The modifications resulting from the expansion of human populations have led to an increased frequency and intensity of climatic extremes (Seneviratne et al., 2021). Rainfall and temperature patterns have globally shifted in response to global warming, and climatic anomalies are projected to increase in frequency and intensity (Seneviratne et al., 2021). Climatic anomalies can alter entire ecosystems, extending their impact also over wildlife disease dynamics (Greenspan et al., 2020; Rohr and Raffel, 2010). This intricate interplay occurs through a wide range of mechanisms, encompassing shifts in pathogen development (Nnadi and Carter, 2021), and alterations in host behavior and physiological traits (Bozinovic and Pörtner, 2015) that often lead to increased susceptibility to diseases (Bradley et al., 2019).

Wildlife disease dynamics are influenced by micro and macro-climatic variables often involving synergistic interactions between pathogens and their hosts (Altizer et al., 2013). Chytridiomycosis is among the most devastating wildlife diseases, driving amphibian population declines worldwide and causing catastrophic, ongoing biodiversity losses (Scheele et al., 2019). Caused by the waterborne fungal pathogen Batrachochytrium dendrobatidis (hereafter Bd), chytridiomycosis dynamics is influenced by climatic variables (Ruggeri et al., 2018). Climatic extremes, such as deficit in rainfall, can intensify seasonal pathogen amplification and trigger localized pathogen clusters (e.g., Moura-Campos et al., 2021), consequently, increasing host disease susceptibility. Simultaneously, these extremes have been linked to significant declines in amphibian populations by increasing desiccating breeding sites and causing recruitment failure (Scheele et al., 2012). Consequently, accelerated climate variability could synergistically intensify these impacts and drive amphibians to the extinction path, as amphibians are already the most threatened vertebrate taxon (IUCN, 2023). The Bd-amphibian system thus provides an opportunity to investigate the impact of climate anomalies on disease dynamics in formally threatened species, such as Admirable Redbelly Toad, Melanophryniscus admirabilis (Bufonidae), from southern Brazil, a region with widespread occurrence of Bd. This microendemic Neotropical species (range size of 1.6 km2, IUCN, 2023) is classified as Critically Endangered (CR) by the IUCN Red List of Threatened Species (IUCN, 2023) and in the Brazilian Red List (Brasil, 2022), further highlighting the urgency of understanding and addressing the Bd infection dynamics and the intricate interplay between climate, Bd, and the conservation of this species (IUCN, 2023).

Melanophryniscus admirabilis uses temporary small pools (0.4–22 cm deep) formed on flat rock outcrops as vocalization and breeding aggregation sites. While evidence of breeding activity has been recorded in nearly every month of the year, the breeding season is concentrated from mid-August to mid-October (Abadie et al., unpublished results). Similarly, Bd depends on water for its growth, survival, and dispersion, although it can be transported by other non-amphibian vectors (e.g., Pontes et al., 2018; Prado et al., 2023). Therefore, rainfall and its anomalies could significantly impact the reproductive biology of M. admirabilis and pathogen infection dynamics (Moura-Campos et al., 2021; Ruggeri et al., 2018). Temperature also plays an important role in the reproductive success of Admirable Redbelly Toad because this species depends on the duration and availability of deepest pools (Bordignon et al., unpublished results), which can quickly evaporate under high temperatures. Additionally, despite Bd exhibiting varying thermal tolerance, temperature can induce alterations in Bd life history (Stevenson et al., 2013) and plays a major role in determining the Bd infection loads in hosts (Bielby et al., 2022). Some amphibians can demonstrate increased susceptibility to chytridiomycosis in the presence of anomalies in environmental temperatures (Cohen et al., 2019). For example, transitions from warm El Niño years to cooler La Niña triggered Bd outbreaks in a Neotropical Bufonidae toad (Rohr and Raffel, 2010), as temperature-induced stress can significantly impair the ability of hosts to mount effective innate immune defenses against Bd (Grogan et al., 2018). Hence, seasonal and historical variations in temperature and rainfall are recognized as relevant environmental variables likely influencing Bd infection dynamics in M. admirabilis.

Alternatively, the environmental context can benefit amphibians in mitigating Bd infections (Karavlan and Venesky, 2016). For instance, Bd growth is significantly suppressed at temperatures above 25 °C (Stevenson et al., 2013), thus, predicted increases in average global temperatures could suppress pathogen growth in amphibians’ skin. However, the interaction of Bd and warming could lead to an increase in mortality of cool-adapted host species at higher temperatures, despite lower infection loads (Neely et al., 2020). This suggests that even when temperatures approach the upper thermal limit of the pathogen, Bd infection may cause declines in cool-adapted toads due to the combined pressures of pathogen infection and warming-related stress (Neely et al., 2020). Specifically, Bd infection can lead to host stress, with downstream impacts on host body condition and fitness (Bosch et al., 2023). Bd infection has also been linked to population declines in wild amphibians through sublethal effects that reduce host fitness, extending beyond immediate consequences to affect long-term population dynamics and persistence (Palomar et al., 2023; Valenzuela-Sánchez et al., 2017). Understanding these broader consequences and Bd dynamics is vital for effective conservation strategies for the Critically Endangered M. admirabilis, particularly in light of its higher vulnerability to extinction due to stochastic events (Fonte et al., 2022).

Considering the importance of Bd on amphibian population declines and pivotal role of climatic variables in predicting amphibian host-pathogen dynamics, we aimed to test whether local monthly climatic fluctuations and climatic anomalies would be associated with changes in Bd dynamics in Admirable Redbelly Toad. Given the fact that our focal amphibian species depends on temporary pools to breed and that Bd is a waterborne pathogen prone to desiccation in dry, warm environments, we hypothesized that seasonal fluctuations in temperature and rainfall impact Bd dynamics. Specifically, due to the preference for reproduction and aggregation at deeper pools (Bordignon et al., unpublished results), we expect that periods with lower temperatures and high rainfall will result in higher Bd prevalence and infections load. Additionally, we hypothesized that the M. admirabilis population will experience higher Bd prevalence and infections load in periods when rainfall exceeds the historical average and when temperatures are below the historical average. Finally, considering Bd sublethal effects (Palomar et al., 2023; Valenzuela-Sánchez et al., 2017; Wu, 2023), we expect that Bd infection status has negative consequences on host body condition. Combined, our goals will allow us to elucidate the Bd dynamics of a critically endangered Neotropical species, representing the first long-term study of Bd dynamics in Admirable Redbelly Toad.

We collected 339 skin swab samples from 297 individuals, and overall Bd prevalence was 15.9 % (54/339; Table 1), and the mean infection load in Bd+ toads was 73.58 GE (± 293.36 SD), ranging from 0.1 to 2,112.45 GE (Table 1). Bd was detected in all nine field campaigns, with the lowest prevalence (1.40 %, 1/71) recorded in November 2020 (Table 1, Fig. 1) and the highest (34.78 %, 16/46) in August 2021 (Table 1, Fig. 1).

Fig. 1.

Proportion of Melanophryniscus admirabilis toads infected with Batrachochytrium dendrobatidis (Bd) and proportion of genomic equivalents of zoospores (GE) by months.

Our most parsimonious GLMM models retained two models within ΔAIC ≤ 2 for Bd prevalence and seven models for Bd infection load (Table S2). Model averaging for Bd prevalence identified temperature as the only significant negative predictor (z = 2.729, P < 0.01; Fig. 2, Table 2). Model averaging explaining Bd infection load did not identify any statistically significant predictors (Table 2).

Fig. 2.

Visualization of the Generalized Linear Model (GLM) fit for Batrachochytrium dendrobatidis (Bd) infection risk (prevalence) and temperature (ºC) (z = 2.729, P < 0.001).

Fig. 3.

Individual variation in Batrachochytrium dendrobatidis (Bd) infection loads (log genomic equivalents of zoospores, GE) in Melanophryniscus admirabilis toads (lines connect the same individual). Values below zero indicate an uninfected sample. Recapture intervals varied between individuals, with the minimum being 75 days and the maximum being 3 years and 2 months.

We did not observe a significant difference in SMI between Bd+ and Bd− toads (t-value = −0.405, df = 39.537, P = 0.687). Additionally, we did not find a significant association between SMI and infection loads of Bd+ individuals (β = 0.059, r = −0.007, P = 0.383; Fig. S3). A total of 262 toads were captured once, 29 captured twice, five captured three times, and one was captured four times. Regarding Bd infection status over time, a total of seven recaptured toads were found infected with Bd at least once (Fig. 3). Despite toads gained infection seven times, while they cleared Bd infection only three times (Fig. 3), this difference was not statistically significant (P = 0.171).

Our study revealed that Bd was consistently infecting the Admirable Redbelly Toad population across all sampling periods spanning more than three years, with some periods showing higher prevalence than the expected 20 % for the Atlantic Forest amphibians (Carvalho et al., 2017). Given that this is the only known population of M. admirabilis, the consistent Bd detection, combined with other interacting stressors, could affect population persistence.

Contrary to our predictions, only one climatic variable predicted Bd prevalence in Admirable Redbelly Toads. Our findings suggest that lower temperatures were key in predicting Bd prevalence in this species. One of the main breeding site selection criteria for M. admirabilis is pool depth and size, with deeper pools being more likely to be used as breeding sites (Bordignon et al., unpublished results). During colder periods, reduced evaporation helps maintain water levels in these pools, ensuring their availability for breeding. Peaks of explosive breeding events occur in periods with mild temperatures, and the highest recorded aggregation – over 300 toads – occurred in August (austral winter) (Abadie et al., unpublished results). Toad aggregations serve as significant reservoirs of infective Bd zoospores (Longo et al., 2010), increasing the likelihood of Bd transmission when toads interact and shed zoospores into water pools (Moura-Campos et al., 2021). Additionally, population density and contact rates among toads have also been linked with higher Bd prevalence in other Melanophryniscus species (Pontes et al., 2021). Although not measured in this study, it is possible that the higher density of toads at the ponds during breeding periods, combined with the seasonal demography of M. admirabilis, may also play a role in Bd infection dynamics in the only known population of this species. These results highlight the importance of considering both climatic and ecological factors when assessing Bd risk in amphibian populations.

Although climatic variables were not good predictors of Bd infection in M. admirabilis, the patoghen was consistently detected throughout the study period. Overall, Bd infection loads were low, – a pattern also found in Melanophryniscus montevidensis species (Pontes et al., 2021) – with the highest load coinciding with the period of prevalence peak. Additionally, even low infection levels can negatively impact bufonids, and Bd+ toads can exhibit lower survival probabilities, even in populations with some capacity to adapt to chytridiomycosis (Palomar et al., 2016, 2023). This suggests that, despite low infection loads, Bd can still impact amphibian persistence and contribute to long-term silent population declines (Palomar et al., 2023; Valenzuela-Sánchez et al., 2017). From a conservation perspective, the Admirable Redbelly Toad population may be facing not only potential impacts from Bd infection, but also multiple environmental and anthropogenic threats, including, for example, exposure to antibiotic-resistant bacteria (Ienes-Lima et al., 2023a,b), pesticide contamination from nearby tobacco crops, and competition with invasive species (IUCN, 2023).

Our findings suggest that Bd presence and infection load were not linked to host body condition. Evidence of sublethal effects of Bd on body condition is rarely observed in wild populations that do not experience chytridiomycosis-related mortality. However, it is worth noting that even at low infection loads, Bd could lead to impaired skin physiology (i.e., skin integrity, osmoregulation, and hormone production) (Wu, 2023). Additionally, Bd is known to alter the amphibian skin microbiome (Becker et al., 2019) and the presence of the bacteria Serratia marcescens could also be playing an important structural role in skin microbiome health in M. admirabilis (Ienes-Lima et al., 2023a). Furthermore, while not statistically significant, our capture-mark-recapture analysis showed that although individuals demonstrated the ability to clear Bd infection, they more often show an increase in infection likelihood rather than clearance over time. The higher probability of becoming Bd+ than the probability of clearance is a characteristic of populations on a path of slow decline (Palomar et al., 2023). Therefore, tracking individual Bd infection status over time remains essential, especially considering our limited sample size, to better understand long-term infection and support future demographic assessments of the population health.

The species within the genus Melanophryniscus could be affected by climate change in different ways, including the reduction of suitable habitats (Zank et al., 2014). This study represents the first long-term investigation into Bd infection dynamics in M. admirabilis under variable climatic conditions and contributes to the IUCN Red List Assessments by providing Bd infection data (IUCN, 2023). While chytridiomycosis may not pose an immediate threat to the Admirable Redbelly Toads, common stressors such as herbicides (da-Silva et al., 2023) and anthropogenic impact (Ienes-Lima et al., 2023b) could amplify the fitness impact of climate change (Greenspan et al., 2017). The results gained from this study underscore the importance of long-term monitoring to assess the impacts of synergistic threats on the M. admirabilis population. Future research should investigate the role of host density, seasonal demographic changes, and habitat characteristics to better understand the mechanisms driving Bd prevalence in Admirable Redbelly Toad. We advocate for the continuation of disease ecology research on the critically endangered M. admirabilis population, including Bd and other amphibian pathogens such as Ranavirus (Ruggeri et al., 2023).

This work was conducted under permits by Instituto Chico Mendes de Conservação da Biodiversidade (SISBio #72718), Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado (SisGen #A3D44D1) and approved by Unicamp animal care and ethics committee (CEUA #5581-1/2020).

This work was funded by São Paulo Research Foundation [FAPESP 2020/00099-0, 2018/23622-0, 2019/03170-0, 2016/25358-3, 2022/11096-8, 2023/10166-5], the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil [CAPES - Finance Code 001]; the National Council for Scientific and Technological Development [CNPq 300896/2016-6, 302834/2020-6]; the Fundação Grupo Boticário, Brazil [1062_20161]; the Rufford Foundation [22286-1], the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) and Idea Wild (PONTBRAZ0720-00).