Date Published: April 29, 2019
Publisher: Public Library of Science
Author(s): Andrés Fernández-Loras, Luz Boyero, Francisco Correa-Araneda, Miguel Tejedo, Attila Hettyey, Jaime Bosch, Wendy C. Turner.
Climate change and infectious disease by the chytrid fungus Batrachochytrium dendrobatidis (Bd) are major drivers of amphibian extinctions, but the potential interactions of these two factors are not fully understood. Temperature is known to influence (1) the infectivity, pathogenicity and virulence of Bd; (2) host-parasite dynamics, especially when both hosts and parasites are ectothermic organisms exhibiting thermal sensitivities that may or may not differ; and (3) amphibian vulnerability to extinction depending on their heat tolerance, which may decrease with infection. Thus, in a global warming scenario, with rising temperatures and more frequent and extreme weather events, amphibians infected by Bd could be expected to be more vulnerable if temperatures approach their critical thermal maximum (CTmax). However, it is also possible that predicted high temperatures could clear the Bd infection, thus enhancing amphibian survival. We tested these hypotheses by measuring CTmax values of Bd-infected and Bd-free aquatic tadpoles and terrestrial toadlets/juveniles of the common midwife toad (Alytes obstetricans) and examining whether exposure of A. obstetricans individuals to peak temperatures reaching their CTmax clears them from Bd infection. We show that (1) Bd has a wide thermal tolerance range; (2) Bd is capable of altering the thermal physiology of A. obstetricans, which is stage-dependent, lowering CTmax in tadpoles but not in toadlets; and (3) Bd infection is not cleared after exposure of tadpoles or toadlets to CTmax. Living under climatic change with rising temperatures, the effect of Bd infection might tip the balance and lead some already threatened amphibian communities towards extinction.
Batrachochytrium dendrobatidis (Bd), a pathogenic chytrid fungus causing chytridiomycosis in many amphibians, is considered the most deadly invasive species on the planet  and a main driver behind amphibian species extinctions globally [2, 3], with profound effects on communities and ecosystems . Environmental conditions can have a large influence on Bd host-parasite dynamics [5, 6], temperature being a major factor influencing its prevalence (i.e., the proportion of infected animals) and virulence . Growth and reproductive characteristics of Bd are known to highly depend on temperature [8–10], and there is a negative correlation between temperature and Bd prevalence or pathogen load, chytrid infections often being more severe in winter or in colder areas [6, 11, 12].
We collected a total of 121 A. obstetricans specimens, both larval (80) and recently metamorphosed, toadlets (41) from two localities: Toro, at mid-altitude population (Zamora, Central Spain, geographic coordinates: 41.37 N, 5.44 W; altitude: 740 m above sea level; 80 tadpoles and 21 toadlets collected) and Acherito, a montane population (Huesca, Northern Spain, geographic coordinates: 42.88 N, 0.71 W; altitude: 1875 m above sea level; 18 tadpoles and 20 toadlets collected). Prevalence of Bd infection in larval stages is known to approach 100% during colder months at both localities [11, 45]. Animals were collected in November 2012 and May 2013 at Toro and in August 2013 at Acherito.
Our main observation that CTmax values obtained for Bd-infected tadpoles were significantly lower than those of uninfected ones supports similar results reported for the adult stage of the Australian frog Litoria spenceri . Therefore, this fungal pathogen may be capable of altering the thermal physiology of the hosts it infects, or, in a narrower sense, to lower their ability to withstand high temperatures. In a global warming scenario this could have serious conservation implications for many amphibian species, especially for tropical species, which often live close to their thermal limits [41, 48]. On the other hand, temperate amphibian species may be relatively secure from similar impacts of warming, since their warming tolerance (the difference between their CTmax and environmental temperatures) is higher in most cases . Because permanent ponds are in general deeper and cooler than shallow ephemeral water bodies, A. obstetricans and many other species using permanent ponds as their larval habitat could be on the safe side in this respect, while species spawning and developing in temporary water bodies may be exposed to higher risk. Nonetheless, amphibians of the temperate zone may also be highly vulnerable to climate change, because temperatures are predicted to rise more steeply in these regions , and, coupled with the observation of Bd-infection lowering CTmax, the presence of the chytrid fungus may push local populations towards extinction. However, we have to note that the decrease in CTmax accountable to Bd-infection was less than 0.5°C for tadpoles and a similar effect could not be detected in toadlets, while CTmax was still higher than 37°C in infected tadpoles and even higher in toadlets. Thus, our results indicate that Bd-infection may lower upper thermal tolerance limits of amphibians, but this decrease is minimal in A. obstetricans and will have to be assessed in a variety of other species before we can determine the importance of this effect.