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Vol. 78: 87–95, 2007 DISEASES OF AQUATIC ORGANISMS Published December 13 doi: 10.3354/dao01861 Dis Aquat Org Survey for the amphibian chytrid Batrachochytrium dendrobatidis in Hong Kong in native amphibians and in the international amphibian trade Jodi J. L. Rowley1, 5,*, Simon Kin Fung Chan2, Wing Sze Tang2, Richard Speare3, Lee F. Skerratt 4, Ross A. Alford1, Ka Shing Cheung 2, Ching Yee Ho2, Ruth Campbell4 1School of Marine and Tropical Biology and Amphibian Disease Ecology Group, James Cook University, Townsville, Queensland, Australia 4811 2Herpetofauna Working Group, Agriculture, Fisheries and Conservation Department, The Government of the Hong Kong Special Administrative Region, 7/F, Cheung Sha Wan Government Offices, 303 Cheung Sha Wan Road, Kowloon, Hong Kong, China 3School of Public Health, Tropical Medicine and Rehabilitation and Amphibian Disease Ecology Group, James Cook University, Townsville, Queensland, Australia 4811 4School of Veterinary and Biomedical Sciences and Amphibian Disease Ecology Group, James Cook University, Townsville, Queensland, Australia 4811 5Present address: Conservation International Indo-Burma, PO Box 1356, Phnom Penh, Cambodia ABSTRACT: Chytridiomycosis, caused by the pathogen Batrachochytrium dendrobatidis, is respon- sible for many amphibian declines and has been identified in wild amphibian populations on all con- tinents where they exist, except for Asia. In order to assess whether B. dendrobatidis is present on the native amphibians of Hong Kong, we sampled wild populations of Amolops hongkongensis, Paa exil- ispinosa, P. spinosa and Rana chloronota during 2005–2006. Amphibians infected with B. dendro- batidis have been found in the international trade, so we also examined the extent and nature of the amphibian trade in Hong Kong during 2005–2006, and assessed whether B. dendrobatidis was pre- sent in imported amphibians. All 274 individuals of 4 native amphibian species sampled tested neg- ative for B. dendrobatidis, giving an upper 95% confidence limit for prevalence of 1.3%. Approxi- mately 4.3 million amphibians of 45 species from 11 countries were imported into Hong Kong via air over 12 mo; we did not detect B. dendrobatidis on any of 137 imported amphibians sampled. As B. dendrobatidis generally occurs at greater than 5% prevalence in infected populations during favor- able environmental conditions, native amphibians in Hong Kong appear free of B. dendrobatidis, and may be at severe risk of impact if it is introduced. Until it is established that the pathogen is present in Hong Kong, management strategies should focus on preventing it from being imported and decreasing the risk of it escaping into the wild amphibian populations if imported. Further research is needed to determine the status of B. dendrobatidis in Hong Kong with greater certainty. KEY WORDS: Batrachochytrium dendrobatidis · Amphibian chytrid fungus · Chytridiomycosis · Asia · China · Disease · Wildlife trade · Frogs Resale or republication not permitted without written consent of the publisher INTRODUCTION Acquired Immunodeficiency Syndrome, Severe Acute Respiratory Syndrome, and H5N1 Avian Influenza. In In recent decades, a number of pathogenic infec- addition to those that are direct threats to human tious diseases that represent a substantial global health, infectious diseases affecting wildlife and plant threat to human health have emerged, including populations are emerging at unusually high rates and *Email: [email protected] © Inter-Research 2007 · www.int-res.com 88 Dis Aquat Org 78: 87–95, 2007 currently pose a great threat to the conservation of The amphibian trade often presents an ideal oppor- global biodiversity (Harvell et al. 1999, Ward & Laf- tunity for dispersal and transport of pathogens. ferty 2004). Species that are thought to have declined Amphibians are transported in crowded conditions, in or been eliminated due to disease are taxonomically contact with multiple other species from many source diverse and include island land birds (Warner 1968, regions, and may escape or be deliberately released van Riper et al. 1986), grassland mammals (Thorne & into natural habitats carrying their associated patho- Williams 1988, Ginsberg et al. 1995), snails (Daszak & gens and parasites. Therefore, it is extremely impor- Cunningham 1999) and frogs (Berger et al. 1998, tant to assess the risk posed by the amphibian trade, Bosch et al. 2001, Bradley et al. 2002, Weldon & Du particularly in areas not presently known to contain Preez 2004, Lips et al. 2006, Rachowicz et al. 2006, Batrachochytrium dendrobatidis. Schloegel et al. 2006). Hong Kong is one of the major world centres for the Perhaps the most alarming wildlife disease known at global amphibian trade, largely due to its strong trans- present is chytridiomycosis, a potentially fatal disease port and economic links with mainland China and of amphibians caused by the pathogen Batracho- many other countries, its open trading policy, economic chytrium dendrobatidis (Berger et al. 1998, Lips et al. success and high demand for wildlife consumption 2003a). Chytridiomycosis is an emerging infectious (Lau et al. 1995). In addition, the keeping of amphib- disease implicated in mass mortalities, population ians as pets is becoming increasingly popular in Hong declines and extinctions of amphibian populations and Kong, with amphibians imported for both local sale species around the world (Berger et al. 1998, Lips 1999, and re-export (Lau et al. 1995). Many Asian countries, Bosch et al. 2001, Bradley et al. 2002, Weldon & Du such as China, Thailand and Indonesia, are major Preez 2004, Lips et al. 2006, Rachowicz et al. 2006). To breeders of food amphibians, producing more than date, B. dendrobatidis has been identified in all conti- 1000 tonnes per country per year (Daszak et al. 2006). nents where wild amphibian populations exist, except Although the trade in amphibians as food in Hong for Asia. However, there has been little survey effort Kong has largely been dominated by Chinese bullfrogs for B. dendrobatidis in Asia. Hoplobatrachus rugulosus from Southeast Asia and The origin of Batrachochytrium dendrobatidis is mainland China, amphibians for the pet trade are controversial, with some groups proposing that B. imported from around the world (Lau et al. 1995). In dendrobatidis is a virulent pathogen spreading addition, Hong Kong is also a transit port for Chinese through amphibian populations (e.g. Skerratt et al. goods intended for international markets (Lau et al. 2007) and others arguing that the evidence is not yet 1995). If Batrachochytrium dendrobatidis is present on strong enough to determine whether B. dendroba- amphibians imported into Hong Kong, this may pose a tidis has recently been dispersed or was widely serious threat to the native amphibians of the region. endemic in amphibian populations prior to their Hong Kong contains 24 native amphibian species, decline (e.g. Rachowicz et al. 2005). If it has recently including a number of species that are endangered, been dispersed from a single origin, it may have near threatened or vulnerable (Chan et al. 2005). The escaped from South Africa via the scientific and climate of the region is likely to be suitable for B. den- medical trade in the African clawed frog Xenopus drobatidis (Ron 2005). All these factors make Hong laevis (Weldon et al. 2004) and become established Kong an ideal location to conduct the first systematic in North America in the early 1960s (Ouellet et al. survey for B. dendrobatidis in mainland Asia. 2005) and Australia in the late 1970s (Berger et al. We therefore aimed to conduct the first systematic 1999). It may also have been dispersed by inter- survey for Batrachochytrium dendrobatidis in China, national trade in amphibians for other purposes (OIE and the most comprehensive to date in Asia, to deter- 2006). Amphibians infected with B. dendrobatidis mine whether B. dendrobatidis occurs in the native have been found in the scientific (Reed et al. 2000, amphibians of Hong Kong. In addition, we aimed to Parker et al. 2002, Weldon et al. 2004), pet (Groff et determine the extent and nature of the amphibian al. 1991, Berger et al. 1999, Mutschmann et al. 2000, trade in Hong Kong, and to assess whether B. dendro- Cunningham et al. 2005), food (Mazzoni et al. 2003, batidis was present in amphibians sold in Hong Kong’s Hanselmann et al. 2004, Garner et al. 2006) and zoo- markets as part of the food and pet trades. logical trades (Nichols et al. 1998, 2001, Pessier et al. 1999, Raverty & Reynolds 2001, Oevermann et al. 2005). Therefore, the trade and human-assisted MATERIALS AND METHODS movement of amphibians may cause disease out- breaks within continents by introducing B. dendroba- Native amphibians of Hong Kong. In order to assess tidis into new areas, or into areas with different whether Batrachochytrium dendrobatidis was present strains of the pathogen. in the native amphibians of Hong Kong, we selected 4 Rowley et al.: Hong Kong amphibian chytrid survey 89 species of native frogs that we considered most likely Frogs were sampled between December 2005 and to be infected with B. dendrobatidis based upon the October 2006. We attempted to sample all frogs during characteristics of infected amphibians in other coun- the winter (December–January in Hong Kong), when tries: the Hong Kong cascade frog Amolops hongkon- higher host infection prevalence and mortality are typ- gensis (Ranidae; World Conservation Union [IUCN] ically observed (Bradley et al. 2002, Berger et al. 2004,