Sara H. Paull

Frontiers in climate change–disease research

The notion that climate change will generally increase human and wildlife diseases has garnered considerable public attention, but remains controversial and seems inconsistent with the expectation that climate change will also cause parasite extinctions. In this review, we highlight the frontiers in climate change–infectious disease research by reviewing knowledge gaps that make this controversy difficult to resolve. We suggest that forecasts of climate-change impacts on disease can be improved by more interdisciplinary collaborations, better linking of data and models, addressing confounding variables and context dependencies, and applying metabolic theory to host–parasite systems with consideration of community-level interactions and functional traits. Finally, although we emphasize host–parasite interactions, we also highlight the applicability of these points to climate-change effects on species interactions in general.

From superspreaders to disease hotspots: linking transmission across hosts and space

Since the identification and imprisonment of “Typhoid Mary”, a woman who infected at least 47 people with typhoid in the early 1900s, epidemiologists have recognized that “superspreading” hosts play a key role in disease epidemics. Such variability in transmission also exists among species within a community and among habitat patches across a landscape, underscoring the need for an integrative framework for studying transmission heterogeneity, or the differences among hosts or locations in their contribution to pathogen spread. Here, we synthesize literature on human, plant, and animal diseases to evaluate the relative influence of host, pathogen, and environmental factors in producing highly infectious individuals, species, and landscapes. We show that host and spatial heterogeneity are closely linked and that quantitatively assessing the contribution of infectious individuals, species, or environmental patches to overall transmission can aid management strategies. We conclude by posing hypotheses regarding how pathogen natural history influences transmission variability and highlight emerging frontiers in this area of study.

Species diversity reduces parasite infection through cross‐generational effects on host abundance

With growing interest in the effects of biodiversity on disease, there is a critical need for studies that empirically identify the mechanisms underlying the diversity-disease relationship. Here, we combined wetland surveys of host community structure with mechanistic experiments involving a multi-host parasite to evaluate competing explanations for the dilution effect. Sampling of 320 wetlands in California indicated that snail host communities were strongly nested, with competent hosts for the trematode Ribeiroia ondatrae predominating in low-richness assemblages and unsuitable hosts increasingly present in more diverse communities. Moreover, competent host density was negatively associated with increases in snail species richness. These patterns in host community assembly support a key prerequisite underlying the dilution effect. Results of multigenerational mesocosm experiments designed to mimic field-observed community assemblages allowed us to evaluate the relative importance of host density and diversity in influencing parasite infection success. Increases in snail species richness (from one to four species) had sharply negative effects on the density of infected hosts (-90% reduction). However, this effect was indirect; competition associated with non-host species led to a 95% reduction in host density (susceptible host regulation), owing primarily to a reduction in host reproduction. Among susceptible hosts, there were no differences in infection prevalence as a function of community structure, indicating a lack of support for a direct effect of diversity on infection (encounter reduction). In monospecific conditions, higher initial host densities increased infection among adult hosts; however, compensatory reproduction in the low-density treatments equalized the final number of infected hosts by the next generation, underscoring the relevance of multigenerational studies in understanding the dilution effect. These findings highlight the role of interspecific competition in mediating the relationship between species richness and parasite infection and emphasize the importance of field-informed experimental research in understanding mechanisms underlying the diversity-disease relationship.

Using physiology to understand climate-driven changes in disease and their implications for conservation

Given that host-parasite interactions are generally mediated by physiological responses, we submit that physiological models could facilitate predicting how host-parasite interactions respond to climate change, and might offer theoretical and terminological cohesion that has been lacking in the climate change-disease literature.

Does life history mediate changing disease risk when communities disassemble

Biodiversity loss sometimes increases disease risk or parasite transmission in humans, wildlife and plants. Some have suggested that this pattern can emerge when host species that persist throughout community disassembly show high host competence - the ability to acquire and transmit infections. Here, we briefly assess the current empirical evidence for covariance between host competence and extirpation risk, and evaluate the consequences for disease dynamics in host communities undergoing disassembly. We find evidence for such covariance, but the mechanisms for and variability around this relationship have received limited consideration. This deficit could lead to spurious assumptions about how and why disease dynamics respond to community disassembly. Using a stochastic simulation model, we demonstrate that weak covariance between competence and extirpation risk may account for inconsistent effects of host diversity on disease risk that have been observed empirically. This model highlights the predictive utility of understanding the degree to which host competence relates to extirpation risk, and the need for a better understanding of the mechanisms underlying such relationships.

The Scaling of Host Density with Richness Affects the Direction, Shape, and Detectability of Diversity-Disease Relationships

Pathogen transmission responds differently to host richness and abundance, two unique components of host diversity. However, the heated debate around whether biodiversity generally increases or decreases disease has not considered the relationships between host richness and abundance that may exist in natural systems. Here we use a multi-species model to study how the scaling of total host community abundance with species richness mediates diversity-disease relationships. For pathogens with density-dependent transmission, non-monotonic trends emerge between pathogen transmission and host richness when host community abundance saturates with richness. Further, host species identity drives high variability in pathogen transmission in depauperate communities, but this effect diminishes as host richness accumulates. Using simulation we show that high variability in low richness communities and the non-monotonic relationship observed with host community saturation may reduce the detectability of trends in empirical data. Our study emphasizes that understanding the patterns and predictability of host community composition and pathogen transmission mode will be crucial for predicting where and when specific diversity-disease relationships should occur in natural systems.

Drought and immunity determine the intensity of west nile virus epidemics and climate change impacts

The effect of global climate change on infectious disease remains hotly debated because multiple extrinsic and intrinsic drivers interact to influence transmission dynamics in nonlinear ways. The dominant drivers of widespread pathogens, like West Nile virus, can be challenging to identify due to regional variability in vector and host ecology, with past studies producing disparate findings. Here, we used analyses at national and state scales to examine a suite of climatic and intrinsic drivers of continental-scale West Nile virus epidemics, including an empirically derived mechanistic relationship between temperature and transmission potential that accounts for spatial variability in vectors. We found that drought was the primary climatic driver of increased West Nile virus epidemics, rather than within-season or winter temperatures, or precipitation independently. Local-scale data from one region suggested drought increased epidemics via changes in mosquito infection prevalence rather than mosquito abundance. In addition, human acquired immunity following regional epidemics limited subsequent transmission in many states. We show that over the next 30 years, increased drought severity from climate change could triple West Nile virus cases, but only in regions with low human immunity. These results illustrate how changes in drought severity can alter the transmission dynamics of vector-borne diseases.

Combined influence of hydroperiod and parasitism on larval amphibian development

Abstract Hydroperiod strongly influences the breeding period and development time of many amphibians, and larvae of various species display developmental plasticity in response to habitat drying. Hydrologic alterations associated with anthropogenic activities potentially can influence host—parasite interactions in humans and wildlife, but few investigators have examined this possibility. Pathogens can delay amphibian development, so infections could constrain the ability of parasitized larvae to respond to a shortened hydroperiod under drying conditions. We examined the individual and joint effects of hydroperiod and infection with a pathogenic trematode parasite (Ribeiroia ondatrae) on larval development of Pacific chorus frogs (Pseudacris regilla) in mesocosms. Tadpoles subjected to accelerated drying were twice as likely to emerge early. However, this tendency was most pronounced among uninfected individuals (96% of early-emerging individuals) and may have arisen from differences in competitive ability between infected and uninfected conspecifics in mesocosms. Our findings indicate the importance of investigating hydrologic variables associated with environmental perturbations, such as climate change, particularly as they relate to the ability of organisms to respond to multiple stressors that include diseases.

Does Climate Change Increase the Risk of Disease? Analyzing Published Literature to Detect Climate–Disease Interactions

The emergence of infectious diseases has lead to the hypothesis that multidecadal changes in temperature, precipitation, and other weather variables has facilitated disease emergence. We examined 30 years of published literature to test this hypothesis and identify the contexts in which alternative scenarios may occur. Research on the links between climate and disease emergence has increased notably since 1990, even after correcting for research effort, and the majority of long-term reports cite a positive association between disease and changing climates. However, an overall shortage of multi-year studies coupled with the challenges of testing this hypothesis in the presence of multiple environmental change drivers; underscore the need for more long-term studies of pathogen communities.