New Frontiers in Crustacean Biology: Proceedings of the Tcs Summer Meeting, Tokyo, 20-24 September 2009

New Frontiers in Crustacean Biology: Proceedings of the TCS Summer Meeting, Tokyo, 20-24 September 2009

CRUSTACEANA MONOGRAPHS constitutes a series of books on carcinology in its widest sense. Contributions are handled by the Series Editor(s) and may be submitted through the office of KONINKLIJKE BRILL Academic Publishers N.V., P.O. Box 9000, NL-2300 PA Leiden, The Netherlands. Series Editor for the present volume: Charles H.J.M. F RANSEN, c/o Netherlands Centre for Biodiversity – Naturalis, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands; e-mail: [email protected] Founding Editor: J.C.

VON

VAUPEL K LEIN, Utrecht, The Netherlands.

Editorial Committee: N.L. B RUCE, Wellington, New Zealand; Mrs. M. C HARMANTIER -DAURES, Montpellier, France; Mrs. D. D EFAYE, Paris, France; H. D IRCKSEN, Stockholm, Sweden; J. F OREST, Paris, France; R.C. G UIA SU ¸ , Toronto, Ontario, Canada; R.G. H ARTNOLL , Port Erin, Isle of Man; E. M ACPHER SON , Blanes, Spain; P.K.L. N G , Singapore, Rep. of Singapore; H.-K. S CHMINKE, Oldenburg, Germany; F.R. S CHRAM, Langley, WA, U.S.A.; C.D. S CHUBART, Regensburg, Germany; G. VAN DER V ELDE, Nijmegen, Netherlands; H.P. WAGNER, Leiden, Netherlands; D.I. W ILLIAMSON, Port Erin, Isle of Man. Published in this series: CRM 001 - Stephan G. Bullard CRM 002 - Spyros Sfenthourakis et al. (eds.) CRM 003 - Tomislav Karanovic CRM 004 - Katsushi Sakai CRM 005 - Kim Larsen CRM 006 - Katsushi Sakai CRM 007 - Ivana Karanovic CRM 008 - Frank D. Ferrari & Hans-Uwe Dahms CRM 009 - Tomislav Karanovic CRM 010 - Carrie E. Schweitzer et al. CRM 011 - Peter Castro et al. (eds.) CRM 012 - Patricio De los Ríos CRM 013 - Katsushi Sakai

CRM 014 – Charles H.J.M. Fransen et al. (eds.) In preparation (provisional titles): CRM 016 - Danielle Defaye et al. (eds.) CRM 01x - Chang-tai Shih

Larvae of anomuran and brachyuran crabs of North Carolina The biology of terrestrial isopods, V Subterranean Copepoda from arid Western Australia Callianassoidea of the world (Decapoda, Thalassinidea) Deep-sea Tanaidacea from the Gulf of Mexico Upogebiidae of the world (Decapoda, Thalassinidea) Candoninae (Ostracoda) from the Pilbara region in Western Australia Post-embryonic development of the Copepoda Marine interstitial Poecilostomatoida and Cyclopoida (Copepoda) of Australia Systematic list of fossil decapod crustacean species Studies on Brachyura: a homage to Danièle Guinot Crustacean zooplankton communities in Chilean inland waters Axioidea of the world and a reconsideration of the Callianassoidea (Decapoda, Thalassinidea, Callianassida) Studies on Malacostraca: Lipke Bijdeley Holthuis Memorial Volume Studies on freshwater Copepoda: a volume in honour of Bernard Dussart Marine Calanoida of the China seas

Editor in chief’s address: Akira Asakura, Department of Biology, Graduate School of Science, Kobe University, Rokkodai 1-1, Nada-ku, Kobe, 657-8501 Japan; [email protected] Cover: Panulirus ornatus (Fabricius, 1798) by Chisato Sugiura (1962-2001) through the courtesy of Miki Masuda. http://sites.google.com/site/chisatosugiura/

New Frontiers in Crustacean Biology: Proceedings of the TCS Summer Meeting, Tokyo, 20-24 September 2009 By Akira Asakura, Kobe University, Japan (Editor in chief) Raymond T. Bauer, University of Louisiana at Lafayette, U.S.A. Anson H. Hines, Smithsonian Environmental Research Center, U.S.A. Martin Thiel, University Católica del Norte, Chile Keiji Wada, Nara Women’s University, Japan Toshiyuki Yamaguchi, Chiba University, Japan Christoph Held, Alfred Wegener Institute of Polar and Marine Research, Germany Christoph Schubart, University of Regensburg, Germany James M. Furse, Griffith University, Queensland, Australia Jason Coughran, Croaking Environment Resources, Australia Tadashi Kawai, Hokkaido Fisheries Experiment Station, Japan Susumu Ohtsuka, Hiroshima University, Japan Miguel V. Archdale, Kagoshima University, Japan Antonio Baeza, Smithsonian Marine Station at Fort Pierce, Florida, U.S.A. Mikio Moriyasu, Gulf Fisheries Centre, Canada (Editorial board) C RUSTACEANA M ONOGRAPHS , 15

LEIDEN • BOSTON

This book is printed on acid-free paper. Library of Congress Cataloging-in-Publication Data The Library of Congress Cataloging-in-Publication Data is available from the Publisher.

ISBN: 378-90-04-17425-2 © 2011 by Koninklijke Brill NV, Leiden, The Netherlands. Koninklijke Brill NV incorporates the imprints BRILL, Hotei Publishing, IDC Publishers, Martinus Nijhoff Publishers and VSP. All rights reserved. No part of this publication may be reproduced, translated, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior written permission from the publisher. Authorization to photocopy items for internal or personal use is granted by Koninklijke Brill NV provided that the appropriate fees are paid directly to The Copyright Clearance Center, 222 Rosewood Drive, Suite 910, Danvers, MA 01923, USA. Fees are subject to change. PRINTED IN THE NETHERLANDS

CONTENTS Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O HTSUKA , S USUMU , TAKEO H ORIGUCHI , Y UKIO H ANAMURA , YAMAGUCHI , M ICHITAKA S HIMOMURA , ATSUSHI T OSHINOBU S UZAKI , K IMIAKI I SHIGURO , H IDEO H ANAOKA , K AYOKO YAMADA & S HUJI O HTANI, Symbiosis of planktonic copepods and mysids with epibionts and parasites in the North Pacific: diversity and interactions . . . . . . . . . . . . . . .

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N AGASAWA , K AZUYA, The biology of Argulus spp. (Branchiura, Argulidae) in Japan: a review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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S HIMOMURA , M ICHITAKA & S USUMU O HTSUKA, Two new species of ectoparasitic isopods (Isopoda, Dajidae) from mysids in Japan. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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V ENMATHI M ARAN , B. A., S USUMU O HTSUKA , I KUO TAKAMI , S HINYA O KABE & G EOFFREY A. B OXSHALL, Recent advances in the biology of the parasitic copepod Pseudocaligus fugu (Siphonostomatoida, Caligidae), host specific to pufferfishes of the genus Takifugu (Actinopterygii, Tetraodontidae) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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VAZQUEZ A RCHDALE , M IGUEL , G UNZO K AWAMURA & K AZUHIKO A NRAKU, Bait improvement for swimming crab trap fisheries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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L ELAND , J. C., J. C OUGHRAN & D. J. B UCHER, A preliminary investigation into the potential value of gastric mills for ageing crustaceans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B UTLER IV, M ARK J., JAMIE S. H EISIG -M ITCHELL , A LISON B. M AC D IARMID & R. JAMES S WANSON, The effect of male size and spermatophore characteristics on reproduction in the Caribbean spiny lobster, Panulirus argus . . . . . . . . . . . . . . . . . . . .

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YAMASAKI , ATSUSHI, Fisheries management of the snow crab, Chionoecetes opilio, off Kyoto Prefecture in the western Sea of Japan, with emphasis on its resource recovery . . . . . . . . . . . . .

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M ORIYASU , M IKIO, Review of the current status of the snow crab Chionoecetes opilio (O. Fabricius, 1788) fisheries and biological knowledge in eastern Canada . . . . . . . . . . . . . . . . . . . . . B ISHOP, G., J. Z HENG , L. M. S LATER , K. S PALINGER & R. G USTAFSON, The current status of the fisheries for Chionoecetes spp. (Decapoda, Oregoniidae) in Alaskan waters Z HENG , J., L. M. S LATER , J. W EBB & G. B ISHOP , The current status of biological knowledge relating to the management of fisheries for Tanner (Chionoecetes bairdi (Rathbun, 1924)) and snow crabs (Chionoecetes opilio (Fabricius, 1788)) in Alaskan waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M ATSUBARA , H AJIME, Record of a male snow crab, Chionoecetes opilio with two extra fingers on the left chela . . . . . . . . . . . . . . . . BAUER , R AYMOND T., Amphidromy and migrations of freshwater shrimps. I. Costs, benefits, evolutionary origins, and an unusual case of amphidromy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . BAUER , R AYMOND T., Amphidromy and migrations of freshwater shrimps. II. Delivery of hatching larvae to the sea, return juvenile upstream migration, and human impacts . . . . . . . . . . . . . S NYDER , M ARCIA N., E LIZABETH P. A NDERSON & C ATHERINE M. P RINGLE, A migratory shrimp’s perspective on habitat fragmentation in the neotropics: extending our knowledge from Puerto Rico . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F UJITA , J UNTA , KOUJI NAKAYAMA , YOSHIAKI K AI , M ASAHIRO U ENO & YOH YAMASHITA, Comparison of genetic population structures between the landlocked shrimp, Neocaridina denticulata denticulata, and the amphidromous shrimp, Caridina leucosticta (Decapoda, Atyidae) as inferred from mitochondrial DNA sequences . . . . . . . . . . . . . . . . . . . . . . . . RÓLIER -L ARA , L UIS & I NGO S. W EHRTMANN, Diversity, abundance and distribution of river shrimps (Decapoda, Caridea) in the largest river basin of Costa Rica, Central America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G HERARDI , F RANCESCA & L AURA AQUILONI, Sexual selection in crayfish: a review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M ONTECLARO , H AROLD , K AZUHIKO A NRAKU & TATSURO M ATSUOKA, Morphology and electrophysiology of crayfish antennules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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M ATSUBARA , H AJIME , AYAKA C HIBA , YOSHIFUMI H ORIE , DAISUKE I WATA , M ASAHARU S HIMIZU , TAKAHIRO K INOSHITA & K AZUYOSHI NAKATA, Effect of pH and water temperature on the development of the Japanese crayfish, Cambaroides japonicus eggs in vitro . . . . . . . . . . . . . . . . . . . . . . . . F URSE , JAMES M. & JASON C OUGHRAN, An assessment of the distribution, biology, threatening processes and conservation status of the freshwater crayfish, genus Euastacus (Decapoda, Parastacidae), in continental Australia. I. Biological background and current status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F URSE , JAMES M. & JASON C OUGHRAN, An assessment of the distribution, biology, threatening processes and conservation status of the freshwater crayfish, genus Euastacus (Decapoda, Parastacidae), in continental Australia. II. Threats, conservation assessments and key findings. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F URSE , JAMES M. & JASON C OUGHRAN, An assessment of the distribution, biology, threatening processes and conservation status of the freshwater crayfish, genus Euastacus (Decapoda, Parastacidae), in continental Australia. III. Case studies and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . K AWAI , TADASHI & V JACHESLAV S. L ABAY, Supplemental information on the taxonomy, synonymy, and distribution of Cambaroides japonicus (Decapoda: Cambaridae) . . . . . . . . . . . . T HIEL , M ARTIN, The evolution of sociality: peracarid crustaceans as model organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . H OSONO , TAKASHI & H IROSHI M INAMI, Stable isotope analysis of epibiotic caprellids (Amphipoda) on loggerhead turtles provides evidence of turtle’s feeding history . . . . . . . . . . . . . . . . . . . . . . . . . T ORRES , G UADALUPE & J IM L OWRY, Peracarids from three low-energy fine-sand beaches of Mexico: western coast of Gulf of California . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . YAMADA , K ATSUMASA , M ASAKAZU H ORI , M ASAHIRO NAKAOKA & M ASAMI H AMAGUCHI, Temporal and spatial variations in functional-trait composition (functional diversity) of macrocrustacean communities in seagrass meadows . . . . . . . K URATA , K ENGO , M ASAHIRO H ORINOUCHI & DAVID L. D ETTMAN, Spatial differences in stable isotope signatures of crustaceans in brackish lake systems, western Japan . . . . . . . . . .

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PREFACE The Crustacean Society Summer Meeting jointly held with the 47th Annual Meeting of the Carcinological Society of Japan, was held 20-24 September 2009 at Shinagawa Campus, Tokyo University of Marine Science and Technology, Tokyo, Japan. This meeting was a truly landmark event in the history of both the CSJ and the TCS, as it was the first time that TCS held its annual meeting in the Asian region and was likened to a happy marriage of the two crustacean societies. Around 350 participants from 25 countries of all over the world came to Tokyo. About 260 papers were presented, including keynote addresses, symposium presentations, and symposium related and general contributed papers of both oral and poster presentations. The symposia held included: Life history migrations of freshwater shrimps – ecological and adaptive significance; Phylogeography and population genetics in decapod Crustacea; Speciation and biogeography in non-decapod crustaceans; Biology of Anomura III; Crustacean chemoreception – identification of cues and their applications; Integrative biology – crustaceans as model systems; Ecology and behavior of peracarids – progress and prospects; Reproductive behavior of decapod crustaceans; The new perspective on barnacle research; Symbiosis in crustaceans – diversity and evolutionary trends; Current status of fisheries and biological knowledge of snow and tanner crabs genus Chionoecetes in the world; Diversity and ecology of thalassinidean shrimps; Impacts of human exploitation on large decapod resources; Conservation biology of freshwater crayfishes – new challenges from Japan, Eastern Asia. On behalf of the organizing committee (Keiji Baba, Akira Asakura, Katsuyuki Hamasaki, Wataru Doi, Seiichi Watanabe, Keiji Wada, Kooichi Konishi), I am grateful to all participants, the sponsors (below) and supporting organizations (below), staffs and students for making this meeting a great success. My special gratitude must go to TCS Past and Current Presidents, Drs. Frederick R. Schram, Jens Høeg, Gary C. B. Poore, Trisha Spears, Jeffrey D. Shields, and Rafael Lemaitre, as well as the board of TCS for their help, efforts and encouragement to the council of Carcinological Society of Japan and myself to make this meeting possible.

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I am convinced that this volume of Crustacean Monographs Series, containing 29 contributions based on the presentations at the meeting, reflects the high standard of the meeting and will contribute to further advancement. The Tokyo Meeting was kindly sponsored by: Carcinological Society of Japan, Toshimitsu Odawara Memorial Fund for Crustacean Research, The Crustacean Society, Tokyo University of Marine Science and Technology, Inoue Foundation for Science, Tokyo University of Marine Science and Technology, Kiwi Breeze, Taiheiyo Synthetic Consultant Co., Ltd., Zukosha Co., Ltd., Seibutsu Kenkyusha Co., Ltd., and The Zoological Society of Japan. Furthermore, the Tokyo Meeting was kindly supported by: Society of Evolutionary Studies, Japan, The Genetic Society of Japan, The Plankton Society of Japan, The Japanese Society of Fisheries Science, The Sessile Organisms Society of Japan, Japanese Society for Aquaculture Research, The Biological Society of Okinawa, The Zoological Society of Japan, Ecology and Civil Engineering Society, Japanese Association of Benthology, The Biogeographical Society of Japan, Ecological Society of Japan, The Society of Population Ecology, Japanese Coral Reef Society, Japan Ethological Society, Japanese Society of Biological Scientists, The Japanese Society of Soil Zoology. A KIRA A SAKURA Editor-in-Chief, for the present volume New Frontiers in Crustacean Biology Secretary General, Organizing Committee, TCS Summer Meeting in Tokyo President, The Crustacean Society

SYMBIOSIS OF PLANKTONIC COPEPODS AND MYSIDS WITH EPIBIONTS AND PARASITES IN THE NORTH PACIFIC: DIVERSITY AND INTERACTIONS BY SUSUMU OHTSUKA1,8 ), TAKEO HORIGUCHI2 ), YUKIO HANAMURA3 ), ATSUSHI YAMAGUCHI4 ), MICHITAKA SHIMOMURA5 ), TOSHINOBU SUZAKI6 ), KIMIAKI ISHIGURO2 ), HIDEO HANAOKA1 ), KAYOKO YAMADA1 ) and SHUJI OHTANI7 ) 1 ) Takehara Marine Science Station, Setouchi Field Center, Graduate School of Biosphere Science, Hiroshima University, 5-8-1 Minato-machi, Takehara, Hiroshima 725-0024, Japan 2 ) Department of Natural History Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan 3 ) National Research Institute of Fisheries Science, 2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa, 236-8648, Japan 4 ) Laboratory of Marine Biology, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minatomachi, Hakodate, Hokkaido 041-8611, Japan 5 ) The Kitakyushu Museum of Natural History and Human History, 2-4-1 Higashida, Yahatahigashi-ku, Kita-Kyushu, Fukuoka 805-0071, Japan 6 ) Department of Biology, Faculty of Science, Kobe University, 1-1 Rokkodai-cho, Nada-ku, Kobe 657-8501, Japan 7 ) Faculty of Education, Shimane University, 1060 Nishikawatsu-cho, Matsue, Shimane 690-8504, Japan

ABSTRACT Planktonic crustaceans such as copepods and mysids are two of the most abundant components of the marine zooplankton community and, although they harbor a diversity of symbionts, their real interactions have been poorly understood. We have been investigating planktonic symbiosis and briefly review the biology of symbionts on planktonic crustaceans based mainly on our research conducted in the North Pacific. Symbiotic histophagous apostome ciliates probably have a significant negative impact on their coastal copepod hosts in view of their high prevalence and their worldwide distributions in the coastal ecosystems. Such symbionts are also likely to impact the populations of the copepod’s predators such as chaetognaths. In contrast, symbiosis between copepods and epibionts such as diatoms and suctorian ciliates may be more or less harmless to the host.

8 ) Corresponding author; e-mail: [email protected]

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Various endoparasitic alveolates have been discovered infecting from copepods, some of which could have evolved as parasitoids. Epibiont peritrichians found on the body of gastrosaccid mysids are generally regarded as a commensal, and showed a remarkably high host-specificity to intertidal species as well as a distinct geographic cline with a preference for boreal waters. The sand-burrowing behavior of the mysids, coupled with the diversity and abundance of their preys possibly contributes substantially to the establishment of the symbiotic association with epibionts. A dajid isopod and a nicothoid copepod compete for the space and possibly, food within the marsupium of the mysid host Siriella okadai. The annual egg production of the host S. okadai seems to be significantly suppressed by these two parasites. Prior to the appearance of mature adults of each of these parasites within the host marsupium, immature individuals occupy particular microhabitats within the host dependent upon the state of maturity of the host. It is important to pay more attention to parasitoid protists on zooplankters in order to better understand the aquatic ecosystem.

INTRODUCTION The study of marine plankton has paid more attention to prey-predator relationships than to symbiosis, in part because the impact of the latter had been improperly underestimated so that symbiosis was considered to play only a minor role in the ecological interactions structuring pelagic communities (Ohtsuka et al., 2007). Recent investigations have, however, clearly revealed that symbionts have more complex and significant impacts on the population dynamics of their host zooplankters. For example, alveolate parasitoids sometimes lead to mass mortalities of host zooplankters including tintinnids, copepods, and euphausiids (Cachon & Cachon, 1987; Coats & Heisler, 1989; Kimmerer & McKinnon, 1990; Capriulo et al., 1991; GómezGutiérrez et al., 2003, 2006, 2009; Ohtsuka et al., 2004, 2007; Skovgaard & Saiz, 2006). Their interactions broadly range from phoresy, to mutualism through to commensalism and parasitism to parasitoidism (Bush et al., 2001; Rhode, 2005). The present paper briefly reviews the symbiotic relationship of copepods and mysids with a variety of microscopic symbionts based mainly on our recent investigations carried out in Japanese waters. Symbiosis is generally defined as an association between two different organisms living together, and usually with a gradient of beneficial or deleterious consequences for at least one of them (Bush et al., 2001). However, we redefine this term considering the interspecific relationships in which usually large-sized “hosts” are infested or infected by symbionts.

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COPEPOD HOSTS Apostome ciliates Apostomes are symbiotic ciliates that mainly infest planktonic and benthic crustaceans at least during one phase of their complex life cycles, which typically include four functionally different morphs: resting phoront, feeding trophont, divisional tomont, and infective tomite stages (Chatton & Lwoff, 1935). Vampyrophrya pelagica Chatton & Lwoff, 1930 is well investigated in terms of its morphology, cytology and ecology, and most likely plays a pivotal role in the brackish to coastal pelagic ecosystems in the world oceans due to its high prevalence and harmful impact both directly on planktonic copepods and indirectly on their invertebrate predators such as chaetognaths (Chatton & Lwoff, 1935; Grimes & Bradbury, 1992; Ohtsuka et al., 2004). Zooplanktonic invertebrate predators that prey upon parasitized copepods obtain fewer nutrients from their preys, because infected copepods are at least partly consumed by the histophagous apostome. The ciliates can increase mortality in the copepod population, if the copepod is injured by any other means, thus reducing the prey availability in the pelagic ecosystem. Thus, the trophic behavior of the histophagous apostome ciliates could have two adverse affects on higher trophic levels in the zooplankton food web: increasing copepod mortality and depleting the resources available to carnivorous zooplanktonic predators. The life cycle of V. pelagica is briefly summarized below based on Ohtsuka et al. (2004), and on our unpublished data from studies carried out in the Seto Inland Sea, Japan. An oval, encysted phoront, within which one cell is enclosed, is typically attached to the ventral side of the prosome and/or to the prosomal appendages of copepods (fig. 1A, B). Host-specificity was expressed: calanoid and “poecilostomatoid” copepods (see Boxshall & Halsey, 2004), were preferred hosts in comparison of other copepod taxonomic groups, irrespective of body sizes and/or behavior, while some species of the cyclopoid Oithona were not selected. The infective tomite of Vampyrophrya was observed swimming rapidly around the body of Oithona, but finally moving away without successful settlement, from which we inferred some kind of physio-chemical interaction between the tomite and host body surface. High incidence of this apostome was observed between August and January, especially in later summer and fall, when prevalence was nearly 100% in the numerically dominant calanoid Paracalanus parvus (Claus, 1863) s.l. Its intensity could exceed 40 cells per host. This stage was characterized by a

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Fig. 1. Life cycle of the apostome ciliate Vampyrophrya pelagica infecting planktonic copepods. A, B, phoronts; C, D, trophonts (cytostome indicated by white arrow in D); E, tomonts; F, tomite (arrowed) releasing from tomont cyst. The phoront excyst having a metamorphosis to trophont stage in about 1 hr after the copepods were crashed by needles (trigger stimulus). Approximate stage durations of trophonts and tomonts at 10 and 25◦ C are indicated in D and E panels, respectively. Scales are in μm. (After Ohtsuka et al., 2004 with permission from InterResearch.)

specialized intracellular structure, numerous lamellae of ca. 0.04 μm thick, which was identified as a precursor of the food vacuole membrane of the trophont. A trophont (fig. 1C, D) excysts from a phoront when the parasitized copepods are: (1) fed upon by invertebrate predators such as chaetognaths or medusae, that break the copepod body allowing the ciliates to excyst, (2) physically damaged, and presumably, (3) unsuccessful in molting (Grimes & Bradbury, 1992; Ohtsuka et al., 2004). In any case, body fluids leaking from the copepod or physically damaged copepods trigger the ciliate metamorphosis. Feeding of fish larvae of fish such as Plecoglossus altivelis altivelis (Temminck & Schlegel, 1846) on parasitized copepods didn’t result in hatching of phoronts in the laboratory. Trophonts enter via fissures in the copepod exoskeleton, and commence to consume copepod tissues by a large cytostome (fig. 1D). The

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cell volume eventually increases to about 30 times that of the initial trophont cell. This increase in trophont size is enabled by the intracellular precursor material of the phoront. Fully-grown trophonts metamorphose into encysted tomonts inside the empty body of the consumed copepod (fig. 1E). Up to 20 tomites cells are released from a tomont. These infective cells search for a new copepod host (fig. 1F) and then metamorphose into phoronts again. In the cold-water season they almost completely disappeare from the hosts except in large-sized species such as Calanus sinicus Brodsky, 1965 (∼3 mm long) with sufficient long longevity to harbor phoronts, which seem to attach just before the phase of intensive production of tomites finished. This phenomenon can be explained by the relationship between seasonal fluctuation in water temperature and duration of development of apostome life stages. In the laboratory low temperature clearly causes delay in developmental duration of each stage, in particular, of the tomont stages. Completion of the divisional stage took about 330 h for 50% cells at 10◦ C, about 20 times longer than at 25◦ C. Production of the infesting tomites appears to be suppressed by low temperature. Suctorian and peritrich ciliates Symbiotic relationships between suctorian ciliates and pelagic copepods have been intensively investigated in the subarctic waters of the North Pacific (Yamaguchi, 2006, unpubl.). The attachment of four epibiont suctorian genera, Paracineta, Pelagacineta, Tokophrya and Trophogemma on copepods was observed exclusively on the urosome of 10 relatively large-sized, mesopelagic species of six calanoid copepod genera. Tokophrya and Trophogemma exhibited high host-specificity on Paraeuchaeta birostrata Brodsky, 1950 and P. elongata (Esterly, 1913), respectively. The attachment of suctorians to copepods seems to be species- and stage-specific. Carnivorous hosts and adult females had higher infestation rates, suggesting higher host-specificity on hosts of larger size, greater longevity, and/or higher escape ability from predators. This means that suctorians are less impacted by being eaten by predators of the copepod hosts. Paracineta (fig. 2F, G) and Pelagacineta suctorian ciliates exclusively infest adult females of the particle-feeding calanoid Metridia pacifica Brodsky, 1950. Prevalence was relatively higher in the Bering Sea and at higher latitudes in the North Pacific in summer and fall with an average of 9.4% (range 0-70%) (table I). A geographical gradient was also observed, with higher attachment in cold waters (20◦ C), whereas the parasitic copepod was present from the mid winter to summer (120 mm CL) were mated with large females (>95 mm CL) and small males (1.946 MM 1.946 MM

0.20.4 MM

Tier 1

Tier 1

30% LM

Tier 2 Maximum

Exploitation rate

10% MMM 20% (100% of MMM new shell male crab 0.13 MM and 15% of old or very 0.13 MM 0.09 MM old shell male crab 0.09 MM 4.003 MM >114 mm CW) 4.003 MM 1.000 LM

>2.938 MM

>1.528 MM

>2.472 MM

0.002495 t MM

15% LM 15% LM

25% LM 25% LM

Tier 2 Tier 1 Tier 2 Maximum >2.246 MM Each section, 45; At least 2 sections must open; >3.104 MM District must total >1.466 MM 181

0.7-1.4 LM >1.400 LM

150 000 km2 ). Threats include: land use practices, pollution, recreational fishing, exotic species, and the known and anticipated effects of climate change. On these bases Euastacus separates into six conservation groups, with 80% (39 species) evaluated as belonging in IUCN threat categories, the majority of these Endangered or Critically Endangered: a bleak assessment.

INTRODUCTION It has long been recognised that Euastacus are of considerable conservation concern (e.g., Horwitz, 1990a, 1995; Merrick, 1997). The last assessment of the genus versus IUCN Red List criteria (in 1996) placed 16 species in threat 1 ) Corresponding author; e-mail: [email protected] 2 ) e-mail: [email protected]

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categories (IUCN, 2009). At the time of writing the conservation status of the other 33 known species is unclear, and a reassessment of the status of the genus is warranted (see Furse & Coughran, 2011a: 241-252, this volume). The aim of this project was to conduct the first systematic assessment of the conservation status of all species in genus Euastacus against Internationally recognised criteria (the IUCN Red List).

METHOD For each of the 49 species the literature was reviewed to identify and evaluate known and potential threats, and determine geographic locations and extent of species’ distributions. Extent of species’ distributions were calculated using topographical maps, remote imaging, and a Geographical Information System to give the Extent Of Occurrence (EOO) in km2 for each species. By IUCN definition the EOO is “the area contained within the shortest continuous imaginary boundary which can be drawn to encompass all the known, inferred or projected sites of present occurrence of a taxon, excluding cases of vagrancy” (IUCN, 2006). It was not possible to calculate Area Of Occupancy (AOO) or the “area of suitable habitat occupied by the taxon” (IUCN, 2006), as such data is not available for any Euastacus. Each species was then assessed versus current IUCN criteria (Version 6.1, 2006), and placed into one of six categories: Data Deficient (DD), Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), or Critically Endangered (CR). Definitions of these categories are provided in the IUCN Guidelines current at the time of our review (IUCN, 2006: 7).

RESULTS & DISCUSSION Identified threats Habitat destruction, fragmentation and modification threaten many species of Euastacus (Horwitz, 1990a, 1995; Merrick, 1995). Agriculture, forestry and urbanisation all involve clearing of native vegetation, which for most species appears to be an essential habitat component. Morgan (1986, 1988, 1997) documented examples of many species that were absent from sites that had been cleared of native vegetation, and Furse & Wild (2002) quantified a

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relationship between density of Euastacus sulcatus Riek, 1951 and vegetative canopy cover over streams. Construction of weirs and reservoirs also impacts on stream flow, temperature and oxygen levels, and thereby impacts on riverine Euastacus that require flowing, cool, well oxygenated conditions (Horwitz, 1990a). There appears to be at least one case of localised extinction due to this: Euastacus bispinosus Clark, 1936 disappeared when Rocklands Reservoir was built in Victoria (Horwitz, 1990a). Water quality and pollution has long been identified as a threat for the genus generally (Horwitz, 1990a, 1995; McKinnon, 1995; Merrick, 1995), and these threats include sedimentation, increased temperature, decreased oxygen levels, eutrophication and pesticide runoff. Given their extremely restricted ranges, many species are susceptible to small-scale, localised impacts and disturbance events (“local disasters”, Merrick, 1995) such as forest management and agricultural practices, water harvesting, bushfires, and “accidents” such as chemical, pesticide or petroleum spills. Climate change poses both direct and indirect threats to almost all species in the genus. Regional modelling of climate change impacts invariably predict increasing temperatures across the distribution of the genus (Howden, 2003; Hughes, 2003; Pittock, 2003; Westoby & Burgman, 2006), and this direct threat is of particular concern for many of the species that appear to require cool conditions. It is established that most Euastacus are already restricted to the extreme upper reaches of the catchments they inhabit (including isolated mountain tops), and evidence from Queensland suggests this is due to a retreat to cooler areas of habitat in response to the warming of the continent during the Pliocene (Ponniah & Hughes, 2004, 2006). If these species are indeed restricted by their thermal tolerance, then any further increase in temperature through climate change poses a significant threat, and could cause extinctions across this genus. Modelling in most areas where Euastacus occur also predicts altered hydrological regimes, including decreased rainfall, runoff and reduced soil moisture (Chiew & McMahon, 2002; Hughes, 2003). This is clearly a threat for riverine species that require flowing conditions, but is perhaps a greater concern for those species that occur in ephemeral habitats (see Coughran, 2007, 2008) and rely on sub-surface water and moist forest soils. It is also predicted that these climate change impacts will lead to other habitat changes, such as shifts in forest type from rainforest to sclerophyllous forest (Hilbert et al., 2001; Hughes, 2003). Since many Euastacus appear to be dependent on rainforest habitats or other specific vegetation types and habitats (e.g., high altitude heathland and Alpine bogs), any climate change induced

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alterations in vegetation communities and their distributions are clearly of concern (Hughes, 2003; Westoby & Burgman, 2006). Climate change is also expected to result in an increased frequency of severe weather events (severe droughts, storms, floods, and tropical cyclones) (Hughes, 2003; IPCC, 2007; Specht, 2008), and these may impact on the quality of habitat and/or more directly on the crayfish themselves (McCormack et al., 2010). For example, a recent localised severe storm event resulted in a mass kill of Euastacus valentulus Riek, 1951 — several hundred crayfish had apparently been directly overwhelmed by the large volume of storm induced flow and had been buried in the alluvium, up to 50 m away from the stream channel (Furse, unpubl.). Mass crayfish kills and emersion events have recently been documented elsewhere in response to severe weather events, particularly floods (Parkyn & Collier, 2004; Lewis & Morris, 2008), therefore any climate change induced increase in severe flooding events is clearly a serious threat to endangered crayfish (Meyer et al., 2007). Climate change will likely also lead to a range of other disturbance events that could contribute to declines in Euastacus or their habitat, such as increased incidence of widespread bushfires, which may in turn lead to “black water events”, and mass emersions and mortalities as have been documented in Euastacus armatus (von Martens, 1866) in such conditions (McKinnon, 1995). Over-exploitation is recognised as a threat for several species, and this extends to large species that are targeted by recreational fishing and smaller species that are targeted by ‘collectors’ (Coughran, 2007). It is also apparent that Euastacus are illegally traded for aquarium use, both domestically and internationally. Because of their striking colouration, size and armature, these crayfishes are highly prized as aquarium specimens, and illegal exploitation to supply this demand may present a considerable threat, particularly for the exceptionally rare species. All available information on the biology of this genus has revealed that they are extremely slow-growing with life history characteristics that are unsuited to even moderate levels of exploitation (e.g., Hoey, 1990; Honan & Mitchell, 1995a, 1995b; Turvey & Merrick, 1997; Furse & Wild, 2004; Wild & Furse, 2004; Coughran, 2006). Illegal poaching from protected areas has been reported for many species, and breaches of fishing regulations for recreational catch species also appears to be common (see Coughran, 2007; Coughran & Furse, 2010). Exotic species are prevalent throughout the range of many Euastacus, and several of these have been known to impact either on crayfish directly, or on crayfish habitat (Green & Osbourne, 1981; Horwitz, 1990a, 1995; Merrick, 1995; O’Brien, 2007; Rowe et al., 2008).

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These animals include cats (Felis catus), foxes (Vulpes vulpes), pigs (Sus scrofa), goats (Capra hircus), trouts (Salmo trutta, and Oncorhynchus mykiss), European carp (Cyprinus carpio), redfin perch (Perca fluviatilis), and toxic cane toads (Bufo marinus). Although there are no foreign crayfish in Australia, a few native species have been widely translocated outside of their natural range (Horwitz, 1990b) and two species are now becoming established on the eastern seaboard of Australia, Cherax destructor Clark, 1936 and Cherax quadricarinatus (von-Martens, 1868) (Coughran & Leckie, 2007; Coughran et al., 2009). Both of these species display a far superior reproductive biology to Euastacus, and thus have the potential to rapidly out-compete them. Many of the above threats compound by the fact that a number of species are distributed in close proximity to, or in some cases, partially within rapidly growing major population centres (ABS, 2009; Furse & Wild, unpubl.). While there are not currently any alien crayfish species in Australia, any illegal importation or introductions of alien crayfish would pose a very serious threat to the native Australian crayfish fauna. Continued vigilance by authorities at Australian borders will be essential to minimise the risk of alien crayfish being introduced onto the Continent. Geographic range The EOO of individual species ranges from 2.5 to >150 000 km2 . However, it is of note that apart from a few widespread species, most Euastacus have highly restricted ranges. Only 12 species have an EOO >5000 km2 . The remainder have restricted EOOs of 150 000