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INTRODUCTION: FRESHWATER FISHES AND THEIR CONSERVATION

Int. Zoo Yb. (2013) 47: 1–5 DOI:10.1111/izy.12021

Introduction to Freshwater Fishes and Their Conservation GORDON MCGREGOR REID Chair, IUCN-SSC/Wetlands International Freshwater Fish Specialist Group; Professor of Conservation Science, Veterinary School, University of Liverpool; Director Emeritus, North of England Zoological Society (Chester Zoo), Zoological Gardens, Upton by Chester, Cheshire CH2 1LH, United Kingdom E-mail: [email protected]

Freshwater fishes are the most threatened large taxon in the world [Carrizo et al., 2013; see also Freshwater Fish Specialist Group (FFSG): http://www.iucnffsg.org]. While fresh waters are globally scarce (15 000 species, representing c. 53% of all fishes and 25% of all vertebrates. Fresh water is essential for all life (humans, domestic livestock, wild animals, plants and microorganisms) and freshwater fishes are a direct indicator of the health of our planet. Most of the threats to their survival are human induced (Reid et al., 2013). Hence, in the long term, our own future will be jeopardized, unless we recognize the high intrinsic and commercial value of fishes and the supporting ecosystem, and take necessary care (Baillie et al., 2010; Barnosky et al., 2012). It is essential, therefore, to improve on environmental monitoring and, where appropriate, develop efficient and effective conservation actions. Zoos and aquariums are often well placed to engage in these activities in partnership with others. The theme for this volume of the International Zoo Yearbook (IZY) picks up on this aspect and reflects aspirations of the Global Aquarium Strategy for Conservation and Sustainability of the World Association of Zoos and Aquariums (WAZA) (Penning et al., 2009). The volume is also inspired by scientific output from the ‘4th International Zoo and Aquarium Symposium: Global

Freshwater Fish Conservation – Linking In Situ and Ex Situ Conservation Actions’. The Symposium was hosted in Chester in 2010 by the North of England Zoological Society (Chester Zoo), the Zoological Society of London (ZSL London Zoo) and the FFSG of the International Union for Conservation of Nature (IUCN) Species Survival Commission (SSC) and Wetlands International (http://www.chesterzoo.org/; http://www.zsl. org/zsl-london-zoo/; http://www.iucnffsg. org/). Delegates represented fish and freshwater interests worldwide in public aquariums, the aquarium hobbyist and fisheries industries, and national and local government agencies. There were also researchers in freshwater ichthyology from universities, museums, scientific institutions and nongovernmental conservation organizations. For the first time, representatives of these diverse groups met to share knowledge and explore exciting new collaborative opportunities in conserving freshwater fishes and their habitats. Several of the delegates kindly prepared updates of their original unpublished presentations for publication here and other topical articles were specially commissioned. In this volume of IZY, global challenges in freshwater-fish conservation related to public aquariums and the aquarium industry are broadly outlined by Reid et al. (2013). These authors provide recent calculations on the extraordinary freshwater-fish biodiversity,

Int. Zoo Yb. (2013) 47: 1–5 © 2013 The Author. International Zoo Yearbook © 2013 The Zoological Society of London

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and highlight the great scarcity and vulnerability of freshwater habitats on the earth’s surface that are ‘available’ to fishes. They stress that fishes and their habitats are increasingly susceptible to the many and growing human-induced threats. With the global human population now above 7 billion (Baillie et al., 2010), there are overwhelming pressures on fresh waters to provide supplies for human use, and wild and farmed fishes as food and (to a far lesser extent) for aquariums (Wetlands International, 2010). This leads to overfishing and a deterioration of the natural aquatic environment through, for example, damming, drought, pollution and the introduction of alien species. Climate change is another all-pervasive strategic threat for fresh waters. The grave long-term implications of this are discussed in depth by Pearce-Kelly et al. (2013). Crucially, the foregoing threat factors (separately or in combination) can result in declining populations of fishes and even extinction of species. Reid et al. (2013) summarize the conservation challenges and opportunities in three sections: review and evaluation, monitoring and research, and practical implementation. The other papers in this volume provide scientific detail on key aspects of these themes. Recent progress towards an IUCN global assessment of the conservation status of freshwater fishes, and the great relevance of this to zoo and aquarium missions, is covered by Carrizo et al. (2013). Accurate knowledge of species threatened in the wild (and of the most vulnerable regions, habitats and ichthyofaunal hotspots) is needed to identify targets for action and to set conservation priorities (IUCN, 2011, 2012). Knowing which fishes are officially listed as Extinct in the Wild but that still survive ex situ in aquarium populations is clearly vital. There is a strong tradition in the zoo and aquarium community of supporting IUCN initiatives in the conservation of freshwater fishes. The FFSG is a voluntary organization hosted and funded by Chester Zoo. Similarly, the FFSG Anguillid (Eel) Specialist Subgroup and FFSG South Asia branch (both established at the 2010 Symposium in Chester) are hosted and

funded, respectively, by ZSL and the Zoo Outreach Organization. The FFSG works with the aquarium community and wider conservation community. As a Red List Authority for threatened species of freshwater fishes, operating in 18 geographical regions, the FFSG also works closely with the executive staff of the IUCN Freshwater Biodiversity Unit, Cambridge, UK (http:// www.iucn.org/about/work/programmes/ species/our_work/about_freshwater/). The Neotropical region represents by far the largest geographical hotspot, containing as many as 8000 species (53%) of all freshwater fishes. Reis (2013) notes that many small, distinctive or brightly coloured Neotropical species are kept by hobbyists and displayed in public aquariums. Hence, these should naturally be a focus for conservation action, where required. Unfortunately, there have been comparatively few regional conservation assessments or worthwhile initiatives to date, in situ or ex situ (but see Chao et al., 2001; Baigún et al., 2012; Tlusty et al., 2013). Reis (2013) and colleagues are certainly taking action to remedy this situation. The Western Ghats is another remarkable example of a hotspot for freshwater-fish biodiversity (Kumar & Devi, 2013). The rivers here drain more than one-third of India, and contain c. 189 endemic species and c. 40% of the total number (>544) of native species of freshwater fishes (http://www.nbfgr. res.in/pdf/ThreatenedFreshwaterFishes.pdf). Kumar & Devi (2013) encourage aquariums to support conservation of the fishes in the Western Ghats in various ways, including through the sustainable acquisition of ‘greencertificated’ wild fishes via the aquarium trade (see also Silas et al., 2011), through research and the cryopreservation and genebanking of gametes (see also Reid et al., 2008; Clarke, 2009; Rawson et al., 2011), and through promoting ecotourism and education via public aquariums (see also Tlusty et al., 2013). Koldewey et al. (2013) cogently argue that a prime conservation goal of aquariums is in awareness raising and in working to establish environmentally sustainable


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behaviours in society (see also Koldewey et al., 2009). In effect, the fishes on display are ‘ambassadors’ for their species. Koldewey et al. (2013) acknowledge other important conservation roles for aquariums both ex situ and in situ. For aquarium programmes, they propose that marine fishes of Least Concern should not take a biased priority over the large number of threatened freshwater species worldwide which urgently need help. Ex situ conservation-breeding programmes for such species are clearly an important role and this may fruitfully involve curators, professional aquarists, scientists, aquarium hobbyists and other partners (Dibble, 2010). However, all of this presumes prudent collection planning, species prioritization, and the development of excellent husbandry, veterinary and other management techniques. Koldewey et al. (2013) carefully place such necessary managerial developments in the context of WAZA’s Global Aquarium Strategy for Conservation and Sustainability (Penning et al., 2009). They also discuss collaborative efforts via the European Endangered Species Programme to breed threatened species organized between the European Fish and Aquatic Invertebrate Taxon Advisory Group, the European Association of Zoos and Aquaria, and the European Union of Aquarium Curators (http://www.eaza.net/activities/cp/Pages/ Collection%20Planning.aspx; http://www. euac.org/). Mycobacteriosis is among the more serious veterinary issues causing problems in the care and breeding of threatened fishes, including those that are Extinct in the Wild (Routh, 2013). This is a zoonotic, widespread, chronic and, in fishes, sometimes fatal disease. It is associated with three or more species of Mycobacterium (Decostere et al., 2004) and has diverse symptoms, including persistent non-healing ulcers and spinal deformities. Routh (2013) elaborates on the considerable challenges in successfully diagnosing, treating and managing this condition, in maintaining biosecurity and in ensuring that aquariumbred populations destined for reintroduction are free of the disease.

Of course natural, fecund reproduction in populations held in aquariums and the maintenance of genetic diversity is sometimes difficult to achieve, especially in the long term (Reid & Hall, 2003; Price, 2010). In such cases, assisted reproduction using commercial aquacultural techniques can be a way forward. O’Brien & Cooper (2013) demonstrate the great benefit of this approach for the conservation breeding of threatened species native to New Zealand, including Shortfin eel Anguilla australis and Giant kokopu Galaxias argenteus. The American Association of Zoos and Aquariums (AZA: http://www.aza.org) has a Freshwater Fish Taxon Advisory Group. This has operated a Lake Victoria Cichlids Species Survival Plan (LVSSP, East Africa) since 1994, initially in collaboration with the IUCN-SSC Conservation Breeding Specialist Group. The AZA LVSSP was established to help conserve the endemic ‘flock’ of 500 or more indigenous haplochromine cichlid species threatened in Lake Victoria-Kyoga (Hemdal, 2012; Hemdal & McMullin, 2013; see also Reid, 1990, for a similar earlier programme in Europe). Working harmoniously between the Lake and public aquariums, the LVSSP serves as an excellent example of a necessary international integration of in situ and ex situ activities. The Pitch-black fulu Haplochromis piceatus is one prioritized species that has been rescued from the Lake, and which has been successfully managed and bred in public aquariums for some 20 years. Hemdal & McMullin (2013) provide a management review for this ‘model’ species and note, encouragingly, that inbreeding depression in populations has been avoided and that a natural genetic diversity has, in large measure, been maintained. Another fine example of an integrated approach is given by Maitland & Lyle (2013) of the Fish Conservation Centre (http://www. taysidebiodiversity.co.uk). The species involved are cold-water salmoniform fishes native to Scotland: Arctic charr Salvelinus alpinus, Powan Coregonus lavaretus and Vendace Coregonus albula. These authors have conducted in situ and ex situ research


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that is relevant to the survival of these taxa, have employed assisted reproduction techniques and have successfully translocated progeny of all three species to new refuge sites. Returning fishes to the wild in restored habitats may, where appropriate, be one of the ultimate strategic objectives of ex situ programmes. Such activities should, of course, strictly follow accepted guidelines (IUCN, 1998). The reintroduction and restoration successes of the Tennessee Aquarium Conservation Institute (http://www.tnaci. org/) provide substantial evidence to encourage this approach (George et al., 2013). This Institute has, in partnership with others, managed to return Lake sturgeon Acipenser fulvescens and Barrens topminnow Fundulus julisia to their native habitats in the United States. They have also skilfully used aquarium marketing and education programmes actively to engage the visiting public and materially support these worthwhile outreach endeavours. In conclusion, I must express my sincere thanks to all of the distinguished authors in the Freshwater Fishes and Their Conservation section for their outstanding practical work in this area, and for their thoughtful, provocative and inspiring scientific contributions to this volume. REFERENCES BAIGÚN, C. R. M., COLAUTTI, D., LÓPEZ, H. L., VAN DAMME, P. A. & REIS, R. E. (2012): Application of extinction risk and conservation criteria for assessing fish species in the lower La Plata River basin, South America. Aquatic Conservation: Marine and Freshwater Ecosystems 22: 181–197. BAILLIE, J. E. M., GRIFFITHS, J., TURVEY, S. T., LOH, J. & COLLEN, B. (Eds) (2010): Evolution lost: status and trends of the world’s vertebrates. London: Zoological Society of London. BARNOSKY, A. D., HADLY, E. A., BASCOMPTE, J., BERLOW, E. L., BROWN, J. H., FORTELIUS, M., GETZ, W. M., HARTE, J., HASTINGS, A., MARQUET, P. A., MARTINEZ, N. D., MOOERS, A., ROOPANARINE, P., VERMEIJ, G., WILLIAMS, J. W., GILLESPIE, R., KITZES, J., MARSHALL, C., MATZKE, N., MINDELL, D. P., RIVELLA, E. & SMITH, A. B. (2012): Approaching a state shift in Earth’s biosphere. Nature 486: 52–58. Available at http://www.nature.com/nature/ journal/v486/n7401/abs/nature11018.html CARRIZO, S. F., SMITH, K. G. & DARWALL, W. R. T. (2013): Progress towards a global assessment of the status of

freshwater fishes (Pisces) for the IUCN Red List: application to conservation programmes in zoos and aquariums. International Zoo Yearbook 47: 46–64. CHAO, N. L., PETRY, P., PRANG, G., SONNESCHIEN, L. & TLUSTY, M. (Eds) (2001): Conservation and management of ornamental fish resources of the Rio Negro basin, Amazonia, Brazil – Project Piaba. Manaus: Editora da Universidade do Amazonas. CLARKE, A. G. (2009): The Frozen Ark Project: the role of zoos and aquariums in preserving the genetic material of threatened animals. International Zoo Yearbook 43: 222–230. DECOSTERE, A., HERMANS, K. & HAESEBROUCK, F. (2004): Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Veterinary Microbiology 99: 159–166. DIBBLE, I. (2010): Aquarists and scientists working together to save species from extinction. In Viviparous fishes II: 415–416. Uribe, M. C. & Grier, H. J. (Eds). Mexico: New Life Publications/New Life Exotic Fish Inc. GEORGE, A. L., HAMILTON, M. T. & ALFORD, K. F. (2013): We all live downstream: engaging partners and visitors in freshwater fish reintroduction programmes. International Zoo Yearbook 47: 140–150. HEMDAL, J. (2012): Lake Victoria cichlid SSPs. 2012 North American regional studbook and husbandry manual. Toledo, OH: Toledo Zoo. HEMDAL, J. & MCMULLIN, E. (2013): Husbandry of a Lake Victoria cichlid, the Pitch-black fulu Haplochromis piceatus, in public aquariums: a 20 year retrospective. International Zoo Yearbook 47: 112–119. IUCN (1998): IUCN guidelines for re-introductions. Gland, Switzerland, and Cambridge, UK: IUCN. Available at http://www.iucnsscrsg.org/policy_guidelines.php IUCN (2011): Guidelines for using the IUCN Red List categories and criteria: version 9.0 (September 2011). Gland, Switzerland, and Cambridge, UK: IUCN. Available at http://www.iucnredlist.org/documents/ RedListGuidelines.pdf IUCN (2012): The IUCN Red List of threatened species. Gland, Switzerland, and Cambridge, UK: IUCN. Available at http://www.iucnredlist.org/ KOLDEWEY, H., ATKINSON, J. & DEBNEY, A. (2009): Threatened species on the menu? Towards sustainable seafood use in zoos and aquariums. International Zoo Yearbook 43: 71–81. KOLDEWEY, H., CLIFFE, A. & ZIMMERMAN, B. (2013): Breeding programme priorities and management techniques for native and exotic freshwater fishes in Europe. International Zoo Yearbook 47: 93–101. KUMAR, R. & DEVI, K. R. (2013): Conservation of the freshwater habitats and fishes in the Western Ghats of India. International Zoo Yearbook 47: 71–80. MAITLAND, P. S. & LYLE, A. A. (2013): Ex situ and in situ approaches, including assisted reproduction, for the conservation of native species of charr (Salmonidae) and whitefish (Coregonidae) in Scotland. International Zoo Yearbook 47: 129–139. O’BRIEN, Q. & COOPER, D. (2013): Conservation breeding of shortfin eels Anguilla australis and giant kokopu


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Galaxias argenteus at Mahurangi Technical Institute using aquarium and aquaculture techniques. International Zoo Yearbook 47: 120–128. PEARCE-KELLY, P., KHELA, S., FERRI, C. & FIELD, D. (2013): Climate-change impact considerations for freshwater-fish conservation, with special reference to the aquarium and zoo community. International Zoo Yearbook 47: 81–92. PENNING, M., REID, G. McG., KOLDEWEY, H., DICK, G., ANDREWS, B., ARAI, K., GARRAT, P., GENDRON, S., LANGE, J., TANNER, K., TONGE, S., VAN DEN SANDE, P., WARMOLTS, D. & GIBSON, C. (Eds) (2009): Turning the tide: a global aquarium strategy for conservation and sustainability. Bern, Switzerland: World Association of Zoos and Aquariums. PRICE, D. J. (2010): Genetic strategies for captive breeding of viviparous fishes for conservation and other purposes: practicalities and limitations. In Viviparous fishes II: 431–434. Uribe, M. C. & Grier, H. J. (Eds). Mexico: New Life Publications/New Life Exotic Fish Inc. RAWSON, D. M., REID, G. MCG. & LLOYD, E. (2011): Conservation rationale, research applications and techniques in the cryopreservation of lower vertebrate biodiversity from marine and freshwater environments. International Zoo Yearbook 45: 108–123. REID, G. MCG. (1990): Captive breeding for the conservation of cichlid fishes. Journal of Fish Biology 37: 157–166. REID, G. MCG. & HALL, H. J. (2003): Reproduction in fishes in relation to conservation. In Reproductive science and integrated conservation: 375–395.

Holt, W. V., Pickard, A. R., Rodger, J. C. & Wildt, D. E. (Eds). Cambridge: University of Cambridge Press, for the Zoological Society of London. REID, G. McG., MACDONALD, A. A., FIDGETT, A. L., HIDDINGA, B. & LEUS, K. (Eds) (2008): Developing the research potential of zoos and aquaria. The EAZA research strategy. Amsterdam: EAZA Executive Office. REID, G. MCG., CONTRERAS MACBEATH, T. & CSATÁDI, K. (2013): Global challenges in freshwater-fish conservation related to public aquariums and the aquarium industry. International Zoo Yearbook 47: 6–45. REIS, R. E. (2013): Conserving the freshwater fishes of South America. International Zoo Yearbook 47: 65–70. ROUTH, A. (2013): Managing mycobacteriosis and associated biosecurity in the care and breeding of threatened freshwater fishes in public aquariums: an overview. International Zoo Yearbook 47: 102–111. SILAS, E. G., GOPALAKRISHNAN, A., RAMACHANDRAN, A., ANNA MERCY, T. V., KRIPAN SARKAR PUSHPANGADAN, K. R., ANIL KUMAR, P., RAM MOHAN, M. K. & ANIKUTTAN, K. K. (2011): Guidelines for green certification of freshwater ornamental fish. Kochi: Marine Products Export Development Authority. TLUSTY, M. F., RHYNE, A. L., KAUFMAN, L., HUTCHINS, M., REID, G. MCG., ANDREWS, C., BOYLE, P., HEMDAL, J., MCGILVRAY, F. & DOWD, S. (2013): Opportunities for public aquariums to increase the sustainability of the aquatic animal trade. Zoo Biology 32: 1–12. WETLANDS INTERNATIONAL (2010): Biodiversity loss and the global water crisis. A fact book on the links between biodiversity and water security. Wageningen: Wetlands International.
