ABSTRACT Wild populations face unprecedented pressure from an assortment of anthropogenic environmental changes and parasites. We sought to understand how host–parasite interactions are affected by the interactive effects of multiple environmental stressors and subsequent parasite infection.We focused on American bullfrog tadpoles (Lithobates catesbeianus) that can become infected by several parasite species (e.g., trematodes in the family Echinostomatidae genus Echinstoma, andBatrachochytrium dendrobatidis; “Bd”) and are affected by abiotic stressors including road salt and variable temperatures attributed to climate change. In a multi‐phase laboratory experiment, we exposed tadpoles to one of two salt treatments (0 and 1.5 g L−1added NaCl sublethal salt) and one of two temperature treatments (constant 23°C and fluctuating between 20°C and 25°C). Next, we exposed these tadpoles to one of four parasite treatments (parasite absent,Bdonly, trematodes only, andBd& trematodes together) at a constant temperature (23°C) without added salt. We then recorded morphological measurements (length, mass, developmental stage) and quantified infection intensity.Tadpoles exposed toBdwere larger in mass than the other parasite treatments, and the effects of trematode exposure on length varied by temperature. We did not detect any effect of our treatments on developmental stage. We found an interaction between the salinity and temperature treatments where tadpoles exposed toBdonly or to fluctuating temperatures andBdand trematodes together had higherBdinfection in the no salt added treatment compared to the sublethal salt treatment. Tadpoles in stable temperatures and no salt treatments had lower subsequentBdinfection loads than those in stable temperatures and elevated salt. With trematode infection, we found that when no salt was added, tadpoles exposed to trematodes only had higher parasite abundance compared to the other treatments (i.e., a salinity by parasite interaction).Our results suggest that the interaction of temperatures and salt pollution in freshwater can increase subsequentBdinfection and that the parasites (Bd& echinostome trematodes) can interact with each other, altering infection levels.
more »
« less
Many roads to reservoirs? How susceptibility and shedding shape host competence in amphibians
Abstract Host competence—the ability to acquire, harbour and transmit infections—drives pathogen spread and persistence in multi‐host communities. Evaluating species‐specific competence is critical for predicting transmission, particularly for generalist fungal pathogens likeBatrachochytrium dendrobatidis(Bd). Despite its central role in disease dynamics, we lack an epidemiologically grounded competence metric that rigorously accounts for how infection intensity affects a host's competence. This knowledge gap limits our ability to compare mechanisms across species and assess their roles in pathogen persistence. To address these challenges, we developed a novel, load‐dependent competence metric using host–pathogen Integral Projection Models (IPMs) that integrates variation in susceptibility, within‐host pathogen growth and pathogen shedding dynamics.We applied this metric to laboratory‐based challenge experiments with three common North American amphibians (Notophthalmus viridescens,Rana clamitansandRana catesbeianus) that persist endemically with Bd. Using dose–response assays and repeated pathogen shedding measurements across species, we asked: (i) is there a consistent, non‐linear relationship between infection intensity and pathogen shedding across species? and (ii) which load‐based traits best predict host competence? We quantified four of five components of host competence—susceptibility, pathogen growth, pathogen survival and load‐dependent shedding—and used these to parameterize species‐specific IPMs, integrating competence into a single relative metric across species.We found that Bd shedding increased non‐linearly with infection intensity, contradicting the standard assumption that Bd shedding is linearly related to infection intensity.Notophthalmus viridescensandR. catesbeianuswere the most competent hosts but through distinct pathways: high susceptibility inN. viridescensand elevated shedding rates inR. catesbeianus. In contrast, density‐dependent reductions in pathogen growth and shedding limitedR. clamitanscompetence. Thus, species‐level competence is not determined by a single trait, but emerges from interactions among multiple load‐based processes.Our results demonstrate that variation in competence emerges from distinct, species‐specific processes across multiple dimensions of competence. By linking individual infection dynamics to population‐level transmission potential, our integrative framework provides a more mechanistic approach to predicting host contributions to community‐level pathogen persistence. Read the freePlain Language Summaryfor this article on the Journal blog.
more »
« less
- Award ID(s):
- 2044897
- PAR ID:
- 10673164
- Publisher / Repository:
- British Ecological Society
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 40
- Issue:
- 3
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- 585 to 598
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Batrachochytrium dendrobatidis(Bd), an aquatic pathogenic fungus, is responsible for the decline of hundreds of amphibian species worldwide and negatively impacts biodiversity globally. Prophylactic exposure to the metabolites produced by Bd can provide protection for naïve tree frogs and reduce subsequent Bd infection intensity.Here, we used a response surface design crossing Bd metabolite prophylaxis concentration and exposure duration to determine how these factors modulate prophylactic protection against Bd in Pacific chorus frog (Pseudacris regilla) tadpoles (5 × 5 surface design) and metamorphs (3 × 3 surface design). We exposed individuals every weekday to one of five Bd metabolite concentrations or a water control for 1–5 weeks, after which all animals were challenged with live Bd to evaluate their susceptibility.Exposure to the Bd metabolite prophylaxis reduced Bd load and prevalence compared to the control for both the tadpoles and metamorphs. Increasing Bd metabolite prophylaxis concentration did not confer additional protection for either life stage, but increasing duration of exposure did benefit metamorphs by decreasing Bd prevalence but not Bd load.On average, control tadpoles and metamorphs had 66.2% and 99.4% higher Bd loads, respectively, than tadpoles and metamorphs exposed to any Bd metabolite prophylaxis.Additionally, Bd metabolite prophylaxis reduced Bd prevalence relative to controls in both tadpoles (20.5% vs. 56.3%, respectively) and metamorphs (21.9% vs. 87.5%, respectively).Synthesis and applications: The efficacy of short‐term exposures of relatively low concentrations of Bd metabolites at reducing Bd infections suggests that this approach has the potential to be scaled up to field use to aid in disease mitigation and conservation. Our results, combined with additional research on Bd metabolite prophylaxis for other amphibian species, suggest that this strategy may represent a broadly useful tool to protect at‐risk amphibian populations.more » « less
-
Some of the amphibian populations in Panama are demonstrating slow recovery decades after severe declines caused by the invasion of the fungal pathogenBatrachochytrium dendrobatidis(Bd). However, new species remain to be described and assessed for the mechanisms of disease resilience. We identified seven skin defense peptides from a presumably novel leopard frog species in the Tabasará range, at Buäbti (Llano Tugrí), Ngäbe-Buglé Comarca, and Santa Fe, Veraguas, Panama, herein called the Ngäbe-Buglé leopard frog. Two of the peptides were previously known: brevinin-1BLb fromRana (Lithobates) blairiand a previously hypothesized “ancestral” peptide, ranatuerin-2BPa. We hypothesized that the peptides are active againstBdand shape the microbiome such that the skin bacterial communities are more similar to those of other leopard frogs than of co-occurring host species. Natural mixtures of the collected skin peptides showed a minimum inhibitory concentration againstBdof 100 μg/ml, which was similar to that of other leopard frogs that have been tested. All sampled individuals hosted high intensity of infection withBd. We sampled nine other amphibian species in nearby habitats and found lower prevalence and intensities ofBdinfection. In addition to the pathogen load, the skin microbiomes were examined using 16S rRNA gene targeted amplicon sequencing. When compared to nine co-occurring amphibians, the Ngäbe-Buglé leopard frog had similar skin bacterial richness and anti-Bdfunction, but the skin microbiome structure differed significantly among species. The community composition of the bacterial skin communities was strongly associated with theBdinfection load. In contrast, the skin microbiome composition of the Ngäbe-Buglé leopard frog was similar to that of five North American leopard frog populations and the sympatric and congenericRana (Lithobates) warszewitschii, with 29 of the 46 core bacteria all demonstrating anti-Bdactivity in culture. Because of the highBdinfection load and prevalence in the Ngäbe-Buglé leopard frog, we suggest that treatment to reduce theBdload in this species might reduce the chytridiomycosis risk in the co-occurring amphibian community, but could potentially disrupt the evolution of skin defenses that provide a mechanism for disease resilience in this species.more » « less
-
Abstract In insects and other invertebrates, prior pathogen exposures can improve immune responses and survival to subsequent infections through immune priming. Alternatively, stress and metabolic costs of multiple infections can impair host immunity and survival. The effects of high‐temperature extremes on host–pathogen interactions are not well understood despite the increasing occurrence of heat waves caused by climate change.The response of insects to heat waves and pathogens depends on recent evolutionary history with selective pressures. Domestication of insect pests has occurred in lab colonies of model species, reducing selective pressures for immune and heat stress responses. Lab strains are often used in immunological or heat stress experiments to represent wild field strains, but the efficacy of this approach is seldom evaluated.Using the tobacco hornworm (Manduca sexta), we tested the impact of a heat wave during initial pathogen exposure on survival of a secondary infection withBacillus thuringiensisbacteria. We used a domesticated lab population and a naturally occurring field population ofM. sextato evaluate the impacts of recent domestication on immune and thermal responses.A heat wave during initial infection significantly increased survival of the secondaryB. thuringiensisinfection in the field, but not the lab population ofM. sexta.In the field population, survival of the repeated infection was temperature dependent: exposure to an initial infection event reduced survival of the secondary infection at the control temperature regime, consistent with a stress effect. However, a heat wave during the initial infection event increased survival of the secondary infection, consistent with immune priming effects.The results of this study demonstrate that (a) insect response to thermal stress and pathogens can depend on recent domestication and (b) responses of hosts to repeat pathogen exposures can be temperature‐dependent, suggesting that cross‐talk between the heat stress and immune memory pathways may have important consequences for host–pathogen outcomes under heat wave events. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
Abstract Ecological niche models (ENMs) have been used frequently to predict the distribution and future spread of the pathogenic chytrid fungusBatrachochytrium dendrobatidis(Bd). Based on the assumption that chytridiomycosis outbreaks are most likely to occur where the conditions are ideal for Bd, many studies have identified high‐risk areas for chytridiomycosis and its associated mortality risk using only known Bd occurrences. However, the presence of a pathogen does not necessarily indicate high infection, disease or associated mortality.We used the BIOMOD2 package implemented in R, 19 bioclimatic variables, and 267 locality records, covering three levels of infection progress (occurrence, high infection loads and disease‐associated mortality), to calculate the potential areas where: (1) Bd is likely to be present, (2) amphibians are prone to harbour high infections and (3) chytridiomycosis‐related mortalities are likely to occur. We evaluate discrepancies among the three potential areas projected by the models, encompassing their spatial extent and associated environmental conditions.When all the Bd occurrences were used, the predicted area subjected to Bd risk covered 17% of the study area. However, when just mortality records were used, the predicted area decreased three‐fold. Notably, the three predicted areas only overlapped in 3% of the total study area, suggesting that the region at risk of mortality plus high infections constituted only one‐fifth of the predicted area for Bd presence. Mean temperature during the wettest and warmest 3 months of the year together with isothermality emerged as the most robust negative predictors in each of the three models.Synthesis and applications. Ecological niche models (ENMs) based on the presence data ofBatrachochytrium dendrobatidis(Bd) can overestimate the mortality risk of chytridiomycosis because the environmental conditions suitable for Bd presence do not always correspond to those conducive to significant host mortality. Distribution modelling can be a powerful tool when used correctly, and this study highlights the significance of careful data selection to ensure alignment with intended objectives. Considering the widespread use of ENMs to inform policy, meticulous design and comprehensive evaluation are imperative.more » « less
An official website of the United States government

