Robert Puschendorf

Widespread amphibian extinctions from epidemic disease driven by global warming

As the Earth warms, many species are likely to disappear, often because of changing disease dynamics. Here we show that a recent mass extinction associated with pathogen outbreaks is tied to global warming. Seventeen years ago, in the mountains of Costa Rica, the Monteverde harlequin frog (Atelopus sp.) vanished along with the golden toad (Bufo periglenes). An estimated 67% of the 110 or so species of Atelopus, which are endemic to the American tropics, have met the same fate, and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) is implicated. Analysing the timing of losses in relation to changes in sea surface and air temperatures, we conclude with ‘very high confidence’ (> 99%, following the Intergovernmental Panel on Climate Change, IPCC) that large-scale warming is a key factor in the disappearances. We propose that temperatures at many highland localities are shifting towards the growth optimum of Batrachochytrium, thus encouraging outbreaks. With climate change promoting infectious disease and eroding biodiversity, the urgency of reducing greenhouse-gas concentrations is now undeniable.

Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis

BackgroundRescuing amphibian diversity is an achievable conservation challenge. Disease mitigation is one essential component of population management. Here we assess existing disease mitigation strategies, some in early experimental stages, which focus on the globally emerging chytrid fungus Batrachochytrium dendrobatidis. We discuss the precedent for each strategy in systems ranging from agriculture to human medicine, and the outlook for each strategy in terms of research needs and long-term potential.ResultsWe find that the effects of exposure to Batrachochytrium dendrobatidis occur on a spectrum from transient commensal to lethal pathogen. Management priorities are divided between (1) halting pathogen spread and developing survival assurance colonies, and (2) prophylactic or remedial disease treatment. Epidemiological models of chytridiomycosis suggest that mitigation strategies can control disease without eliminating the pathogen. Ecological ethics guide wildlife disease research, but several ethical questions remain for managing disease in the field.ConclusionsBecause sustainable conservation of amphibians in nature is dependent on long-term population persistence and co-evolution with potentially lethal pathogens, we suggest that disease mitigation not focus exclusively on the elimination or containment of the pathogen, or on the captive breeding of amphibian hosts. Rather, successful disease mitigation must be context specific with epidemiologically informed strategies to manage already infected populations by decreasing pathogenicity and host susceptibility. We propose population level treatments based on three steps: first, identify mechanisms of disease suppression; second, parameterize epizootiological models of disease and population dynamics for testing under semi-natural conditions; and third, begin a process of adaptive management in field trials with natural populations.

Environmental refuge from disease-driven amphibian extinction.

Species that are tolerant of broad environmental gradients may be less vulnerable to epizootic outbreaks of disease. Chytridriomycosis, caused by the fungus Batrachochytrium dendrobatidis, has been linked to extirpations and extinctions of amphibian species in many regions. The pathogen thrives in cool, moist environments, and high amphibian mortality rates have commonly occurred during chytridiomycosis outbreaks in amphibian populations in high-elevation tropical rainforests. In Australia several high-elevation species, including the armored mist frog (Litoria lorica), which is designated as critically endangered by the International Union for the Conservation of Nature (IUCN), were believed to have gone extinct during chytridiomycosis outbreaks in the 1980s and early 1990s. Species with greater elevational ranges disappeared from higher elevations, but remained common in the lowlands. In June 2008, we surveyed a stream in a high-elevation dry sclerophyll forest and discovered a previously unknown population of L. lorica and a population of the waterfall frog (Litoria nannotis). We conducted 6 additional surveys in June 2008, September 2008, March 2009, and August 2009. Prevalences of B. dendrobatidis infection (number infected per total sampled) were consistently high in frogs (mean 82.5%, minimum 69%) of both species and in tadpoles (100%) during both winter (starting July) and summer (starting February). However, no individuals of either species showed clinical signs of disease, and they remained abundant (3.25 - 8.75 individuals of L. lorica and 6.5-12.5 individuals of L. nannotis found/person/100 m over 13 months). The high-elevation dry sclerophyll site had little canopy cover, low annual precipitation, and a more defined dry season than a nearby rainforest site, where L. nannotis was more negatively affected by chytridiomycosis. We hypothesize this lack of canopy cover allowed the rocks on which frogs perched to warm up, thereby slowing growth and reproduction of the pathogen on the hosts. In addition, we suggest surveys for apparently extinct or rare species should not be limited to core environments.

Ecology: Clouded futures

Global warming is altering the distribution and abundance of plant and animal species. Application of a basic law of ecology predicts that many will vanish if temperatures continue to rise.

Amphibian Chytrid Fungus Broadly Distributed in the Brazilian Atlantic Rain Forest

To investigate the occurrence of the chytrid fungus Batrachochytrium dendrobatidis in Brazil, we conducted histological screenings of 96 preserved specimens of anurans collected at 10 sites in the Atlantic rain forest. Data show this fungus to be widely distributed. Infected specimens included Colostethus olfersioides (Dendrobatidae), Bokermannohyla gouveai and Hypsiboas freicanecae (Hylidae), as well as Thoropa miliaris and Crossodactylus caramaschii (Leptodactylidae), extending the area of B. dendrobatidis occurrence in Brazil approximately 1,600 km N, 200 km S, and 270 km E. The altitudinal range of the chytrid is broad, spanning from less than 100 m (Estação Ecológica Juréia-Itatins, Reserva Biológica do Tinguá) to about 2,400 m (Parque Nacional do Itatiaia). An infection record dating to 1981 roughly coincides with the time of the first observations of amphibian declines in the country. Widespread occurrence of B. dendrobatidis in the Atlantic Forest adds to the challenge of conserving an already endangered biome given the potential risk of further local biodiversity loss. Further research is needed to understand how environmental and genetic factors relate to chytridiomycosis in leading to or preventing local die-offs. Protected sites at mid and high elevations may be particularly threatened, while lowland populations may be functioning as reservoirs. Conservation efforts should also involve monitoring studies and habitat protection.

Context-dependent conservation responses to emerging wildlife diseases

Emerging infectious diseases pose an important threat to wildlife. While established protocols exist for combating outbreaks of human and agricultural pathogens, appropriate management actions before, during, and after the invasion of wildlife pathogens have not been developed. We describe stage-specific goals and management actions that minimize disease impacts on wildlife, and the research required to implement them. Before pathogen arrival, reducing the probability of introduction through quarantine and trade restrictions is key because prevention is more cost effective than subsequent responses. On the invasion front, the main goals are limiting pathogen spread and preventing establishment. In locations experiencing an epidemic, management should focus on reducing transmission and disease, and promoting the development of resistance or tolerance. Finally, if pathogen and host populations reach a stable stage, then recovery of host populations in the face of new threats is paramount. Successful management of wildlife disease requires risk-taking, rapid implementation, and an adaptive approach.

The distribution and host range of the pandemic disease chytridiomycosis in Australia, spanning surveys from 1956–2007

Chytridiomycosis is the worst disease to affect vertebrate biodiversity on record. In Australia, it is thought to have caused the extinction of four frog species, and it threatens the survival of at least 10 more. We report the current distribution and host range of this invasive disease in Australia, which is essential knowledge for conservation management. We envisage that the data be used in a global and national context for predictive modeling, meta-analyses, and risk assessment. Our continent-wide data set comprises 821 sites in Australia and includes 10 183 records from >80 contributors spanning collection dates from 1956 to 2007. Sick and dead frogs from the field and apparently healthy frogs from museum collections were tested opportunistically for the presence of Batrachochytrium dendrobatidis, the fungal pathogen causing chytridiomycosis, and apparently healthy frogs and tadpoles found during surveys were tested purposively. The diagnostic tests used were histology of skin samples and quantitative PCR of skin swabs. Chytridiomycosis was found in all Australian states and the Australian Capital Territory, but not in the Northern Territory. Currently it appears to be confined to the relatively cool and wet areas of Australia, such as along the Great Dividing Range and adjacent coastal areas in the eastern mainland states of Queensland, New South Wales, and Victoria, eastern and central Tasmania, southern South Australia, and southwestern Western Australia. Batrachochytrium dendrobatidis may have been introduced into Australia via the port of Brisbane around 1978 and spread northward and southward. It did not appear to arrive in Western Australia until 1985. The earliest records from South Australia and Tasmania are from 1995 and 2004, respectively, although archival studies from these states are lacking. We also report negative findings showing that the disease does not currently occur in some areas that appear to be environmentally suitable, including Cape York Peninsula in Queensland and most of the World Heritage Area in western Tasmania. Infection with B. dendrobatidis has been recorded from 63 frog species in Australia to date, all belonging to the Hylidae, Limnodynastidae, and Myobatrachidae, with the exception of one individual of a species from the Microhylidae and the introduced cane toad of the family Bufonidae.

DETECTION OF BATRACHOCHYTRIUM DENDROBATIDIS IN ELEUTHERODACTYLUS FITZINGERI: EFFECTS OF SKIN SAMPLE LOCATION AND HISTOLOGIC STAIN

Batrachochytrium dendrobatidis is a fungal pathogen that has been implicated in amphibian declines worldwide. Histopathologic techniques have been used to diagnose the disease, but their sensitivity has not been determined. It is also unclear whether the probability of detection varies between skin samples derived from different body parts. We examined 24 Fitzingers rainfrogs (Eleutherodactylus fitzingeri) with chytridiomycosis. This is a common frog species with a broad range and high abundance throughout most of Costa Rica. We sampled 12 different body parts from each animal, and alternated the staining between a routinely used stain (hematoxylin and eosin [H&E]), and a more fungus-specific stain (periodic acid–Schiff [PAS]). The pelvic patch and the innermost finger of the hand were consistently the best places to detect the disease, although significant differences were found only with the gular area, the abdomen, and toes four and five. We found more positive samples using PAS than using H&E in all body parts, although significant differences were detected only in samples derived from the pelvic patch. Using the best combination of factors (stain and body part) and animals with the lightest infections (to test the sensitivity of the technique), we calculated that at least 17 sections are needed in order to reach 95% confidence that a frog is or is not infected. We conclude that the choice of stain and body part can significantly alter estimates of prevalence of B. dendrobatidis.

Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America

The virulence of a pathogen can vary strongly through time. While cyclical variation in virulence is regularly observed, directional shifts in virulence are less commonly observed and are typically associated with decreasing virulence of biological control agents through coevolution. It is increasingly appreciated, however, that spatial effects can lead to evolutionary trajectories that differ from standard expectations. One such possibility is that, as a pathogen spreads through a naive host population, its virulence increases on the invasion front. In Central America, there is compelling evidence for the recent spread of pathogenic Batrachochytrium dendrobatidis (Bd) and for its strong impact on amphibian populations. Here, we re-examine data on Bd prevalence and amphibian population decline across 13 sites from southern Mexico through Central America, and show that, in the initial phases of the Bd invasion, amphibian population decline lagged approximately 9 years behind the arrival of the pathogen, but that this lag diminished markedly over time. In total, our analysis suggests an increase in Bd virulence as it spread southwards, a pattern consistent with rapid evolution of increased virulence on Bds invading front. The impact of Bd on amphibians might therefore be driven by rapid evolution in addition to more proximate environmental drivers.

Chytridiomycosis in Wild Frogs from Pico Bonito National Park, Honduras

Almost half of the endemic species of Honduran amphibians have declining populations; some of which seem to be extinct since they have not been seen in several years in places where they were once common. Disappearances in pristine and protected habitats have occurred in several highland localities throughout the country. The highland amphibian fauna of Pico Bonito National Park declined sometime between 1989 and 1995. An amphibian chytrid fungus, Batrachochytrium dendrobatidis has been linked to similar declines in other neotropical regions. We checked 19 specimens for this disease, which were collected in the park in 2003. The only Rana maculata examined was found to be infected, as were three of the six Eleutherodactylus aurilegulus surveyed for the disease. Two of the infected E. aurilegulus were collected at 120 m elevation and showed strong infections. One of these was lethargic and did not react when it was collected in the field, although it was still alive. A complete necropsy could help determine if the B. dendrobatidis infection was responsible for these symptoms, and further research might show how susceptible E. aurilegulus is to this pathogen at low altitudes. More research should be focused on the distribution of this pathogen in Honduras, and on how this disease has affected the local amphibian fauna.