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  1. Abstract

    Biodiversity in ecosystems plays an important role in supporting human welfare, including regulating the transmission of infectious diseases. Many of these services are not fully-appreciated due to complex environmental dynamics and lack of baseline data. Multicontinental amphibian decline due to the fungal pathogenBatrachochytrium dendrobatidis(Bd) provides a stark example. Even though amphibians are known to affect natural food webs—including mosquitoes that transmit human diseases—the human health impacts connected to their massive decline have received little attention. Here we leverage a unique ensemble of ecological surveys, satellite data, and newly digitized public health records to show an empirical link between a wave of Bd-driven collapse of amphibians in Costa Rica and Panama and increased human malaria incidence. Subsequent to the estimated date of Bd-driven amphibian decline in each ‘county’ (canton or distrito), we find that malaria cases are significantly elevated for several years. For the six year peak of the estimated effect, the annual expected county-level increase in malaria ranges from 0.76 to 1.1 additional cases per 1000 population. This is a substantial increase given that cases country-wide per 1000 population peaked during the timeframe of our study at approximately 1.5 for Costa Rica and 1.1 for Panama. This previously unidentified impact of biodiversity loss illustrates the often hidden human welfare costs of conservation failures. These findings also show the importance of mitigating international trade-driven spread of similar emergent pathogens likeBatrachochytrium salamandrivorans.

     
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  2. Biodiversity is declining at unprecedented rates worldwide. Yet cascading effects of biodiversity loss on other taxa are largely unknown because baseline data are often unavailable. We document the collapse of a Neotropical snake community after the invasive fungal pathogen Batrachochytrium dendrobatidis caused a chytridiomycosis epizootic leading to the catastrophic loss of amphibians, a food source for snakes. After mass mortality of amphibians, the snake community contained fewer species and was more homogeneous across the study site, with several species in poorer body condition, despite no other systematic changes in the environment. The demise of the snake community after amphibian loss demonstrates the repercussive and often unnoticed consequences of the biodiversity crisis and calls attention to the invisible declines of rare and data-deficient species. 
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  3. Abstract

    Understanding the responses of naïve communities to the invasion of multihost pathogens requires accurate estimates of susceptibility across taxa. In the Americas, the likely emergence of a second amphibian pathogenic fungus (Batrachochytrium salamandrivorans, Bsal) calls for new ways of prioritizing disease mitigation among species due to the high diversity of naïve hosts with priorB. dendrobatidis(Bd) infections. Here, we applied the concept of pathogenic potential to quantify the virulence of chytrid fungi on naïve amphibians and evaluate species for conservation efforts in the event of an outbreak. The benefit of this measure is that it combines and summarizes the variation in disease effects into a single numerical index, allowing for comparisons across species, populations or groups of individuals that may inherently exhibit differences in susceptibility. As a proof of concept, we obtained standardized responses of disease severity by performing experimental infections withBsalon five plethodontid salamanders from southeastern United States. Four out of five species carried natural infections ofBdat the start of the experiments. We showed thatBsalexhibited its highest value of pathogenic potential in a species that is already declining (Desmognathus auriculatus). We find that this index provides additional information beyond the standard measures of disease prevalence, intensity, and mortality, because it leveraged these disease parameters within each categorical group. Scientists and practitioners could use this measure to justify research, funding, trade, or conservation measures.

     
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  4. Abstract

    Resilience of ecosystems to the sudden decline of large‐bodied species is dependent on characteristics of surviving guild members. However, that response may also be mediated by local habitat conditions. Here, we examine the mechanisms behind the observed lack of functional compensation in the algal‐grazing guild by insect grazers following the decline of tadpole grazers in a forested Panamanian stream. We examined: (1) shifts to the individual size distribution of insect grazers between pre‐ and post‐tadpole declines in pool and riffle habitats; (2) tadpole and insect preferences for small‐, medium‐, and large‐sized diatoms; and (3) a causal explanation for why insects did not functionally compensate for tadpole declines. The size distribution of insect grazers following tadpole declines differed between habitats, becoming uniform in pools and more right skewed toward a smaller size class in riffles. In both habitats, tadpoles selectively consumed medium‐sized diatoms but avoided the largest‐sized diatoms. In contrast, grazing insects selectively consumed small‐sized diatoms, but switched to medium‐sized diatoms after tadpole declines. Tadpole declines led to the loss of the strongest interactions between consumers and diatoms. Smaller‐bodied grazing insects could not duplicate these interactions, even with a shift in resource use, providing an explanation for the lack of functional compensation. Furthermore, tadpole declines led to different community structures in each habitat indicating that local habitat conditions mediated the response of surviving guild members. This suggests that the sudden decline of a large‐bodied species does not lead to a singular outcome for the surviving community.

     
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  5. Abstract

    Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungusBatrachochytrium dendrobatidis(Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.

     
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