Jean-Marc Hero

The Decline of the Sharp-Snouted Day Frog (Taudactylus acutirostris): The First Documented Case of Extinction by Infection in a Free-Ranging Wildlife Species?

Infectious diseases are increasingly recognized as the cause of mass mortality events, population declines, and the local extirpation of wildlife species. In a number of cases, it has been hypothesized that pathogens have caused species extinctions in wildlife. However, there is only one definitively proven case of extinction by infection, and this was in a remnant captive population of a Polynesian tree snail. In this article, we review the potential involvement of infectious disease in the recent extinction of the sharp-snouted day frog Taudactylus acutirostris. Our review of available evidence suggests that a virulent pathogen of amphibians, Batrachochytrium dendrobatidis, caused a rapid, catastrophic decline of this species, from which it did not recover. We propose that this is the first case of extinction by infection of a free-ranging wildlife species where disease acted as both the proximate and ultimate cause of extinction. This highlights a probable underreporting of infectious disease as a cause of biodiversity loss historically and currently.

Multiple determinants of Australian tropical frog biodiversity

Distribution data on rainforest frogs within 22 subregions of the Australian Wet Tropics were used to analyse biogeographic patterns in assemblage composition and diversity, and to relate these patterns to environmental factors. The ecological correlates of species richness and spatial patterns of assemblage structure suggested that the patterns of species richness fell into three categories, each being influenced by different processes. The species richness of habitat generalists was largely unaffected by rainforest variables and was primarily related to broad habitat diversity and climate. The spatial patterns of species richness of non-microhylid rainforest frogs were the result of processes associated with historical biogeography, especially extinctions and subsequent recolonisations in those subregions most affected by Quaternary fluctuations in rainforest area. This group of frogs has undergone severe population declines in recent years and the declines represent a significant loss in regional biodiversity since it is this group that produces the majority of regional variability in frog diversity. In contrast, the most significant influence on spatial patterns of microhylid species richness may have been in situ speciation in areas of consistent rainfall, driven by altitudinal gradients, isolation and low dispersal ability. These results stress the necessity of using meaningful and objective groups based on functional ecology in order to understand the determinants of biodiversity: it is not sufficient to examine patterns based purely on species richness within a broad taxonomic group.

Overview of the conservation status of Australian frogs

A review of the current conservation status of Australian amphibians was recently completed as part of a World Conservation Union (IUCN) sponsored Global Amphibian Assessment (GAA). Fifty of 216 amphibian species (23%) in Australia are now recognized as threatened or extinct in accord with IUCN Red List Categories and Criteria. Here we report on the categories and criteria under which individual species qualified for listing and provide a summary of supporting information pertaining to population and distribution declines. Major threatening processes contributing to listing of species are also reviewed.

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 10u200a183 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.

Daily behaviour and microhabitat use of the waterfall frog Litoria nannotis in Tully Gorge, Eastern Australia

[Extract] The daily activities of amphibians are influenced by their need to obtain food, mates and shelter, avoid predators, and maintain adequate physiological conditions (Dole, 1965; Beshkov and Jameson, 1980; Wool-bright, 1985; Zug, 1993; Cohen and Alford, 1996; De Oliveira, 1996). Most amphibians share certain behavioral similarities. Because of the permeability of their skin, they are highly susceptible to dehydration from evaporative water loss. Therefore most amphibians are typically nocturnal and tend to shelter in moist refuges during the day and become active only at night (Duellman and Trueb, 1986).

Characteristics distinguishing Leptodactylus pentadactylus and L. knudseni in the Central Amazon Rainforest

Etude des caracteristiques morphologiques et comportementales permettant de distinguer ces deux especes du genre Leptodactylus.Comparaison avec les donnees de la litterature, notamment pour lespece L. pentadactylus en Amerique Central.

Palatability of Bufo Marinus Tadpoles to a Vertebrate Fish Predator Decreases with Development

This investigation showed an ontogenetic shift in the palatability of Bufo marinus tadpoles by measuring consumption of tadpoles at three different developmental stages (newly hatched, intermediate and pre- metamorphic) by an Australian predatory fish, Lates calcarifer (barramundi). A known-palatable tadpole, Limnodynastes ornatus, was used as the control. B. marinus tadpoles at all developmental stages were unpalatable relative to a palatable alternative, with the later stages being the least palatable. Choice experiments further demonstrated that L. calcarifer were able to recognise and choose L. ornatus tadpoles in preference to those of B. marinus. Our experiments demonstrate that at all stages of development, B. marinus tadpoles were unpalatable to L. calcarifer. Contrary to the model proposed by Brodie and Formanowicz (1987), our results suggest an ontogenetic shift in palatability of B. marinus tadpoles to a vertebrate fish predator, with the later stages being less palatable.

Seasonal, sexual and ontogenetic variations in the diet of the 'declining' frogs Litoria nannotis, Litoria rheocola and Nyctimystes dayi

Faecal analyses were used to investigate the diets of the endangered frogs Litoria nannotis, L. rheocola and Nyctimystes dayi in Tully Gorge, North Queensland. Comparisons of diet and food availability indicate that thesespecies feed indiscriminately on a range of terrestrial and aquatic invertebrates. Changes in morphology and foraging behaviour significantly influenced diet composition and created subtle shifts in the degree of selectivity displayed in prey choice. Interspecific differences in numeric and volumetric diet composition were attributed to variations in gape size and microhabitat selection. Within the diets of L. nannotis and L. rheocola, a decline in prey selectivity observed during the dry season reflected a reduction in foraging activity. Differences in the gape size and foraging behaviour of males and females of L. nannotis were responsible for sex-specific differences in diet composition. L. nannotis also diplayed an ontogenetic shift in prey size and type. As snout-vent length increased, L. nannotis consumed fewer, but larger prey and increasingly discriminated against dipterans, dipteran larvae and hemipterans. Importantly, L. nannotis, L. rheocola and N. dayi demonstrated the capacity to compensate for fluctuations in food availability by feeding on less lucrative prey.

Austral Amphibians: Gondwanan relicts in Peril

Over 30% of Australasian amphibians are currently threatened with extinction. While habitat loss, introduced species and disease have been identified as major threats, the impacts of climate change are understudied. Threatened frogs fall into distinct biogeographical and ecological groupings that can be linked to specific threats (e.g. mountain- top endemics and climate change; stream-dwelling wet forest frogs and disease; and small island endemics and feral pests). The impacts of gradual climate change over millions of years has isolated specific species into climatic refugia (resulting in restricted geographic ranges), which combined with the ecological traits of these species (e.g. small clutch-size) dramatically increases extinction risk. Australasian frogs demonstrate intrinsic links between biogeographic history, species ecology and conservation status. The solutions to most threats are clear at a broad level, stop land clearing, reduce CO emissions and control feral animals; however, declines linked to the disease chytridiomycosis are not easily resolved. Chytridiomycosis is not a universal threat and understanding the causes of variation in impact is critically important. While the threats of land clearing, disease and introduced species are regional and/or species specific, the impacts of climate change must be examined carefully as all species are likely to affected. Here we cover these issues for Australasian frogs, presenting regional examples that highlight threats and avenues for future research and management. Phylogenetic and biogeographic history Over 30% of amphibian species are threatened with extinction globally making them the most threatened of the vertebrate groups (Wake and Vredenburg 2008). There are multiple threats to Austral frogs: e.g. disease – critically chytrid fungus for species with more aquatic lifestyles; small clutch size and limited range associated with higher decline or extinction risk; introduced species (Gambusia and trout in Australia, Gillespie and Hero, 1999; Murray et al., 2011; Rattus in New Zealand, Thurley and Bell, 1994; and mongoose in the Pacific Islands, Pernetta and Watling, 1979) and less specific threats,identified in both Austral and global analyses of amphibian declines: e.g. climate change (Hero et al., 2006, 2008; Hof et al., 2011) and habitat loss and fragmentation (Hero et al., 2008). These factors pose serious threats in many other regions of the world (Stuart, 2008) and their impacts vary among species and genera, depending on their current distribution and habitat use (Table 21.1).