Amphibian survival compromised by long-term effects of chytrid fungus

Abstract

Chytridiomycosis, the disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has been unambiguously implicated in the decline of amphibian populations worldwide. However, the impact of this devastating infectious disease can be difficult to gauge without empirical data on the population-level effects of Bd. Often, assessments of the amphibian chytridiomycosis panzootic are based primarily on expert opinions; as a result, declines in tropical areas are promptly attributed to Bd while its impact on temperate species not suffering from adult mass mortalities is frequently overlooked. Here, we investigated the survival probability in an amphibian species from a temperate area that until now has not been considered to be severely impacted by the disease. Specifically, we related individual survival to Bd infection status using long-term capture-mark-recapture data of male spiny common toads (Bufo spinosus) in Sierra de Guadarrama National Park in central Spain. Even though the study population has demonstrated potential for adaptation to Bd and die-offs of adult individuals have not been recorded, our results clearly indicated that the probability of survival was lower for Bd-positive individuals. Moreover, the probability of becoming Bd-positive was higher than the probability of clearance, driving the population to a slow but certain decline. These results are consistent with other indicators of a negative population trend and suggest that the impact of Bd on temperate species of less concern may be greater than previously thought.

Drivers of Batrachochytrium dendrobatidis infection load, with evidence of infection tolerance in adult male toads (Bufo spinosus)

“…For example, if a host is infected with a parasite that negatively impacts its survival or is chronic, current reproductive effort can increase, because future reproductive opportunities may be compromised (Roznik et al 2015 , Valenzuela-Sanchez et al 2021 , 2022 ). In our data, we may see this effect with individuals having increased their reproductive effort (in this case expressed by their body condition and the time they stay in water for reproduction) in response to an elevated infection burden, potentially at the cost of reduced survival post-breeding (Palomar et al 2023 ). Previous research on bufonid species suggests that males with higher body condition may maintain higher volumes of sperm and higher fertilisation rates than individuals of lower initial condition (Hettyey et al 2009 ), and may also more likely to pair with females rather than participate in breeding balls or remain single (Gastón and Vaira 2020 ).…”

“…Despite this initial response, and the absence of die-offs of adult individuals, long-term negative effects of Bd have been recorded; clutch counts of B. spinosus have declined in the years between 1999 and 2016 in this study population (Bosch et al 2014 , 2018 ) and inconspicuous mass mortalities of recent metamorphosed individuals continues year to year from 1999 (Bosch et al unpublished results) in this study population. This decline may be underpinned not only by mass mortalities of toadlets, but also by infected adult individuals having a lower survival probability, and the probability of becoming infected being higher than that of clearance of infection (Palomar et al 2023 ). Combined data suggest that even in the absence of noticeable mass die-offs, there is a long-term decline in this species in response to Bd exposure and infection.…”

Climatic drivers of chytrid prevalence in the critically endangered Admirable Redbelly Toad

“…As Bd infection depends on interaction between the thermal performance of the pathogen and the host (Cohen et al 2017), even at low infection level, the synergistic effects of warming and Bd could result in host mortality in cool-adapted anurans (Neely et al 2020). This implies that the combined effects of Bd infection and climate change, mainly temperature anomalies, might be underestimated, as Bd affect the amphibian persistence even with low prevalence and infection loads (Valenzuela-Sánchez et al 2017; Palomar et al 2023). This highlights the signi cance of population-level impacts of Bd (Valenzuela-Sánchez et al 2017) that may potentially lead to slow and steady long-term declines.…”

“…Furthermore, the capture-mark-recapture analysis showed that although the Admirable Redbelly Toads demonstrated the ability to clear Bd infection, they still gained more infection than managed to clear over time. The probability of becoming Bd + higher than the probability of clearance is a characteristic of population on a path of slow decline (Palomar et al 2023).…”

“…Consequently, we expect higher Bd prevalence and infection loads in period when temperature exceeds the historical average. Finally, considering sublethal effects caused by Bd infection (Valenzuela-Sánchez et al 2017; Palomar et al 2023;Wu, 2023), we expect that Bd infection status has consequences on host body condition. Combined, our goals will allow us to elucidate the disease dynamics of a critically endangered micro-endemic tropical species.…”