Synergistic effects of warming and disease linked to high mortality in cool-adapted terrestrial frogs

Neely, Wesley J.; Greenspan, Sasha E.; Ribeiro, Luisa P.; Carvalho, Tamilie; Martins, Renato Augusto; Rodríguez, David; Rohr, Jason R.; Haddad, Célio F. B.; Toledo, Luı́s Felipe; Becker, C. Guilherme

doi:10.1016/j.biocon.2020.108521

Cited by 20 publications

(25 citation statements)

References 66 publications

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“…One likely explanation for why our results and those of Neely et al (2020) did not fully support the thermal mismatch hypothesis is that we did not produce enough thermal variation in our experimental design. The difference between the highest and lowest amphibian temperature measured in our experiment was 9.3°C and the difference between the highest and lowest environmental temperature in Neely et al (2020) was 10 C; most of the amphibian species used in Cohen et al (2017) experienced an 18°C difference between the lowest and highest experimental temperature. If an increase in the warm treatment were to cause an increase in Bd infection abundance (or Bd ‐induced mortality) in the cool‐tolerant striped salamanders, our results would fully support the thermal mismatch hypothesis.…”

Section: Discussioncontrasting

confidence: 88%

“…Instead of supporting the thermal mismatch hypothesis, this particular finding corroborates previous work demonstrating that Bd does not grow well in warm temperatures (Piotrowski et al, 2004; Voyles et al, 2012) and that striped salamanders are more resistant to Bd than unstriped salamanders (Venesky et al, 2015). Recently, Neely et al (2020) tested the thermal mismatch hypothesis using Bd and host species of tropical frogs that have different thermal tolerances. Although their patterns of Bd ‐induced mortality were consistent with those of the thermal mismatch hypothesis, all three species had lower Bd infections when exposed at warm experimental temperatures compared with cool experimental temperatures (Neely et al, 2020), a result that was consistent with our infection data.…”

Section: Discussionmentioning

confidence: 99%

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Does the thermal mismatch hypothesis predict disease outcomes in different morphs of a terrestrial salamander?

et al. 2022

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Many aspects of ectotherm physiology are temperature‐dependent. The immune system of temperate‐dwelling ectothermic host species is no exception and their immune function is often downregulated in cold temperatures. Likewise, species of ectothermic pathogens experience temperature‐mediated effects on rates of transmission and/or virulence. Although seemingly straightforward, predicting the outcomes of ectothermic host−pathogen interactions is quite challenging. A recent hypothesis termed the thermal mismatch hypothesis posits that cool‐adapted host species should be most susceptible to pathogen infection during warm temperature periods whereas warm‐adapted host species should be most susceptible to pathogens during periods of cool temperatures. We explore this hypothesis using two ecologically and physiologically differentiated color morphs of the Eastern Red‐backed Salamander (Plethodon cinereus) and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis; hereafter “Bd”) using a fully factorial laboratory experiment. At cool temperatures, unstriped salamanders (i.e., those that are tolerant of warm temperatures) had a significantly higher probability of Bd infection compared with cool‐tolerant striped salamanders, consistent with the thermal mismatch hypothesis. However, we found no support for this hypothesis when salamanders were exposed to Bd at warm temperatures: the probability of Bd infection in the cool‐tolerant striped salamanders was nearly identical in both cool and warm temperatures, opposite the predictions of the thermal mismatch hypothesis. Our results are most consistent with the fact that Bd grows poorly at warm temperatures. Alternatively, our data could indicate that the two color morphs do not differ in their tolerance to warm temperatures but that striped salamanders are more tolerant to cool temperatures than unstriped salamanders.

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Section: Discussioncontrasting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Does the thermal mismatch hypothesis predict disease outcomes in different morphs of a terrestrial salamander?

et al. 2022

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“…It is important to note that higher temperatures do not always confer a benefit against Bd infection. Cool adapted and montane animals often have higher mortality due to Bd infection at warmer temperatures (Neely et al ., 2020; Sauer et al ., 2020).…”

Section: Environmental Factorsmentioning

confidence: 99%

Mechanisms underlying host persistence following amphibian disease emergence determine appropriate management strategies

et al. 2020

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Emerging infectious diseases have caused many species declines, changes in communities and even extinctions. There are also many species that persist following devastating declines due to disease. The broad mechanisms that enable host persistence following declines include evolution of resistance or tolerance, changes in immunity and behaviour, compensatory recruitment, pathogen attenuation, environmental refugia, density-dependent transmission and changes in community composition. Here we examine the case of chytridiomycosis, the most important wildlife disease of the past century. We review the full breadth of mechanisms allowing host persistence, and synthesise research on host, pathogen, environmental and community factors driving persistence following chytridiomycosis-related declines and overview the current evidence and the information required to support each mechanism. We found that for most species the mechanisms facilitating persistence have not been identified. We illustrate how the mechanisms that drive long-term host population dynamics determine the most effective conservation management strategies. Therefore, understanding mechanisms of host persistence is important because many species continue to be threatened by disease, some of which will require intervention. The conceptual framework we describe is broadly applicable to other novel disease systems.

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“…The thermal mismatch hypothesis predicts that climate warming will threaten cool‐adapted hosts during warmer periods (Cohen et al., 2017), as parasites typically have broader thermal limits than hosts and therefore are better at coping with warming (Rohr et al., 2018). Results from a study on cool‐adapted frogs in Brazil indicate that the interaction of warmer temperature and Bd‐infection may lead to population declines in the endemic Ischnocnema parva (Neely et al., 2020). Recent findings also indicate that Bd‐infected amphibians have reduced weight (Cheatsazan et al., 2013; Meurling, 2019), lower diversity of skin microbiota (Bletz et al., 2017), and directional selection on MHC molecules resisting Bd, likely making infected populations vulnerable to other novel pathogens due to lower genetic variance (Kosch et al., 2016).…”

Section: Discussionmentioning

confidence: 99%

The first detection of the fungal pathogen batrachochytrium dendrobatidis in Norway with no evidence of population declines for great crested and smooth newts based on modeling on traditional trapping data

et al. 2021

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Amphibian species are in decline throughout the world, where the stressors are numerous and comprise factors such as habitat destruction, climate change, and invasive species (Catenazzi, 2015).The invasive fungal pathogen Batrachochytrium dendrobatidis (hereafter referred to as Bd) has received considerable attention for being one of the key drivers of amphibian population declines worldwide since the 1970s, causing the infectious skin disease chytridiomycosis (Berger et al., 1998;Scheele et al., 2019). Not all amphibians respond equally to infection, and host responses range from resistant via tolerable to susceptible, where the clinical outcome depends on the host species, the Bd strain, and other environmental determinants (Van Rooij et al., 2015).

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Synergistic effects of warming and disease linked to high mortality in cool-adapted terrestrial frogs

Cited by 20 publications

References 66 publications

Does the thermal mismatch hypothesis predict disease outcomes in different morphs of a terrestrial salamander?

Does the thermal mismatch hypothesis predict disease outcomes in different morphs of a terrestrial salamander?

Mechanisms underlying host persistence following amphibian disease emergence determine appropriate management strategies

The first detection of the fungal pathogen batrachochytrium dendrobatidis in Norway with no evidence of population declines for great crested and smooth newts based on modeling on traditional trapping data

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