Infectious Disease Threats to Amphibian Conservation

The Glasgow Naturalist (2018) Volume 27, Supplement. The Amphibians and Reptiles of Scotland Infectious disease threats to amphibian conservation A.A. Cunningham Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY E-mail: [email protected] ABSTRACT Amphibian Populations Task Force (DAPTF) to The unexplained decline of amphibian populations investigate if the reported declines of amphibians across the world was first recognised in the late 20th was a true phenomenon and, if so, what was, or were, century. When investigated, most of these the cause(s) of it. The DAPTF brought together “enigmatic” declines have been shown to be due to experts from across the world and from across one of two types of infectious disease: ranavirosis disciplines to promote research into amphibian caused by infection with FV3-like ranavirus or with declines and to collate and evaluate evidence that common midwife toad virus, or chytridiomycosis showed amphibians were undergoing caused by infection with Batrachochytrium unprecedented declines around the world including dendrobatidis or B. salamandrivorans. In all cases in protected areas and in pristine habitats. Indeed, it examined, infection has been via the human- is now known that 41% of known amphibian species mediated introduction of the pathogen to a species are threatened with extinction, which is a much or population in which it has not naturally co- higher percentage than for mammals (25%) and evolved. While ranaviruses and B. salamandrivorans over three times the percentage for birds (13%) have caused regionally localised amphibian (IUCN, 2018). Perhaps just as worrying is that over population declines in Europe, the chytrid fungus, B. 61% of known amphibian species are either “Not dendrobatidis, has caused catastrophic multi-species Evaluated” or have out-of-date assessments; this amphibian population declines and species compares to just 0.2% of mammals and 0% of birds extinctions globally. These diseases have already (Tapley et al., 2018). caused the loss of amphibian biodiversity, and over 40% of known amphibian species are threatened Initially, habitat destruction, overexploitation, with extinction. If this biodiversity loss is to be excessive UV-B irradiation, pesticide use, acid rain halted, it is imperative that regulations are put in and other pollutants were all put forward as likely place – and enforced – to prevent the spread of causes of the amphibian decline phenomenon. known and yet-to-be discovered amphibian Through the work of the DAPTF’s Diseases and pathogens. Also, it is incumbent on those who keep Pathology Working Group, however, infectious or study amphibians to take measures to minimise disease - and one in particular, chytridiomycosis due the risk of disease spread, including from captive to infection with the non-hyphal, zoosporic fungus, B. animals to those in the wild. dendrobatidis - was identified as elevating amphibian mortality rates and driving amphibian INTRODUCTION population declines across multiple continents When the first World Congress of Herpetology was (Cunningham, 1998). This fungus was discovered held in Canterbury, Kent in 1989, no papers were contemporaneously as the cause of multi-species presented about the amphibian conservation crisis. mortality of wild amphibians where frog populations It was only during social interactions at coffee and were declining catastrophically in the rain forests of tea breaks and in the evenings that many Panama and Australia (Berger et al., 1998) and was herpetologists from around the world realised that it named following its isolation from a captive blue was not only their own study species that appeared poison dart frog (Dendrobates azureus) (Longcore et to be undergoing declines or even local al., 1999). disappearances, but also those being studied by many of their colleagues. Whilst “localised” declines While previously dismissed as being irrelevant to were initially thought to be due to natural population species demographics, in recent decades infectious cycles or local, short-term factors such as extreme disease has been increasingly identified as a driver of weather events, it soon became clear that there was species declines and extinctions (Daszak et al., 2000; a larger issue affecting amphibians and a call for Cunningham et al., 2017). For amphibians, in action was made. particular, there is now substantial and irrefutable evidence of the role of infectious disease in multiple In response, the International Union for the species declines and in some species extinctions (e.g. Conservation of Nature (IUCN) set up the Declining Schloegel et al., 2006; Skerratt et al., 2007). The presence of disease, however, should not always be incidents, described globally (Duffus et al., 2015). Of seen as a negative thing. Disease-causing agents, these, only two have been shown to cause long-term such as pathogens, are important components of amphibian population declines: a frog virus 3-like ecosystems, often crucial for the regulation of ranavirus in the U.K (Teacher et al., 2010) and species abundances and for ecosystem function; for common midwife toad virus (CMTV) in Spain (Price example, the experimental removal of fungal et al., 2014). Ranavirus-associated amphibian pathogens from rain forest plants has been shown to mortality was first detected in the U.K. in the early adversely affect biodiversity through the reduction 1990s, although it had probably been occurring for of species richness (Bagchi et al., 2014). When some years before this (Drury et al., 1995; infectious disease threatens species conservation it Cunningham et al., 1996). Large disease outbreaks is inevitably a consequence of human-mediated involving the deaths of tens or hundreds of animals, factors that have decreased the resilience of a species usually the common frog (Rana temporaria), but also to a pre-existing pathogen, or that have introduced a the common toad (Bufo bufo), were reported “novel” pathogen to a naïve species (Cunningham et (Cunningham et al., 1996; Cunningham et al., 2007). al., 2003). In most cases, outbreaks affected adult animals, occurred in the summer months and were peracute When pathogens are in the “wrong” place (i.e. in (i.e. very short period from first signs of illness to species or locations in which they did not co-evolve), death), with a large number of dead animals being their presence can lead to adverse effects on found in the vicinity of a breeding pond over a short biodiversity and ecosystem function (Cunningham period of time (hours or days) (Fig. 1). In the U.K, two 1996; Daszak et al., 2000; Cunningham et al., 2017). types of disease (or syndrome) have been described This usually is consequent to human-mediated due to ranavirus infection: haemorrhagic syndrome introduction: a process which has been termed and skin-ulceration syndrome (Cunningham et al., “pathogen pollution” (Cunningham et al., 2003). The 1996; Cunningham, 2001). With haemorrhagic introduction of pathogens can have long-term, syndrome, affected animals – although dead - usually profound and unpredictable impacts on nature. One appear normal from the outside, although bleeding example of this is the introduction of myxomatosis to might be seen from the mouth or vent and the skin the rabbit (Oryctolagus cuniculus) population in the can appear reddened, especially on the underside of United Kingdom (U.K). Who could have predicted the hind legs and body. On post mortem examination, that, through complex interactions between rabbits, animals are often in good body condition but with grasses, wild thyme (Thymus polytrichus), and a red evidence of bleeding throughout most of the body ant (Myrmica sabuleti), that the introduction of a systems, including into the gastro-intestinal tract, rabbit virus would, over a course of 30 years, lead to reproductive tract, skeletal musculature, and even the extinction of the large blue butterfly (Maculinea into the fat bodies (stores). These animals are killed arion) in the U.K. (Sumption & Flowerdew, 1985)? very quickly by the virus; usually within a matter of hours after the first onset of illness. Animals which Until recently, amphibians were very much the develop skin-ulceration syndrome, however, can be “Cinderella” of the wildlife disease world, with very ill for weeks or even months before they die. These little attention being given to identifying, animals develop skin ulceration, which can be understanding or mitigating the causes of amphibian extensive and which can occur over any part of the morbidity or mortality. Many advances in this field body but is most frequently seen over the ventral have been made in the past 30 years or so. However, hind legs (Fig. 2). Affected animals can also undergo although many infectious diseases of amphibians are necrosis (death) of the limbs. While, if present, this now recognised – and there are undoubtedly many usually affects the hind and fore feet, it can extend more waiting to be discovered – only two have been higher up the limbs to reach the body. During the shown to cause amphibian population declines in period of illness, animals stop feeding and become wild populations: ranavirosis and chytridiomycosis. listless and lethargic. By the time they die they are The key points about these diseases, with particular usually in very poor body condition and sometimes reference to the situation in the U.K., will now be are emaciated. There is, however, some evidence reviewed. that a small proportion of common frogs affected

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