Natural disturbance reduces disease risk in endangered rainforest frog populations

Natural disturbances can drive disease dynamics in animal populations by altering the microclimates experienced by hosts and their pathogens. Many pathogens are highly sensitive to temperature and moisture, and therefore small changes in habitat structure can alter the microclimate in ways that increase or decrease infection prevalence and intensity in host populations. Here we show that a reduction of rainforest canopy cover caused by a severe tropical cyclone decreased the risk of endangered rainforest frogs (Litoria rheocola) becoming infected by a fungal pathogen (Batrachochytrium dendrobatidis). Reductions in canopy cover increased the temperatures and rates of evaporative water loss in frog microhabitats, which reduced B. dendrobatidis infection risk in frogs by an average of 11–28% in cyclone-damaged areas, relative to una ected areas. Natural disturbances to the rainforest canopy can therefore provide an immediate bene t to frogs by altering the microclimate in ways that reduce infection risk. This could increase host survival and reduce the probability of epidemic disease outbreaks. For amphibian populations under immediate threat from this pathogen, targeted manipulation of canopy cover could increase the availability of warmer, drier microclimates and therefore tip the balance from host extinction to coexistence

Robust calling performance in frogs infected by a deadly fungal pathogen

Reproduction is an energetically costly behavior for many organisms, including species with mating systems in which males call to attract females. In these species, calling males can often attract more females by displaying more often, with higher intensity, or at certain frequencies. Male frogs attract females almost exclusively by calling, and we know little about how pathogens, including the globally devastating fungus, Batrachochytrium dendrobatidis, influence calling effort and call traits. A previous study demonstrated that the nightly probability of calling by male treefrogs, Litoria rheocola, is elevated when they are in good body condition and are infected by B. dendrobatidis. This suggests that infections may cause males to increase their present investment in mate attraction to compensate for potential decreases in future reproduction. However, if infection by B. dendrobatidis decreases the attractiveness of their calls, infected males might experience decreased reproductive success despite increases in calling effort. We examined whether calls emitted by L. rheocola infected by B. dendrobatidis differed from those of uninfected individuals in duration, pulse rate, dominant frequency, call rate, or intercall interval, the attributes commonly linked to mate choice. We found no effects of fungal infection status or infection intensity on any call attribute. Our results indicate that infected males produce calls similar in all the qualities we measured to those of uninfected males. It is therefore likely that the calls of infected and uninfected males should be equally attractive to females. The increased nightly probability of calling previously demonstrated for infected males in good condition may therefore lead to greater reproductive success than that of uninfected males. This could reduce the effectiveness of natural selection for resistance to infection, but could increase the effectiveness of selection for infection tolerance, the ability to limit the harm caused by infection, such as reductions in body condition

Predicting the growth of the amphibian chytrid fungus in varying temperature environments

Environmental temperature is a crucial abiotic factor that influences the success of ectothermic organisms, including hosts and pathogens in disease systems. One example is the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), which has led to widespread amphibian population declines. Understanding its thermal ecology is essential to effectively predict outbreaks. Studies that examine the impact of temperature on hosts and pathogens often do so in controlled constant temperatures. Although varying temperature experiments are becoming increasingly common, it is unrealistic to test every temperature scenario. Thus, reliable methods that use constant temperature data to predict performance in varying temperatures are needed. In this study, we tested whether we could accurately predict Bd growth in three varying temperature regimes, using a Bayesian hierarchical model fit with constant temperature Bd growth data. We fit the Bayesian hierarchical model five times, each time changing the thermal performance curve (TPC) used to constrain the logistic growth rate to determine how TPCs influence the predictions. We then validated the model predictions using Bd growth data collected from the three tested varying temperature regimes. Although all TPCs overpredicted Bd growth in the varying temperature regimes, some functional forms performed better than others. Varying temperature impacts on disease systems are still not well understood and improving our understanding and methodologies to predict these effects could provide insights into disease systems and help conservation efforts

Hydric Balance and Locomotor Performance of Native and Invasive Frogs

An animal's physiology should be closely adapted to its environment to optimize organismal function, so physiological traits may be mismatched when animals are introduced to new locations. For introduced amphibians, mismatched traits involving hydric balance or performance across hydric states could have profound impacts on their abundance and distribution, and thus their invasion success. We examined susceptibility to dehydration in invasive Cuban treefrogs (Osteopilus septentrionalis) and two sympatric native treefrogs (Hyla spp.) in Florida, USA, by measuring rates of evaporative water loss, rates of water uptake, and sensitivity of locomotor performance to dehydration. Of the three species, Cuban treefrogs were the most susceptible to dehydration by experiencing the highest rate of evaporative water loss and lowest rate of water uptake. Green treefrogs (Hyla cinerea) were the most resistant to dehydration by losing water the slowest and gaining water the fastest, and squirrel treefrogs (Hyla squirella) were intermediate in rates of water loss and uptake. Dehydrating frogs by 20% of their fully hydrated body masses affected the locomotor performance of all species by decreasing maximum jump lengths, decreasing speed, and increasing successive jump lengths. The maximum jump lengths of Cuban treefrogs and green treefrogs were more sensitive to dehydration than those of squirrel treefrogs. Despite this sensitivity, Cuban treefrogs still outperformed both native species in maximum jump length and speed, even when controlling for body size. Consequently, the performance of dehydrated Cuban treefrogs was similar to that of fully hydrated native treefrogs. Our results suggest that Cuban treefrogs are more susceptible to dehydration and its effects than several native competitors; however, they may be able to at least partly compensate for these effects with their large body size, superior locomotor performance, and strong affinity for refugia. Our findings highlight different strategies used by frogs to maintain water balance and suggest that Cuban treefrog densities may be higher in areas with greater moisture availability and habitat complexity, including urban and densely forested areas. Native treefrogs may experience stronger competition and predation from Cuban treefrogs in these areas, which supports anecdotal reports of native frog declines

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 ~4 °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

Effects of individual behaviour on host-pathogen interactions: Australian rainforest frogs and the chytrid fungus Batrachochytrium dendrobatidis

Diseases are strongly influenced by host behaviour, which affects pathogen transmission and the microclimatic conditions that are experienced by both hosts and pathogens. The amphibian disease chytridiomycosis, which is caused by the chytrid fungus Batrachochytrium dendrobatidis, has caused severe population declines in many regions of the world. This pathogen is transmitted by contact with water and is highly sensitive to thermal and hydric conditions; it requires relatively cool, moist conditions to survive and reproduce (15-25°C optimal, >28°C lethal). This thesis focuses on the behaviour of stream-breeding frogs that occur in tropical rainforests of northeastern Australia. This thesis demonstrates that the behaviour of individual frogs plays an important role in this host-pathogen system. Patterns of microenvironment use, microhabitat use, and movement by individual hosts can affect their interactions with the pathogen. Frogs that used cooler, moister microenvironments were more likely to be infected than frogs that experienced warmer, drier conditions, likely as a result of differences in rates of pathogen transmission and growth rates associated with these microenvironments. Differences in the microenvironments experienced by infected and uninfected frogs are caused by their patterns of movement and microhabitat use. Laboratory experiments revealed that B. dendrobatidis infections can change the behaviour of some, but not all, species. This suggests that in some species, behavioural differences between infected and uninfected frogs reflect effects of innate behaviour on the probability of acquiring or retaining infections, but in other species, such differences can be caused by changes in the behaviour of infected frogs.\ud \ud This thesis also provides the first demonstration that B. dendrobatidis infections can have sublethal effects that interact with male body condition to influence calling probability, a major fitness determinant in frogs. These effects involve complex, potentially adaptive tradeoffs; infected frogs in poor body condition were less likely to call than uninfected frogs in similar condition, but infected frogs in good condition often had a higher probability of calling than uninfected frogs. These effects should influence fitness and may serve to maximise the lifetime reproductive success of infected frogs. Finally, this thesis demonstrates the important role of habitat heterogeneity in reducing the impact of B. dendrobatidis. A severe tropical cyclone dramatically reduced rainforest canopy cover at some study sites, which increased temperatures and decreased moisture levels in frog microhabitats. These microclimatic changes reduced infection risk in frogs, presumably by slowing pathogen growth rates. The effects of this natural experiment suggest that targeted manipulations of canopy cover may reduce the intensity of epidemic outbreaks of chytridiomycosis. Overall, this thesis highlights the importance of individual behaviour in this host-pathogen system, and the complexity of the relationships between B. dendrobatidis and different host species. This thesis also demonstrates that B. dendrobatidis infection dynamics are strongly driven by environmental conditions, and that habitat characteristics play an important role in influencing the conditions available to individual amphibians

Does waterproofing Thermochron iButton dataloggers influence temperature readings?

Miniature Thermochron iButton dataloggers have transformed the ways in which researchers collect thermal data. However, one important limitation is that these dataloggers are not waterproof, which can lead to device failure and loss of data under field conditions. Several methods have been used to increase their water resistance, but no study to date has investigated whether any of these techniques affects the accuracy of temperature readings. Waterproofing potentially could affect the accuracy of iButtons by biasing temperatures or altering rates of warming and cooling. We compared temperature profiles of unmodified Thermochron iButtons (model DS1921G) to iButtons that we coated with a clear plastic dip (designed to coat tool handles) to determine whether this waterproof coating affects the accuracy of temperatures they record. We also compared temperatures recorded by uncoated and coated iButtons that were embedded within physical models that mimic frog body temperatures. Finally, we used our field data to test whether coating iButtons with plastic prevents failure of dataloggers during fieldwork. Although we found statistically significant differences between the temperatures recorded by uncoated and coated iButtons, and also between uncoated and coated iButtons embedded in frog models, these effects were relatively small (0–1.3 °C). We also found that coating iButtons with plastic reduced the likelihood of device failure under field conditions (from 8.3% to 0%). We conclude that coating Thermochron iButtons with plastic is an affordable and reliable method of waterproofing dataloggers that prevents device failure and data loss with minimal influence on temperature readings

Using pairs of physiological models to estimate temporal variation in amphibian body temperature

Physical models are often used to estimate ectotherm body temperatures, but designing accurate models for amphibians is difficult because they can vary in cutaneous resistance to evaporative water loss. To account for this variability, a recently published technique requires a pair of agar models that mimic amphibians with 0% and 100% resistance to evaporative water loss; the temperatures of these models define the lower and upper boundaries of possible amphibian body temperatures for the location in which they are placed. The goal of our study was to develop a method for using these pairs of models to estimate parameters describing the distributions of body temperatures of frogs under field conditions. We radiotracked green-eyed treefrogs (Litoria serrata) and collected semi continuous thermal data using both temperature sensitive radiotransmitters with an automated datalogging receiver, and pairs of agar models placed in frog locations, and we collected discrete thermal data using a noncontact infrared thermometer when frogs were located. We first examined the accuracy of temperature-sensitive transmitters in estimating frog body temperatures by comparing transmitter data with direct temperature measurements taken simultaneously for the same individuals We then compared parameters (mean, minimum, maximum, standard deviation) characterizing the distributions of temperatures of individual frogs estimated from data collected using each of the three methods. We found strong relationships between thermal parameters estimated from data collected using automated radio-telemetry and both types of thermal models. These relationships were stronger for data collected using automated radiotelemetry and impermeable thermal models, suggesting that in the field, L. serrata has relatively high resistance to evaporative water loss.Our results demonstrate that placing pairs of thermal models in frog locations can provide accurate estimates of the disributions of temperatures experienced by individual frogs, and that comparing temperatures from mode lpairs to direct measurements collected simultaneously on frogs can be used to broadly characterize the skin resistance of a species ,and to select which model type is most appropriate for estimating temperature distributions for that species

Seasonal ecology and behavior of an endangered rainforest frog (Litoria rheocola) threatened by disease

One of the most devastating wildlife diseases ever recorded is chytridiomycosis, a recently emerged amphibian disease that is caused by the chytrid fungus Batrachochytrium dendrobatidis. Understanding, predicting, and managing the impacts of chytridiomycosis on any amphibian species will require detailed information on its ecology and behavior because this pathogen is transmitted by contact with water or other individuals, and pathogen growth rates are thermally sensitive. The common mistfrog (Litoria rheocola) is an endangered tropical rainforest frog that has declined due to chytridiomycosis. We tracked L. rheocola during the winter (cool/dry) and summer (warm/wet) seasons at a low- and high-elevation site. We found that seasonal differences in environmental temperatures and frog behavior should render this species most vulnerable to B. dendrobatidis during cooler months and at higher elevations, which matches observed patterns of infection prevalence in this species. During winter, frogs moved shorter distances than during summer, and they spent less time in vegetation and more time in the stream, which should increase exposure to aquatic B. dendrobatidis zoospores. At a low-elevation site (40 m ASL), estimated body temperatures were within the optimal range for B. dendrobatidis growth (15-25°C) most of the time during winter, but they reached temperatures above this threshold frequently in summer. At a higher elevation (750 m ASL), estimated body temperatures were within the range most favorable for B. dendrobatidis year-round, and did not exceed 25°C, even during summer. Our study provides the first detailed information on the ecology and behavior of L. rheocola and suggests ecological mechanisms for infection dynamics that have been observed in this endangered species