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

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

Home range and habitat selection in the eastern box turtle (Terrepene carolina carolina) in a longleaf pine\ud (Pinus palustris) reserve

The Eastern Box Turtle (Terrapene carolina) is a species of conservation concern throughout North America, with recent population declines attributed primarily to habitat loss. The habitat requirements of this species in the southeastern United States have not been fully described. Our objectives were to estimate home range size and to describe habitat selection of Eastern Box Turtles (subspecies T. c. carolina) in a landscape dominated by Longleaf Pine (Pin us palustris) forest, the once dominant ecosystem in the Southeastern Coastal Plain. We conducted a radio-telemetry study of adult Eastern Box Turtles in a managed Longleaf Pine reserve in southwestern Georgia, USA. Home ranges expressed as 95% minimum convex polygons were 0.33-54.37 ha in size and averaged 10.33 +/- 3.33 ha (SE). Turtles exhibited landscape-scale selection of pine-hardwood forests and hardwood forests. At a local scale, turtles used forbs more than bare ground, litter, and grass. Our study provides much-needed baseline information about home range size and habitat use of Eastern Box Turtles in the endangered Longleaf Pine ecosystem. Additional studies, particularly regarding use of disturbed habitats that are more characteristic of the modern southeastern landscape, would further clarify the status of Eastern Box Turtles in this region

Home range and habitat selection in the eastern box turtle (Terrepene carolina carolina) in a longleaf pine (Pinus palustris) reserve

The Eastern Box Turtle (Terrapene carolina) is a species of conservation concern throughout North America, with recent population declines attributed primarily to habitat loss. The habitat requirements of this species in the southeastern United States have not been fully described. Our objectives were to estimate home range size and to describe habitat selection of Eastern Box Turtles (subspecies T. c. carolina) in a landscape dominated by Longleaf Pine (Pin us palustris) forest, the once dominant ecosystem in the Southeastern Coastal Plain. We conducted a radio-telemetry study of adult Eastern Box Turtles in a managed Longleaf Pine reserve in southwestern Georgia, USA. Home ranges expressed as 95% minimum convex polygons were 0.33-54.37 ha in size and averaged 10.33 +/- 3.33 ha (SE). Turtles exhibited landscape-scale selection of pine-hardwood forests and hardwood forests. At a local scale, turtles used forbs more than bare ground, litter, and grass. Our study provides much-needed baseline information about home range size and habitat use of Eastern Box Turtles in the endangered Longleaf Pine ecosystem. Additional studies, particularly regarding use of disturbed habitats that are more characteristic of the modern southeastern landscape, would further clarify the status of Eastern Box Turtles in this region

Host thermoregulatory constraints predict growth of an amphibian chytrid pathogen (Batrachochytrium dendrobatidis)

1. The course and outcome of many wildlife diseases are context-dependent, and therefore change depending on the behaviour of hosts and environmental response of the pathogen. 2. Contemporary declines in amphibian populations are widely attributed to chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis. Despite the thermal sensitivity of the pathogen and its amphibian hosts, we do not understand how host thermal regimes experienced by frogs in the wild directly influence pathogen growth. 3. We tested how thermal regimes experienced by the rainforest frog Litoria rheocola in the wild influence pathogen growth in the laboratory, and whether these responses differ from pathogen growth under available environmental thermal regimes. 4. Frog thermal regimes mimicked in the laboratory accelerated pathogen growth during conditions representative of winter at high elevations more so than if temperatures matched air or stream water temperatures. By contrast, winter frog thermal regimes at low elevations slowed pathogen growth relative to air temperatures, but not water temperatures. 5. The growth pattern of the fungus under frog thermal regimes matches field prevalence and intensity of infections for this species (high elevation winter > high elevation summer > low elevation winter > low elevation summer), whereas pathogen growth trajectories under environmental temperatures did not match these patterns. 6. If these laboratory results translate into field responses, tropical frogs may be able to reduce disease impacts by regulating their body temperatures to limit pathogen growth (e.g., by using microhabitats that facilitate basking to reach high temperatures); in other cases, the environment may limit the ability of frogs to thermoregulate such that individuals are more vulnerable to this pathogen (e.g., in dense forests at high elevations). 7. Species-specific thermoregulatory behaviour, and interactions with and constraints imposed by the environment, are therefore essential to understanding and predicting the spatial and temporal impacts of this global disease

White blood cell profiles in amphibians help to explain disease susceptibility following temperature shifts

Temperature variability, and in particular temperature decreases, can increase susceptibility of amphibians to infections by the fungus Batrachochytrium dendrobatidis (Bd). However, the effects of temperature shifts on the immune systems of Bd-infected amphibians are unresolved. We acclimated frogs to 16 °C and 26 °C (baseline), simultaneously transferred them to an intermediate temperature (21 °C) and inoculated them with Bd (treatment), and tracked their infection levels and white blood cell profiles over six weeks. Average weekly infection loads were consistently higher in 26°C-history frogs, a group that experienced a 5 °C temperature decrease, than in 16°C-history frogs, a group that experienced a 5 °C temperature increase, but this pattern only approached statistical significance. The 16°C-acclimated frogs had high neutrophil:lymphocyte (N:L) ratios (suggestive of a hematopoietic stress response) at baseline, which were conserved post-treatment. In contrast, the 26°C-acclimated frogs had low N:L ratios at baseline which reversed to high N:L ratios post-treatment (suggestive of immune system activation). Our results suggest that infections were less physiologically taxing for the 16°C-history frogs than the 26°C-history frogs because they had already adjusted immune parameters in response to challenging conditions (cold). Our findings provide a possible mechanistic explanation for observations that amphibians are more susceptible to Bd infection following temperature decreases compared to increases and underscore the consensus that increased temperature variability associated with climate change may increase the impact of infectious diseases

Low-cost fluctuating-temperature chamber for experimental ecology

Commercially available fluctuating-temperature chambers are large and costly. This poses a challenge to experimental ecologists endeavouring to recreate natural temperature cycles in the laboratory because the large number of commercial chambers required for replicated study designs is prohibitively expensive to purchase, requires a large amount of space and consumes a great deal of energy. We developed and validated a design for economical, programmable fluctuating-temperature chambers based on a relatively small (23 L) commercially manufactured constant temperature chamber ($140US) modified with a customized, user-friendly microcontroller ($15US). Over a 1-week trial, these chambers reliably reproduced a real-world fluctuating (13·1–35·5 °C) body temperature regime of an individual frog, with a near-perfect 1 : 1 fit between target and actual temperatures (y = 1·0036x + 0·1366, R2 = 0·9977, 95% confidence interval for slope = 1·0026, 1·0046). Over 30-day trials, they also reliably produced a simpler daily fluctuating-temperature scheme (sine wave fluctuating between 10 and 25 °C each 24 h) and a range of constant temperature regimes. The design is inexpensive and simple to assemble in large numbers, enabling genuine replication of even highly complex, many treatment study designs. For example, it is possible to simultaneously examine in replicate chambers the responses of organisms to constant regimes, regimes that fluctuate following the means experienced by populations and regimes that exactly mimic fluctuations measured over any length of time for particular individuals that differ in behaviour or microhabitat use. These chambers thus vastly expand the pool of resources available for manipulative experiments in thermal biology and ecology

Low-cost fluctuating-temperature chamber for experimental ecology

Commercially available fluctuating-temperature chambers are large and costly. This poses a challenge to experimental ecologists endeavouring to recreate natural temperature cycles in the laboratory because the large number of commercial chambers required for replicated study designs is prohibitively expensive to purchase, requires a large amount of space and consumes a great deal of energy. We developed and validated a design for economical, programmable fluctuating-temperature chambers based on a relatively small (23 L) commercially manufactured constant temperature chamber ($140US) modified with a customized, user-friendly microcontroller ($15US). Over a 1-week trial, these chambers reliably reproduced a real-world fluctuating (13·1–35·5 °C) body temperature regime of an individual frog, with a near-perfect 1 : 1 fit between target and actual temperatures (y = 1·0036x + 0·1366, R2 = 0·9977, 95% confidence interval for slope = 1·0026, 1·0046). Over 30-day trials, they also reliably produced a simpler daily fluctuating-temperature scheme (sine wave fluctuating between 10 and 25 °C each 24 h) and a range of constant temperature regimes. The design is inexpensive and simple to assemble in large numbers, enabling genuine replication of even highly complex, many treatment study designs. For example, it is possible to simultaneously examine in replicate chambers the responses of organisms to constant regimes, regimes that fluctuate following the means experienced by populations and regimes that exactly mimic fluctuations measured over any length of time for particular individuals that differ in behaviour or microhabitat use. These chambers thus vastly expand the pool of resources available for manipulative experiments in thermal biology and ecology

White blood cell profiles in amphibians help to explain disease susceptibility following temperature shifts

Temperature variability, and in particular temperature decreases, can increase susceptibility of amphibians to infections by the fungus Batrachochytrium dendrobatidis (Bd). However, the effects of temperature shifts on the immune systems of Bd-infected amphibians are unresolved. We acclimated frogs to 16 degrees C and 26 degrees C (baseline), simultaneously transferred them to an intermediate temperature (21 degrees C) and inoculated them with Bd (treatment), and tracked their infection levels and white blood cell profiles over six weeks. Average weekly infection loads were consistently higher in 26 degrees C-history frogs, a group that experienced a 5 degrees C temperature decrease, than in 16 degrees C-history frogs, a group that experienced a 5 degrees C temperature increase, but this pattern only approached statistical significance. The 16 degrees C-acclimated frogs had high neutrophil:lymphocyte (N:L) ratios (suggestive of a hematopoietic stress response) at baseline, which were conserved post-treatment. In contrast, the 26 degrees C-acclimated frogs had low N:L ratios at baseline which reversed to high N:L ratios post-treatment (suggestive of immune system activation). Our results suggest that infections were less physiologically taxing for the 16 degrees C-history frogs than the 26 degrees C-history frogs because they had already adjusted immune parameters in response to challenging conditions (cold). Our findings provide a possible mechanistic explanation for observations that amphibians are more susceptible to Bd infection following temperature decreases compared to increases and underscore the consensus that increased temperature variability associated with climate change may increase the impact of infectious diseases. (C) 2017 Elsevier Ltd. All rights reserved

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

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