Are novel or locally adapted pathogens more devastating and why? Resolving opposing hypotheses.

There is a rich literature highlighting that pathogens are generally better adapted to infect local than novel hosts, and a separate seemingly contradictory literature indicating that novel pathogens pose the greatest threat to biodiversity and public health. Here, using Batrachochytrium dendrobatidis, the fungus associated with worldwide amphibian declines, we test the hypothesis that there is enough variance in "novel" (quantified by geographic and phylogenetic distance) host-pathogen outcomes to pose substantial risk of pathogen introductions despite local adaptation being common. Our continental-scale common garden experiment and global-scale meta-analysis demonstrate that local amphibian-fungal interactions result in higher pathogen prevalence, pathogen growth, and host mortality, but novel interactions led to variable consequences with especially virulent host-pathogen combinations still occurring. Thus, while most pathogen introductions are benign, enough variance exists in novel host-pathogen outcomes that moving organisms around the planet greatly increases the chance of pathogen introductions causing profound harm.

Male pathology regardless of behaviour drives transmission in an avian host-pathogen system.

Host sex is an important source of heterogeneity in the severity of epidemics. Pinpointing the mechanisms causing this heterogeneity can be difficult because differences in behaviour among sexes (e.g. greater territorial aggression in males) can bias exposure risk, obfuscating the role of immune function, which can lead to differences in pathology, in driving differential susceptibility between sexes. Thus, sex-biased transmission driven by differences in immune function independent of behaviour is poorly understood, especially in non-mammalian systems. Here we examine the previously unexplored potential for male-biased pathology to affect transmission using an avian host-pathogen system. We employ a sex-dependent multistate transmission model parameterized with isolated, individual-based experimental exposures of domestic canaries and experimental transmission data of house finches. The experiment revealed that male birds have shorter incubation periods, longer recovery periods, higher pathogen burdens and greater disease pathology than females. Our model revealed that male-biased pathology led to epidemic size rapidly increasing with the proportion of male birds, with a nearly 10-fold increase in total epidemic size from an all-female to an all-male simulation. Our results demonstrate that female-biased resistance, independent of male behaviour, can drive sex-dependent transmission in wildlife, indicating that sex-based differences in immune function, not just differences in exposure risk, can shape epidemic dynamics.

Habitat complexity, connectivity, and introduced fish drive pond community structure along an urban to rural gradient.

Urbanization can influence local richness (alpha diversity) and community composition (beta diversity) in numerous ways. For instance, reduced connectivity and land cover change may lead to the loss of native specialist taxa, decreasing alpha diversity. Alternatively, if urbanization facilitates nonnative species introductions and generalist taxa, alpha diversity may remain unchanged or increase, while beta diversity could decline due to the homogenization of community structure. Wetlands and ponds provide critical ecosystem services and support diverse communities, making them important systems in which to understand the consequences of urbanization. To determine how urban development shapes pond community structure, we surveyed 68 ponds around Madison, Wisconsin, USA, which were classified as urban, greenspace, or rural based on surrounding land use. We evaluated how landscape and local pond factors were correlated with the alpha diversity of aquatic plants, macroinvertebrates, and aquatic vertebrates. We also analyzed whether surrounding land use was associated with changes in community composition and the presence of specific taxa. We found a 23% decrease in mean richness (alpha diversity) from rural to urban pond sites and a 15% decrease from rural to greenspace pond sites. Among landscape factors, adjacent developed land, mowed lawn cover, and greater distances to other waterbodies were negatively correlated with observed pond richness. Among pond level factors, habitat complexity was associated with increased richness, while nonnative fishes were associated with decreased richness. Beta diversity was relatively high for all ponds due to turnover in composition between sites. Urban ponds supported more nonnative species, lacked a subset of native species found in rural ponds, and had slightly higher beta diversity than greenspace and rural ponds. Our results suggest that integrating ponds into connected greenspaces, maintaining riparian vegetation, preventing nonnative fish introductions, and promoting habitat complexity may mitigate the negative effects of urbanization on aquatic richness. While ponds are small in size and rarely incorporated into urban conservation planning, the high beta diversity of distinct pond communities emphasizes their importance for supporting urban biodiversity.

Divergent impacts of warming weather on wildlife disease risk across climates.

Disease outbreaks among wildlife have surged in recent decades alongside climate change, although it remains unclear how climate change alters disease dynamics across different geographic regions. We amassed a global, spatiotemporal dataset describing parasite prevalence across 7346 wildlife populations and 2021 host-parasite combinations, compiling local weather and climate records at each location. We found that hosts from cool and warm climates experienced increased disease risk at abnormally warm and cool temperatures, respectively, as predicted by the thermal mismatch hypothesis. This effect was greatest in ectothermic hosts and similar in terrestrial and freshwater systems. Projections based on climate change models indicate that ectothermic wildlife hosts from temperate and tropical zones may experience sharp increases and moderate reductions in disease risk, respectively, though the magnitude of these changes depends on parasite identity.

Infection pathology and competition mediate host biomass overcompensation from disease.

Predators can increase the biomass of their prey, particularly when prey life stages differ in competitive ability and predation is stage specific. Akin to predators, parasites influence host population sizes and engage in stage-structured interactions, yet whether parasites can increase host population biomass remains relatively unexplored. Using a stage-structured consumer-resource model and a mesocosm experiment with snails and castrating trematodes, we examined responses of host biomass to changes in infection prevalence under variation in host pathology and resource competition. Equilibrium adult host biomass increased with infection prevalence in the model when parasites castrated hosts and adults were superior competitors to juveniles. Juvenile biomass increased with infection prevalence whether parasites caused mortality or castration, but only when juveniles were superior competitors. In mesocosms, increases in infection by castrating trematodes reduced snail egg production, juvenile abundance, and adult survival. At high competition, juvenile growth and total biomass increased with infection prevalence due to competitive release. At low competition, juvenile biomass decreased with infection due to reduced reproduction. These results highlight how disease-induced biomass overcompensation depends on infection pathology, resource availability, and competitive interactions within and between host life stages. Considering such characteristics may benefit biocontrol efforts using parasites.

A meta-analysis reveals temperature, dose, life stage, and taxonomy influence host susceptibility to a fungal parasite.

Complex ecological relationships, such as host-parasite interactions, are often modeled with laboratory experiments. However, some experimental laboratory conditions, such as temperature or infection dose, are regularly chosen based on convenience or convention, and it is unclear how these decisions systematically affect experimental outcomes. Here, we conducted a meta-analysis of 58 laboratory studies that exposed amphibians to the pathogenic fungus Batrachochytrium dendrobatidis (Bd) to understand better how laboratory temperature, host life stage, infection dose, and host species affect host mortality. We found that host mortality was driven by thermal mismatches: hosts native to cooler environments experienced greater Bd-induced mortality at relatively warm experimental temperatures and vice versa. We also found that Bd dose positively predicted Bd-induced host mortality and that the superfamilies Bufonoidea and Hyloidea were especially susceptible to Bd. Finally, the effect of Bd on host mortality varied across host life stages, with larval amphibians experiencing lower risk of Bd-induced mortality than adults or metamorphs. Metamorphs were especially susceptible and experienced mortality when inoculated with much smaller Bd doses than the average dose used by researchers. Our results suggest that when designing experiments on species interactions, researchers should carefully consider the experimental temperature, inoculum dose, and life stage, and taxonomy of the host species.

Impacts of thermal mismatches on chytrid fungus Batrachochytrium dendrobatidis prevalence are moderated by life stage, body size, elevation and latitude.

Global climate change is increasing the frequency of unpredictable weather conditions; however, it remains unclear how species-level and geographic factors, including body size and latitude, moderate impacts of unusually warm or cool temperatures on disease. Because larger and lower-latitude hosts generally have slower acclimation times than smaller and higher-latitude hosts, we hypothesised that their disease susceptibility increases under 'thermal mismatches' or differences between baseline climate and the temperature during surveying for disease. Here, we examined how thermal mismatches interact with body size, life stage, habitat, latitude, elevation, phylogeny and International Union for Conservation of Nature (IUCN) conservation status to predict infection prevalence of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in a global analysis of 32 291 amphibian hosts. As hypothesised, we found that the susceptibility of larger hosts and hosts from lower latitudes to Bd was influenced by thermal mismatches. Furthermore, hosts of conservation concern were more susceptible than others following thermal mismatches, suggesting that thermal mismatches might have contributed to recent amphibian declines.

Behavioural fever reduces ranaviral infection in toads.

1. Host behaviour is known to influence disease dynamics. Additionally, hosts often change their behaviours in response to pathogen detection to resist and avoid disease. The capacity of wildlife populations to respond to pathogens using behavioural plasticity is critical for reducing the impacts of disease outbreaks. However, there is limited information regarding the ability of ectothermic vertebrates to resist diseases via behavioural plasticity. 2. Here, we experimentally examine the effect of host behaviour on ranaviral infections, which affect at least 175 species of ectothermic vertebrates. We placed metamorphic (temporal block 1) or adult (block 2) Southern toads (Anaxyrus terrestris) in thermal gradients, tested their temperature preferences before and after oral inoculation by measuring individual-level body temperature over time, and measured ranaviral loads of viral-exposed individuals. 3. We found significant individual-level variation in temperature preference and evidence for behavioural fever in both metamorph and adult A. terrestris during the first two days after exposure. Additionally, we found that individual-level change in temperature preference was negatively correlated with ranaviral load and a better predictor of load than average temperature preference or maximum temperature reached by an individual. In other words, an increase in baseline temperature preference was more important than simply reaching an absolute temperature. 4. These results suggest that behavioural fever is an effective mechanism for resisting ranaviral infections.

Variation in individual temperature preferences, not behavioural fever, affects susceptibility to chytridiomycosis in amphibians.

The ability of wildlife populations to mount rapid responses to novel pathogens will be critical for mitigating the impacts of disease outbreaks in a changing climate. Field studies have documented that amphibians preferring warmer temperatures are less likely to be infected with the fungal pathogen Batrachochytrium dendrobatidis (Bd). However, it is unclear whether this phenomenon is driven by behavioural fever or natural variation in thermal preference. Here, we placed frogs in thermal gradients, tested for temperature preferences and measured Bd growth, prevalence, and the survival of infected animals. Although there was significant individual- and species-level variation in temperature preferences, we found no consistent evidence of behavioural fever across five frog species. Interestingly, for species that preferred warmer temperatures, the preferred temperatures of individuals were negatively correlated with Bd growth on hosts, while the opposite correlation was true for species preferring cooler temperatures. Our results suggest that variation in thermal preference, but not behavioural fever, might shape the outcomes of Bd infections for individuals and populations, potentially resulting in selection for individual hosts and host species whose temperature preferences minimize Bd growth and enhance host survival during epidemics.

The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease.

Parasites typically have broader thermal limits than hosts, so large performance gaps between pathogens and their cold- and warm-adapted hosts should occur at relatively warm and cold temperatures, respectively. We tested this thermal mismatch hypothesis by quantifying the temperature-dependent susceptibility of cold- and warm-adapted amphibian species to the fungal pathogen Batrachochytrium dendrobatidis (Bd) using laboratory experiments and field prevalence estimates from 15 410 individuals in 598 populations. In both the laboratory and field, we found that the greatest susceptibility of cold- and warm-adapted hosts occurred at relatively warm and cool temperatures, respectively, providing support for the thermal mismatch hypothesis. Our results suggest that as climate change shifts hosts away from their optimal temperatures, the probability of increased host susceptibility to infectious disease might increase, but the effect will depend on the host species and the direction of the climate shift. Our findings help explain the tremendous variation in species responses to Bd across climates and spatial, temporal and species-level variation in disease outbreaks associated with extreme weather events that are becoming more common with climate change.

An efficient and inexpensive method for measuring long-term thermoregulatory behavior.

Thermoregulatory ability and behavior influence organismal responses to their environment. By measuring thermal preferences, researchers can better understand the effects that temperature tolerances have on ecological and physiological responses to both biotic and abiotic stressors. However, because of funding limitations and confounders, measuring thermoregulation can often be difficult. Here, we provide an effective, affordable (~$50 USD per unit), easy to construct, and validated apparatus for measuring the long-term thermal preferences of animals. In tests, the apparatus spanned temperatures from 9.29 to 33.94°C, and we provide methods to further increase this range. Additionally, we provide simple methods to non-invasively measure animal and substrate temperatures and to prevent temperature preferences of the focal organisms from being confounded with temperature preferences of its prey and its humidity preferences. To validate the apparatus, we show that it was capable of detecting individual-level consistency and among individual-level variation in the preferred body temperatures of Southern toads (Anaxyrus terrestris) and Cuban tree frogs (Osteopilus septentrionalis) over three-weeks. Nearly every aspect of our design is adaptable to meet the needs of a multitude of study systems, including various terrestrial amphibious, and aquatic organisms. The apparatus and methods described here can be used to quantify behavioral thermal preferences, which can be critical for determining temperature tolerances across species and thus the resiliency of species to current and impending climate change.

Spatial scale modulates the strength of ecological processes driving disease distributions.

Humans are altering the distribution of species by changing the climate and disrupting biotic interactions and dispersal. A fundamental hypothesis in spatial ecology suggests that these effects are scale dependent; biotic interactions should shape distributions at local scales, whereas climate should dominate at regional scales. If so, common single-scale analyses might misestimate the impacts of anthropogenic modifications on biodiversity and the environment. However, large-scale datasets necessary to test these hypotheses have not been available until recently. Here we conduct a cross-continental, cross-scale (almost five orders of magnitude) analysis of the influence of biotic and abiotic processes and human population density on the distribution of three emerging pathogens: the amphibian chytrid fungus implicated in worldwide amphibian declines and West Nile virus and the bacterium that causes Lyme disease (Borrelia burgdorferi), which are responsible for ongoing human health crises. In all three systems, we show that biotic factors were significant predictors of pathogen distributions in multiple regression models only at local scales (∼10(2)-10(3) km(2)), whereas climate and human population density always were significant only at relatively larger, regional scales (usually >10(4) km(2)). Spatial autocorrelation analyses revealed that biotic factors were more variable at smaller scales, whereas climatic factors were more variable at larger scales, as is consistent with the prediction that factors should be important at the scales at which they vary the most. Finally, no single scale could detect the importance of all three categories of processes. These results highlight that common single-scale analyses can misrepresent the true impact of anthropogenic modifications on biodiversity and the environment.

Linking manipulative experiments to field data to test the dilution effect.

The dilution effect, the hypothesis that biodiversity reduces disease risk, has received support in many systems. However, few dilution effect studies have linked mechanistic experiments to field patterns to establish both causality and ecological relevance. We conducted a series of laboratory experiments and tested the dilution effect hypothesis in an amphibian-Batrachochytrium dendrobatidis (Bd) system and tested for consistency between our laboratory experiments and field patterns of amphibian species richness, host identity and Bd prevalence. In our laboratory experiments, we show that tadpoles can filter feed Bd zoospores and that the degree of suspension feeding was positively associated with their dilution potential. The obligate suspension feeder, Gastrophryne carolinensis, generally diluted the risk of chytridiomycosis for tadpoles of Bufo terrestris and Hyla cinerea, whereas tadpoles of B. terrestris (an obligate benthos feeder) generally amplified infections for the other species. In addition, G. carolinensis reduced Bd abundance on H. cinerea more so in the presence than absence of B. terrestris and B. terrestris amplified Bd abundance on H. cinerea more so in the absence than presence of G. carolinensis. Also, when ignoring species identity, species richness was a significant negative predictor of Bd abundance. In our analysis of field data, the presence of Bufo spp. and Gastrophryne spp. were significant positive and negative predictors of Bd prevalence, respectively, even after controlling for climate, vegetation, anthropogenic factors (human footprint), species richness and sampling effort. These patterns of dilution and amplification supported our laboratory findings, demonstrating that the results are likely ecologically relevant. The results from our laboratory and field data support the dilution effect hypothesis and also suggest that dilution and amplification are predictable based on host traits. Our study is among the first to link manipulative experiments, in which a potential dilution mechanism is supported, with analyses of field data on species richness, host identity, spatial autocorrelation and disease prevalence.