Pieter T. J. Johnson

Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines

Since amphibian declines were first proposed as a global phenomenon over a quarter century ago, the conservation community has made little progress in halting or reversing these trends. The early search for a “smoking gun” was replaced with the expectation that declines are caused by multiple drivers. While field observations and experiments have identified factors leading to increased local extinction risk, evidence for effects of these drivers is lacking at large spatial scales. Here, we use observations of 389 time-series of 83 species and complexes from 61 study areas across North America to test the effects of 4 of the major hypothesized drivers of declines. While we find that local amphibian populations are being lost from metapopulations at an average rate of 3.79% per year, these declines are not related to any particular threat at the continental scale; likewise the effect of each stressor is variable at regional scales. This result - that exposure to threats varies spatially, and populations vary in their response - provides little generality in the development of conservation strategies. Greater emphasis on local solutions to this globally shared phenomenon is needed.

Parasites in food webs: the ultimate missing links

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food-web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food-web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food-web stability, interaction strength and energy flow. Food-web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food-web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food-web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.

Climate Change and Infectious Diseases: From Evidence to a Predictive Framework

Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.

Dam invaders: impoundments facilitate biological invasions into freshwaters

Freshwater ecosystems are at the forefront of the global biodiversity crisis, with more declining and extinct species than in terrestrial or marine environments. Hydrologic alterations and biological invasions represent two of the greatest threats to freshwater biota, yet the importance of linkages between these drivers of environmental change remains uncertain. Here, we quantitatively test the hypothesis that impoundments facilitate the introduction and establishment of aquatic invasive species in lake ecosystems. By combining data on boating activity, water body physicochemistry, and geographical distribution of five nuisance invaders in the Laurentian Great Lakes region, we show that non-indigenous species are 2.4 to 300 times more likely to occur in impoundments than in natural lakes, and that impoundments frequently support multiple invaders. Furthermore, comparisons of the contemporary and historical landscapes revealed that impoundments enhance the invasion risk of natural lakes by increasing their...

Aquatic eutrophication promotes pathogenic infection in amphibians

The widespread emergence of human and wildlife diseases has challenged ecologists to understand how large-scale agents of environmental change affect host–pathogen interactions. Accelerated eutrophication of aquatic ecosystems owing to nitrogen and phosphorus enrichment is a pervasive form of environmental change that has been implicated in the emergence of diseases through direct and indirect pathways. We provide experimental evidence linking eutrophication and disease in a multihost parasite system. The trematode parasite Ribeiroia ondatrae sequentially infects birds, snails, and amphibian larvae, frequently causing severe limb deformities and mortality. Eutrophication has been implicated in the emergence of this parasite, but definitive evidence, as well as a mechanistic understanding, have been lacking until now. We show that the effects of eutrophication cascade through the parasite life cycle to promote algal production, the density of snail hosts, and, ultimately, the intensity of infection in amphibians. Infection also negatively affected the survival of developing amphibians. Mechanistically, eutrophication promoted amphibian disease through two distinctive pathways: by increasing the density of infected snail hosts and by enhancing per-snail production of infectious parasites. Given forecasted increases in global eutrophication, amphibian extinctions, and similarities between Ribeiroia and important human and wildlife pathogens, our results have broad epidemiological and ecological significance.

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.

Linking environmental nutrient enrichment and disease emergence in humans and wildlife

Worldwide increases in human and wildlife diseases have challenged ecologists to understand how large-scale environmental changes affect host-parasite interactions. One of the most profound changes to Earths ecosystems is the alteration of global nutrient cycles, including those of phosphorus (P) and especially nitrogen (N). Along with the obvious direct benefits of nutrient application for food production, anthropogenic inputs of N and P can indirectly affect the abundance of infectious and noninfectious pathogens. The mechanisms underpinning observed correlations, however, and how such patterns vary with disease type, have long remained conjectural. Here, we highlight recent experimental advances to critically evaluate the relationship between environmental nutrient enrichment and disease. Given the interrelated nature of human and wildlife disease emergence, we include a broad range of human and wildlife examples from terrestrial, marine, and freshwater ecosystems. We examine the consequences of nutrient pollution on directly transmitted, vector-borne, complex life cycle, and noninfectious pathogens, including West Nile virus, malaria, harmful algal blooms, coral reef diseases, and amphibian malformations. Our synthetic examination suggests that the effects of environmental nutrient enrichment on disease are complex and multifaceted, varying with the type of pathogen, host species and condition, attributes of the ecosystem, and the degree of enrichment; some pathogens increase in abundance whereas others decline or disappear. Nevertheless, available evidence indicates that ecological changes associated with nutrient enrichment often exacerbate infection and disease caused by generalist parasites with direct or simple life cycles. Observed mechanisms include changes in host/vector density, host distribution, infection resistance, pathogen virulence or toxicity, and the direct supplementation of pathogens. Collectively, these pathogens may be particularly dangerous because they can continue to cause mortality even as their hosts decline, potentially leading to sustained epidemics or chronic pathology. We suggest that interactions between nutrient enrichment and disease will become increasingly important in tropical and subtropical regions, where forecasted increases in nutrient application will occur in an environment rich with infectious pathogens. We emphasize the importance of careful disease management in conjunction with continued intensification of global nutrient cycles.

Diversity, decoys and the dilution effect: how ecological communities affect disease risk

SUMMARY Growing interest in ecology has recently focused on the hypothesis that community diversity can mediate infection levels and disease (‘dilution effect’). In turn, biodiversity loss — a widespread consequence of environmental change — can indirectly promote increases in disease, including those of medical and veterinary importance. While this work has focused primarily on correlational studies involving vector-borne microparasite diseases (e.g. Lyme disease, West Nile virus), we argue that parasites with complex life cycles (e.g. helminths, protists, myxosporeans and many fungi) offer an excellent additional model in which to experimentally address mechanistic questions underlying the dilution effect. Here, we unite recent ecological research on the dilution effect in microparasites with decades of parasitological research on the decoy effect in macroparasites to explore key questions surrounding the relationship between community structure and disease. We find consistent evidence that community diversity significantly alters parasite transmission and pathology under laboratory as well as natural conditions. Empirical examples and simple transmission models highlight the diversity of mechanisms through which such changes occur, typically involving predators, parasite decoys, low competency hosts or other parasites. However, the degree of transmission reduction varies among diluting species, parasite stage, and across spatial scales, challenging efforts to make quantitative, taxon-specific predictions about disease. Taken together, this synthesis highlights the broad link between community structure and disease while underscoring the importance of mitigating ongoing changes in biological communities owing to species introductions and extirpations.

Biodiversity decreases disease through predictable changes in host community competence

Accelerating rates of species extinctions and disease emergence underscore the importance of understanding how changes in biodiversity affect disease outcomes. Over the past decade, a growing number of studies have reported negative correlations between host biodiversity and disease risk, prompting suggestions that biodiversity conservation could promote human and wildlife health. Yet the generality of the diversity–disease linkage remains conjectural, in part because empirical evidence of a relationship between host competence (the ability to maintain and transmit infections) and the order in which communities assemble has proven elusive. Here we integrate high-resolution field data with multi-scale experiments to show that host diversity inhibits transmission of the virulent pathogen Ribeiroia ondatrae and reduces amphibian disease as a result of consistent linkages among species richness, host composition and community competence. Surveys of 345 wetlands indicated that community composition changed nonrandomly with species richness, such that highly competent hosts dominated in species-poor assemblages whereas more resistant species became progressively more common in diverse assemblages. As a result, amphibian species richness strongly moderated pathogen transmission and disease pathology among 24,215 examined hosts, with a 78.4% decline in realized transmission in richer assemblages. Laboratory and mesocosm manipulations revealed an approximately 50% decrease in pathogen transmission and host pathology across a realistic diversity gradient while controlling for host density, helping to establish mechanisms underlying the diversity–disease relationship and their consequences for host fitness. By revealing a consistent link between species richness and community competence, these findings highlight the influence of biodiversity on infection risk and emphasize the benefit of a community-based approach to understanding infectious diseases.

When parasites become prey: ecological and epidemiological significance of eating parasites

Recent efforts to include parasites in food webs have drawn attention to a previously ignored facet of foraging ecology: parasites commonly function as prey within ecosystems. Because of the high productivity of parasites, their unique nutritional composition and their pathogenicity in hosts, their consumption affects both food-web topology and disease risk in humans and wildlife. Here, we evaluate the ecological, evolutionary and epidemiological significance of feeding on parasites, including concomitant predation, grooming, predation on free-living stages and intraguild predation. Combining empirical data and theoretical models, we show that consumption of parasites is neither rare nor accidental, and that it can sharply affect parasite transmission and food web properties. Broader consideration of predation on parasites will enhance our understanding of disease control, food web structure and energy transfer, and the evolution of complex life cycles.