 205 258 226 257 283

Table 19-2. Number of sets per trip by ship (a); catch per trip by ship (b) and catch rate (catch per set) per trip by ship (c) from June 2013 to September 2014.

106

23 24 25 26 27 28 29 Total Mean

257 10.7

8 16

7 7 8 10 12 7 12 256 8.8

15 23 8 10 12 7 12 513 17.7

23 24 25 26 27 28 29 Total Mean 63430 2643

3080 3050

2420 3286 3500 5000 3000 2200 2100 69876 2410

5500 6336 3500 5000 3000 2200 2100 133306 4597

Observations on the Catch and Biology of Pacific Hagfish 23 24 25 26 27 28 29 Total Mean 247 258

385 191

346 469 438 500 250 314 175 273 268

367 275 438 500 250 314 175 85150 255

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Table 19-3. Frequency of sets per trap type and soak time (A); frequency of sets per type of trap and depth (intervals of 100 m) (B); catch per type of trap and soak time (C); catch per type of trap and depth (intervals of 100 m) (D). Soak time (x 24 hr) Total 1 2 3 4 5 6 Ship 1 209 8 16 21 3 257 10 L 108 3 9 10 130 20 L 101 5 7 11 3 127 Ship 2 199 10 12 6 10 3 240 10 L 100 7 6 3 5 1 122 20 L 99 3 6 3 5 2 118 Total 816 36 56 54 26 6 994 A

B Ship 1 10 L 20 L Ship 2 10 L 20 L Total C Ship 1 10 L 20 L Ship 2 10 L 20 L Total

100 174 84 90 178 89 89 704

1 50480 20480 30000 53690 22705 30985 208340

Depth interval (m) 200 300 400 500 22 2 24 30 12 2 12 16 10 12 14 23 2 9 32 12 1 1 20 11 1 8 12 90 8 66 124 Soak time (x 24 hr) 2 3 4 2580 4540 4970 680 1880 2110 1900 2660 2860 2560 3610 1100 1520 1360 460 1040 2250 640 10280 16300 12140

5 860 860 2420 1110 1310 6560

Total

600 5 4 1 12 6 6 34

257 130 127 256 129 127 1026

6

930 210 720 1860

Total 63430 25150 38280 64310 27365 36945 255480

Observations on the Catch and Biology of Pacific Hagfish

D Ship 1 10 L 20 L Ship 2 10 L 20 L Total

100 43545 16610 26935 49996 21290 28706 187082

Depth interval (m) 200 300 400 500 4340 400 5700 8145 1890 400 2010 3430 2450 3690 4715 5440 400 3110 7855 2150 230 200 4430 3290 170 2910 3425 19560 1600 17620 32000

600 1300 810 490 3075 1035 2040 8750

109

Total 63430 25150 38280 69876 29335 40541 266612

Figure 19-6. Frequency distribution of catch (A), catch rates, kg/L (B) and kg/L/day (C).

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Figure 19-7. Spatial density of the catch in the exploratory hagfish fishery in the northwest of Mexico.

Discussion In Mexico, exploratory hagfish fishing represents an opportunity to develop a new activity that could provide sources of regional employment. However, the fishery is still in the stage of development and pertinent data on abundance and biology is being systematically collected by government agency to ensure that there is a sustainable fishery.

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The data analyzed in our study, as part of exploratory fishery, represents a virgin population as there was no previous exploitation of hagfish in the region. Also, there are no records of hagfish bycatch in other fisheries that represent a source of fishing mortality. Although we believe there is some size selection by the trap, only small individuals are not represented in the size structure (Fig. 19-2). During the early development of this exploratory fishery (2006–2008), the size structure reported for the hagfish ranged from 13–65 cm TL with an average of 39.3 cm TL (Flores– Olivares et al. 2009). The size range reported in the present study is 32–59 cm TL with an average of 43.3 cm TL. The parameters of the weight–length relationship reported by Flores– Olivares et al. (2009) for the hagfish in the same area were a= 0.033 and b= 2.3 which represents a negative allometric growth (b