Deborah S. Bower

Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian

Ontogenetic changes in disease susceptibility have been demonstrated in many vertebrate taxa, as immature immune systems and limited prior exposure to pathogens can place less developed juveniles at a greater disease risk. By causing the disease chytridiomycosis, Batrachochytrium dendrobatidis (Bd) infection has led to the decline of many amphibian species. Despite increasing knowledge on how Bd varies in its effects among species, little is known on the interaction between susceptibility and development within host species. We compared the ontogenetic susceptibility of post-metamorphic green and golden bell frogs Litoria aurea to chytridiomycosis by simultaneously measuring three host-pathogen responses as indicators of the development of the fungus—infection load, survival rate, and host immunocompetence—following Bd exposure in three life stages (recently metamorphosed juveniles, subadults, adults) over 95xa0days. Frogs exposed to Bd as recently metamorphosed juveniles acquired higher infection loads and experienced lower immune function and lower survivorship than subadults and adults, indicating an ontogenetic decline in chytridiomycosis susceptibility. By corresponding with an intrinsic developmental maturation in immunocompetence seen in uninfected frogs, we suggest these developmental changes in host susceptibility in L. aurea may be immune mediated. Consequently, the physiological relationship between ontogeny and immunity may affect host population structure and demography through variation in life stage survival, and understanding this can shape management targets for effective amphibian conservation.

Island provides a pathogen refuge within climatically suitable area

Surveillance of pathogens can lead to significant advances towards making effective decisions in research and management for species threatened by disease. Batrachochytrium dendrobatidis has been a major contributing factor to the global decline of amphibians. Knowledge of the distribution of B. dendrobatidis can contribute to understanding patterns of species decline and prioritizing action. Therefore, we surveyed four spatially distinct populations of a B. dendrobatidis susceptible species, the green and golden bell frog (Litoria aurea), for evidence of infection in the population. Three mainland populations were infected at a prevalence of 3.5–28.3xa0%, with median infection loads of 0.28–627.18 genomic equivalents (GE). Conversely, we did not detect infection in an island population 3xa0km from the mainland; the isolation and infrequent visitation of the island suggests that the pathogen has not arrived. Management actions for B. dendrobatidis and conservation of susceptible frog species are heavily dependent on the presence and absence of the pathogen in the population. Prevention of the accidental introduction of B. dendrobatidis and safe guarding genetic diversity of L. aurea is necessary to preserve unique diversity of the island population, whereas containment and control of the pathogen can be directed towards mainland populations. Knowledge of disease dynamics also provides a context to understand the ecology of remaining populations as variation in the physiology or habitat of the mainland populations have facilitated persistence of these populations alongside B. dendrobatidis. Other islands should be a priority target in disease surveillance, to discover refuges that can assist conservation.

Amphibians on the brink

Preemptive policies can protect amphibians from devastating fungal diseases Over the past three decades, the emergence of a globalized pandemic lineage of chytrid fungus (Batrachochytrium dendrobatidis) has caused declines of amphibian species in Central America, Europe, Australia, and North America (see the figure). By 2004, where documented, 43.2% of amphibian species globally experienced some level of population decrease, and the amphibian chytrid fungus was identified as a major contributing factor for hundreds of species (1). The recent discovery of a related but functionally distinct chytrid fungus, Batrachochytrium salamandrivorans, that has begun exterminating salamanders in Europe (2) fulfills predictions that further infectious fungal pathogens will continue to emerge (3). The threat of chytrids and similar fungal pathogens to areas where they have not yet emerged—for example, in New Guinea—is of critical conservation concern.

Realistic heat pulses protect frogs from disease under simulated rainforest frog thermal regimes

Recent emergences of fungal diseases have caused catastrophic global losses of biodiversity. Temperature is one of the most important factors influencing host–fungus associations but the effects of temperature variability on disease development are rarely examined. n nThe chytrid pathogen Batrachochytrium dendrobatidis (Bd) has had severe effects on populations of hundreds of rainforest-endemic amphibian species but we know little about the effects of rainforest-specific host body temperature cycles on infection patterns. n nTo address this challenge, we used body temperature regimes experienced in nature by frogs in the Australian Wet Tropics to guide a controlled experiment investigating the effects of body temperature fluctuations on infection patterns in a model host (Litoria spenceri), with emphasis on exposing frogs to realistic “heat pulses” that only marginally exceed the thermal optimum of the fungus. We then exposed cultured Bd to an expanded array of heat pulse treatments and measured parameters of population growth to help resolve the role of host immunity in our in vivo results. n nInfections developed more slowly in frogs exposed to daily 4-hr heat pulses of 26°C or 29°C than in frogs in constant temperature treatments without heat pulses (control). Frogs that experienced heat pulses were also less likely to exceed infection intensities at which morbidity and mortality become likely. Ten of 11 (91%) frogs from the daily 29°C heat pulse treatment even cleared their infections after approximately 9 weeks. n nCultured Bd also grew more slowly when exposed to heat pulses than in constant-temperature control treatments, suggesting that mild heat pulses have direct negative effects on Bd growth in nature, but precluding us from determining whether there was a concurrent benefit of heat pulses to host immunity. n nOur results suggest that even in habitats where average temperatures may be suitable for fungal growth and reproduction, infection risk or the outcome of existing infections may be heavily influenced by short but frequent exposures to temperatures that only slightly exceed the optimum for the fungus. n nOur findings provide support for management interventions that promote warm microenvironments for hosts, such as small-scale removal of branches overhanging critical habitat or provision of artificial heat sources.

Infection increases vulnerability to climate change via effects on host thermal tolerance

Unprecedented global climate change and increasing rates of infectious disease emergence are occurring simultaneously. Infection with emerging pathogens may alter the thermal thresholds of hosts. However, the effects of fungal infection on host thermal limits have not been examined. Moreover, the influence of infections on the heat tolerance of hosts has rarely been investigated within the context of realistic thermal acclimation regimes and potential anthropogenic climate change. We tested for effects of fungal infection on host thermal tolerance in a model system: frogs infected with the chytrid Batrachochytrium dendrobatidis. Infection reduced the critical thermal maxima (CTmax) of hosts by up to ~4u2009°C. Acclimation to realistic daily heat pulses enhanced thermal tolerance among infected individuals, but the magnitude of the parasitism effect usually exceeded the magnitude of the acclimation effect. In ectotherms, behaviors that elevate body temperature may decrease parasite performance or increase immune function, thereby reducing infection risk or the intensity of existing infections. However, increased heat sensitivity from infections may discourage these protective behaviors, even at temperatures below critical maxima, tipping the balance in favor of the parasite. We conclude that infectious disease could lead to increased uncertainty in estimates of species’ vulnerability to climate change.

Fighting an uphill battle: the recovery of frogs in Australia's Wet Tropics

[Extract] In the 1980s and early 1990s, an outbreak of the fungal disease chytridiomycosis caused multiple species of frog to decline or disappear throughout the Wet Tropics of northern Queensland, Australia (Richards et al. 1993, McDonald and Alford 1999). This disease is caused by the pathogen Batrachochytrium dendrobatidis (Bd; Berger et al. 1998), which does not grow well at warm temperatures (Piotrowski et al. 2004). As a result, the declines often followed elevational gradients, with the most severe declines occurring at cool, high‐elevation sites. For example, populations of the waterfall frog (Litoria nannotis), common mist frog (Litoria rheocola), and Australian lace‐lid frog (Litoria [Nyctimystes] dayi) disappeared above 300–400 m, but these species did not decline noticeably in the lowlands (Richards et al. 1993; Laurance et al. 1996; McDonald and Alford 1999). The green‐eyed tree frog (Litoria serrata; formerly L. genimaculata) also declined sharply above 300–400 m, but it did not completely disappear from those sites (Richards and Alford 2005). Although these declines and disappearances are well documented, much less attention has been given to the fact that many of the upland populations have recovered to varying degrees, even though Bd persists at a relatively high prevalence.

Effects of emerging infectious diseases on host population genetics: a review

Emerging infectious diseases threaten the survival of many species and populations by causing large declines and altering life history traits and population demographics. Therefore, it is imperative to understand how diseases impact wildlife populations so that effective management strategies can be planned. Many studies have focused on understanding the ecology of host/pathogen interactions, but it is equally important to understand the effects on host population genetic structure. In this review, we examined the literature on how infectious diseases influence host population genetic makeup, with a particular focus on whether or not they alter gene flow patterns, reduce genetic variability, and drive selection. Although the results were mixed, there was evidence for all of these outcomes. Diseases often fragmented populations into small, genetically distinct units with limited gene flow among them. In some cases, these isolated populations showed the genetic hallmarks of bottlenecks and inbreeding, but in other populations, there was sufficient gene flow or enough survivors to prevent genetic drift and inbreeding. Direct evidence of diseases acting as selective pressures in wild populations is somewhat limited, but there are several clear examples of it occurring. Also, several studies found that gene flow can impact the evolution of small populations either beneficially, by providing them with variation, or detrimentally, by swamping them with alleles that are not locally adaptive. Thus, differences in gene flow levels may explain why some species adapt while others do not. There are also intermediate cases, whereby some species may adapt to disease, but not at a rate that is meaningful for conservation purposes.

The role of non-declining amphibian species as alternative hosts for Batrachochytrium dendrobatidis in an amphibian community

Abstract Context. Pathogens with reservoir hosts have been responsible for most disease-induced wildlife extinctions because the decline of susceptible hosts does not cause the decline of the pathogen. The existence of reservoirs for Batrachochytrium dendrobatidis limits population recovery and conservation actions for threatened amphibians. As such, the effect of reservoirs on disease risk within host community assemblages needs to be considered, but rarely is. Aims. In this study we aimed to determine if amphibian species co-occurring with the green and golden bell frog Litoria aurea, a declining species susceptible to B. dendrobatidis, act as alternate hosts. Methods. We quantified B. dendrobatidis infection levels, sub-lethal effects on body condition and terminal signs of disease in amphibian communities on Kooragang Island and Sydney Olympic Park in New South Wales, Australia, where two of the largest remaining L. aurea populations persist. Key results. We found L. aurea carried infections at a similar prevalence (6–38%) to alternate species. Infection loads ranged widely (0.01–11u2009107.3 zoospore equivalents) and L. aurea differed from only one alternate host species (higher median load in Litoria fallax) at one site. There were no terminal or sub-lethal signs of disease in any species co-occurring with L. aurea. Conclusion. Our results suggest that co-occurring species are acting as alternate hosts to L. aurea and whether their presence dilutes or amplifies B. dendrobatidis in the community is a priority for future research. Implications. For L. aurea and many other susceptible species, confirming the existence of reservoir hosts and understanding their role in community disease dynamics will be important for optimising the outcomes of threat mitigation and habitat creation initiatives for their long-term conservation.

Salinity tolerances and use of saline environments by freshwater turtles: implications of sea level rise: Freshwater turtles in saline environments

The projected rise in global mean sea levels places many freshwater turtle species at risk of saltwater intrusion into freshwater habitats. Freshwater turtles are disproportionately more threatened than other taxa; thus, understanding the role of salinity in determining their contemporary distribution and evolution should be a research priority. Freshwater turtles are a slowly evolving lineage; however, they can adapt physiologically or behaviourally to various levels of salinity and, therefore, temporarily occur in marine or brackish environments. Here, we provide the first comprehensive global review on freshwater turtle use and tolerance of brackish water ecosystems. We link together current knowledge of geographic occurrence, salinity tolerance, phylogenetic relationships, and physiological and behavioural mechanisms to generate a baseline understanding of the response of freshwater turtles to changing saline environments. We also review the potential origins of salinity tolerance in freshwater turtles. Finally, we integrate 2100 sea level rise (SLR) projections, species distribution maps, literature gathered on brackish water use, and a phylogeny to predict the exposure of freshwater turtles to projected SLR globally. From our synthesis of published literature and available data, we build a framework for spatial and phylogenetic conservation prioritization of coastal freshwater turtles. Based on our literature review, 70 species (∼30% of coastal freshwater turtle species) from 10 of the 11 freshwater turtle families have been reported in brackish water ecosystems. Most anecdotal records, observations, and descriptions do not imply long‐term salinity tolerance among freshwater turtles. Rather, experiments show that some species exhibit potential for adaptation and plasticity in physiological, behavioural, and life‐history traits that enable them to endure varying periods (e.g. days or months) and levels of saltwater exposure. Species that specialize on brackish water habitats are likely to be vulnerable to SLR because of their exclusive coastal distributions and adaptations to a narrow range of salinities. Most species, however, have not been documented in brackish water habitats but may also be highly vulnerable to projected SLR. Our analysis suggests that approximately 90% of coastal freshwater turtle species assessed in our study will be affected by a 1‐m increase in global mean SLR by 2100. Most at risk are freshwater turtles found in New Guinea, Southeast Asia, Australia, and North and South America that may lose more than 10% of their present geographic range. In addition, turtle species in the families Chelidae, Emydidae, and Trionychidae may experience the greatest exposure to projected SLR in their present geographic ranges. Better understanding of survival, growth, reproductive and population‐level responses to SLR will improve region‐specific population viability predictions of freshwater turtles that are increasingly exposed to SLR. Integrating phylogenetic, physiological, and spatial frameworks to assess the effects of projected SLR may improve identification of vulnerable species, guilds, and geographic regions in need of conservation prioritization. We conclude that the use of brackish and marine environments by freshwater turtles provides clues about the evolutionary processes that have prolonged their existence, shaped their unique coastal distributions, and may prove useful in predicting their response to a changing world.

Using a Bayesian network to clarify areas requiring research in a host-pathogen system

Bayesian network analyses can be used to interactively change the strength of effect of variables in a model to explore complex relationships in new ways. In doing so, they allow one to identify influential nodes that are not well studied empirically so that future research can be prioritized. We identified relationships in host and pathogen biology to examine disease-driven declines of amphibians associated with amphibian chytrid fungus (Batrachochytrium dendrobatidis). We constructed a Bayesian network consisting of behavioral, genetic, physiological, and environmental variables that influence disease and used them to predict host population trends. We varied the impacts of specific variables in the model to reveal factors with the most influence on host population trend. The behavior of the nodes (the way in which the variables probabilistically responded to changes in states of the parents, which are the nodes or variables that directly influenced them in the graphical model) was consistent with published results. The frog population had a 49% probability of decline when all states were set at their original values, and this probability increased when body temperatures were cold, the immune system was not suppressing infection, and the ambient environment was conducive to growth of B. dendrobatidis. These findings suggest the construction of our model reflected the complex relationships characteristic of host-pathogen interactions. Changes to climatic variables alone did not strongly influence the probability of population decline, which suggests that climate interacts with other factors such as the capacity of the frog immune system to suppress disease. Changes to the adaptive immune system and disease reservoirs had a large effect on the population trend, but there was little empirical information available for model construction. Our model inputs can be used as a base to examine other systems, and our results show that such analyses are useful tools for reviewing existing literature, identifying links poorly supported by evidence, and understanding complexities in emerging infectious-disease systems.