A meta-analysis on global change drivers and the risk of infectious disease.

Anthropogenic change is contributing to the rise in emerging infectious diseases, which are significantly correlated with socioeconomic, environmental and ecological factors1. Studies have shown that infectious disease risk is modified by changes to biodiversity2-6, climate change7-11, chemical pollution12-14, landscape transformations15-20 and species introductions21. However, it remains unclear which global change drivers most increase disease and under what contexts. Here we amassed a dataset from the literature that contains 2,938 observations of infectious disease responses to global change drivers across 1,497 host-parasite combinations, including plant, animal and human hosts. We found that biodiversity loss, chemical pollution, climate change and introduced species are associated with increases in disease-related end points or harm, whereas urbanization is associated with decreases in disease end points. Natural biodiversity gradients, deforestation and forest fragmentation are comparatively unimportant or idiosyncratic as drivers of disease. Overall, these results are consistent across human and non-human diseases. Nevertheless, context-dependent effects of the global change drivers on disease were found to be common. The findings uncovered by this meta-analysis should help target disease management and surveillance efforts towards global change drivers that increase disease. Specifically, reducing greenhouse gas emissions, managing ecosystem health, and preventing biological invasions and biodiversity loss could help to reduce the burden of plant, animal and human diseases, especially when coupled with improvements to social and economic determinants of health.

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.

Mean species responses predict effects of environmental change on coexistence.

Environmental change research is plagued by the curse of dimensionality: the number of communities at risk and the number of environmental drivers are both large. This raises the pressing question if a general understanding of ecological effects is achievable. Here, we show evidence that this is indeed possible. Using theoretical and simulation-based evidence for bi- and tritrophic communities, we show that environmental change effects on coexistence are proportional to mean species responses and depend on how trophic levels on average interact prior to environmental change. We then benchmark our findings using relevant cases of environmental change, showing that means of temperature optima and of species sensitivities to pollution predict concomitant effects on coexistence. Finally, we demonstrate how to apply our theory to the analysis of field data, finding support for effects of land use change on coexistence in natural invertebrate communities.

Density declines, richness increases, and composition shifts in stream macroinvertebrates.

Documenting trends of stream macroinvertebrate biodiversity is challenging because biomonitoring often has limited spatial, temporal, and taxonomic scopes. We analyzed biodiversity and composition of assemblages of >500 genera, spanning 27 years, and 6131 stream sites across forested, grassland, urban, and agricultural land uses throughout the United States. In this dataset, macroinvertebrate density declined by 11% and richness increased by 12.2%, and insect density and richness declined by 23.3 and 6.8%, respectively, over 27 years. In addition, differences in richness and composition between urban and agricultural versus forested and grassland streams have increased over time. Urban and agricultural streams lost the few disturbance-sensitive taxa they once had and gained disturbance-tolerant taxa. These results suggest that current efforts to protect and restore streams are not sufficient to mitigate anthropogenic effects.

Variability in environmental persistence but not per capita transmission rates of the amphibian chytrid fungus leads to differences in host infection prevalence.

Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance. The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds]. We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water. These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free-living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies.

Pesticides alter ecosystem respiration via phytoplankton abundance and community structure: Effects on the carbon cycle?

Freshwater systems are critical to life on earth, yet they are threatened by the increasing rate of synthetic chemical pollution. Current predictions of the effects of synthetic chemicals on freshwater ecosystems are hampered by the sheer number of chemical contaminants entering aquatic systems, the diversity of organisms inhabiting these systems, the myriad possible direct and indirect effects resulting from these combinations, and uncertainties concerning how contaminants might alter ecosystem metabolism via changes in biodiversity. To address these knowledge gaps, we conducted a mesocosm experiment that elucidated the responses of ponds composed of phytoplankton and zooplankton to standardized concentrations of 12 pesticides, nested within four pesticide classes, and two pesticide types. We show that the effects of the pesticides on algae were consistent within herbicides and insecticides and that responses of over 70 phytoplankton species and genera were consistent within broad taxonomic groups. Insecticides generated top-down effects on phytoplankton community composition and abundance, which were associated with persistent increases in ecosystem respiration. Insecticides had direct toxic effects on cladocerans, which led to competitive release of copepods. These changes in the zooplankton community led to a decrease in green algae and a modest increase in diatoms. Herbicides did not change phytoplankton composition but reduced total phytoplankton abundance. This reduction in phytoplankton led to short-term decreases in ecosystem respiration. Given that ponds release atmospheric carbon and that worldwide pesticide pollution continues to increase exponentially, scientists and policy makers should pay more attention to the ways pesticides alter the carbon cycle in ponds via changes in communities, as demonstrated by our results. Our results show that these predictions can be simplified by grouping pesticides into types and species into functional groups. Adopting this approach provides an opportunity to improve the efficiency of risk assessment and mitigation responses to global change.

Consistent effects of pesticides on community structure and ecosystem function in freshwater systems.

Predicting ecological effects of contaminants remains challenging because of the sheer number of chemicals and their ambiguous role in biodiversity-ecosystem function relationships. We evaluate responses of experimental pond ecosystems to standardized concentrations of 12 pesticides, nested in four pesticide classes and two pesticide types. We show consistent effects of herbicides and insecticides on ecosystem function, and slightly less consistent effects on community composition. Effects of pesticides on ecosystem function are mediated by alterations in the abundance and community composition of functional groups. Through bottom-up effects, herbicides reduce respiration and primary productivity by decreasing the abundance of phytoplankton. The effects of insecticides on respiration and primary productivity of phytoplankton are driven by top-down effects on zooplankton composition and abundance, but not richness. By demonstrating consistent effects of pesticides on communities and ecosystem functions and linking pesticide-induced changes in functional groups of organisms to ecosystem functions, the study suggests that ecological risk assessment of registered chemicals could be simplified to synthetic chemical classes or types and groups of organisms with similar functions and chemical toxicities.

Effects of agrochemical pollution on schistosomiasis transmission: a systematic review and modelling analysis.

BACKGROUND: Agrochemical pollution of surface waters is a growing global environmental challenge, especially in areas where agriculture is rapidly expanding and intensifying. Agrochemicals might affect schistosomiasis transmission through direct and indirect effects on Schistosoma parasites, their intermediate snail hosts, snail predators, and snail algal resources. We aimed to review and summarise the effects of these agrochemicals on schistosomiasis transmission dynamics. METHODS: We did a systematic review of agrochemical effects on the lifecycle of Schistosoma spp and fitted dose-response models to data regarding the association between components of the lifecycle and agrochemical concentrations. We incorporated these dose-response functions and environmentally relevant concentrations of agrochemicals into a mathematical model to estimate agrochemical effects on schistosomiasis transmission. Dose-response functions were used to estimate individual agrochemical effects on estimates of the agrochemically influenced basic reproduction number, R0, for Schistosoma haematobium. We incorporated time series of environmentally relevant agrochemical concentrations into the model and simulated mass drug administration control efforts in the presence of agrochemicals. FINDINGS: We derived 120 dose-response functions describing the effects of agrochemicals on schistosome lifecycle components. The median estimate of the basic reproduction number under agrochemical-free conditions, was 1·65 (IQR 1·47-1·79). Agrochemical effects on estimates of R0 for S haematobium ranged from a median three-times increase (R0 5·05, IQR 4·06-5·97) to transmission elimination (R0 0). Simulations of transmission dynamics subject to interacting annual mass drug administration and agrochemical pollution yielded a median estimate of 64·82 disability-adjusted life-years (DALYs) lost per 100 000 people per year (IQR 62·52-67·68) attributable to atrazine use. In areas where aquatic arthropod predators of intermediate host snails suppress transmission, the insecticides chlorpyrifos (6·82 DALYs lost per 100 000 people per year, IQR 4·13-8·69) and profenofos (103·06 DALYs lost per 100 000 people per year, IQR 89·63-104·90) might also increase the disability burden through their toxic effects on arthropods. INTERPRETATION: Expected environmental concentrations of agrochemicals alter schistosomiasis transmission through direct and indirect effects on intermediate host and parasite densities. As industrial agricultural practices expand in areas where schistosomiasis is endemic, strategies to prevent increases in transmission due to agrochemical pollution should be developed and pursued. FUNDING: National Science Foundation, National Institutes of Health.

LETHAL AND SUBLETHAL AMPHIBIAN HOST RESPONSES TO BATRACHOCHYTRIUM DENDROBATIDIS EXPOSURE ARE DETERMINED BY THE ADDITIVE INFLUENCE OF HOST RESOURCE AVAILABILITY.

Host species may differ in their responses to pathogen exposures based on host energy reserves, which could be important for long-term trends in host population growth. Batrachochytrium dendrobatidis (BD) is a pathogen associated with amphibian population declines but also occurs without causing mass mortalities. The impact of BD in populations without associated declines is not well understood, and food abundance could play a role in determining the magnitude of its effects. We exposed American toad (Anaxyrus americanus), northern leopard frog (Lithobates pipiens), and cricket frog (Acris blanchardi) metamorphs to BD under low or high food treatments. Overall, anuran species responded differently to BD exposure and the combined effect of BD exposure and food abundance was additive. American toad survival was lowered by BD exposure and low food availability. Based on these results, we developed a population model for American toads to estimate how reductions in survival could influence population growth. We found that BD could reduce population growth by 14% with high food availability and 21% with low food availability. In contrast, survival of northern leopard frogs was high across all treatments, but their growth was negatively impacted by the additive effects of BD exposure and low food availability. Cricket frog growth and survival were unaffected by BD exposure, suggesting that this species is not sensitive to the effects of this pathogen in terms of growth and survival across environments of different quality in the time period examined. Our results showed that low food availability additively increased the species-specific lethal and sublethal impacts of BD on hosts, which could have implications for long-term host population dynamics.

Evaluating improvements to exposure estimates from fate and transport models by incorporating environmental sampling effort and contaminant use.

Widespread chemical contamination represents one of the largest threats of the Anthropocene. The Pesticide in Water Calculator (PWC) is a fate and transport model used by the Environmental Protection Agency and Health Canada to estimate pesticide exposures in lentic freshwater ecosystems and make pesticide registration decisions. Here, we show that maximum measured concentrations of 31% of herbicides and 42% of insecticides exceeded maximum estimated environmental concentrations (EECs) produced by the PWC, suggesting that EECs often do not represent worst-case exposure as they have been purported to do. Based on this observation, we generated statistical models using EECs and over 600,000 field measurements of 31 common insecticides and herbicides to document if the congruence of EECs and maximum field measurements could be improved by accounting for environmental sampling effort (number of times a pesticide is sampled) and contaminant application, factors commonly ignored in most fate and transport models. For lentic systems, variance in pesticide field measurements explained by EECs increased by 50% when sampling effort was included. For lotic systems, variance explained increased by only 4%, most likely because lotic systems are sampled over 4.9 times as much as lentic systems. Including use more than doubled the ability of the EECs to predict maximum pesticides concentrations in lentic systems. Our results suggest that exposure characterization in risk assessment can likely be improved by considering sampling effort and use, thus providing more defensible environmental standards and regulations.

Effects of pesticides on exposure and susceptibility to parasites can be generalised to pesticide class and type in aquatic communities.

Pesticide pollution can alter parasite transmission, but scientists are unaware if effects of pesticides on parasite exposure and host susceptibility (i.e. infection risk given exposure) can be generalised within a community context. Using replicated temperate pond communities, we evaluate effects of 12 pesticides, nested in four pesticide classes (chloroacetanilides, triazines, carbamates organophosphates) and two pesticide types (herbicides, insecticides) applied at standardised environmental concentrations on larval amphibian exposure and susceptibility to trematode parasites. Most of the variation in exposure and susceptibility occurred at the level of pesticide class and type, not individual compounds. The organophosphate class of insecticides increased snail abundance (first intermediate host) and thus trematode exposure by increasing mortality of snail predators (top-down mechanism). While a similar pattern in snail abundance and trematode exposure was observed with triazine herbicides, this effect was driven by increases in snail resources (periphytic algae, bottom-up mechanism). Additionally, herbicides indirectly increased host susceptibility and trematode infections by (1) increasing time spent in susceptible early developmental stages and (2) suppressing tadpole immunity. Understanding generalisable effects associated with contaminant class and type on transmission is critical in reducing complexities in predicting disease dynamics in at-risk host populations.

High juvenile mortality in amphibians during overwintering related to fungal pathogen exposure.

The result of pathogen exposures may depend upon trade-offs in energetic demands for immune responses against host growth and survival. Environmental conditions may influence these trade-offs by affecting host size, or trade-offs may change across seasons, altering impacts of pathogens. We exposed northern leopard frog Lithobates pipiens tadpoles to different larval environments (low leaf litter, high density of conspecifics, atrazine, caged fish, or controls) that influenced size at metamorphosis. Subsequently, we exposed metamorphs to Batrachochytrium dendrobatidis (Bd), a fungal pathogen, just after metamorphosis and/or prior to overwintering 12 wk later. Bd exposure dramatically reduced survival during overwintering, with the strongest effects when hosts were exposed at both time points. Larval environments resulted in differences in host size. Those exposed to caged fish were 2.5 times larger than the smallest (those exposed to high density of conspecifics), but larval environment did not influence Bd effects on growth and survival. The largest frogs exposed to caged fish had greater survival through overwintering, but in the absence of Bd. We built stage-structured models to evaluate if overwinter mortality from Bd is capable of having effects on host populations. Our models suggest that Bd exposure after metamorphosis or before overwintering can reduce population growth rates. Our study demonstrates that hosts suffer little effects of Bd exposures following metamorphosis and that small body size did not hamper growth and survival. Instead, we provide evidence that winter mortality from Bd exposure is capable of reducing population sizes, providing a plausible mechanism for amphibian declines in temperate regions.

Host size influences the effects of four isolates of an amphibian chytrid fungus.

Understanding factors that influence host-pathogen interactions is key to predicting outbreaks in natural systems experiencing environmental change. Many amphibian population declines have been attributed to an amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). While this fungus is widespread, not all Bd-positive populations have been associated with declines, which could be attributed to differences in pathogen virulence or host susceptibility. In a laboratory experiment, we examined the effects of Bd isolate origin, two from areas with Bd-associated amphibian population declines (El Copé, Panama, and California, USA) and two from areas without Bd-related population declines (Ohio and Maine, USA), on the terrestrial growth and survival of American toad (Anaxyrus americanus) metamorphs reared in larval environments with low or high intraspecific density. We predicted that (1) Bd isolates from areas experiencing declines would have greater negative effects than Bd isolates from areas without declines, and (2) across all isolates, growth and survival of smaller toads from high-density larval conditions would be reduced by Bd exposure compared to larger toads from low-density larval conditions. Our results showed that terrestrial survival was reduced for smaller toads exposed to Bd with variation in the response to different isolates, suggesting that smaller size increased susceptibility to Bd. Toads exposed to Bd gained less mass, which varied by isolate. Bd isolates from areas with population declines, however, did not have more negative effects than isolates from areas without recorded declines. Most strikingly, our study supports that host condition, measured by size, can be indicative of the negative effects of Bd exposure. Further, Bd isolates' impact may vary in ways not predictable from place of origin or occurrence of disease-related population declines. This research suggests that amphibian populations outside of areas experiencing Bd-associated declines could be impacted by this pathogen and that the size of individuals could influence the magnitude of Bd's impact.

The effects of the amphibian chytrid fungus, insecticide exposure, and temperature on larval anuran development and survival.

Chytridiomycosis, a disease caused by Batrachochytrium dendrobatidis (Bd), has been implicated as a cause of amphibian declines. Susceptibility may be influenced by environmental factors that suppress the immune response. The authors conducted a laboratory study to examine the effect of temperature, insecticide exposure, and Bd exposure during larval anuran development. The authors examined the consequences of exposure to Bd, an insecticide (carbaryl or malathion), and static or fluctuating temperature (15 °C, 20 °C, 25 °C, or 15 °C to 25 °C 72-h flux) on larval development through metamorphosis of the Pacific treefrog (Pseudacris regilla). High and fluctuating temperature had negative effects on survival in the presence of Bd. Insecticides inhibited the effects of Bd; time to tail resorption of Pacific treefrogs decreased when tadpoles were exposed to carbaryl. The present study indicates that abiotic factors may play a role in the host-pathogen interactions in this system.

Effects of amphibian chytrid fungus exposure on American toads in the presence of an insecticide.

Abiotic factors such as pesticides may alter the impact of a pathogen on hosts, which could have implications for host-pathogen interactions and may explain variation in disease outbreaks in nature. In the present laboratory experiment, American toad (Anaxyrus americanus) metamorphs were exposed to the amphibian chytrid fungal pathogen Batrachochytrium dendrobatidis (Bd) and environmentally relevant concentrations of the insecticide malathion to determine whether malathion altered the effects of Bd exposure on growth and survival of toad metamorphs. Exposure to Bd significantly decreased survival over the 51 d of the experiment, suggesting that Bd could reduce recruitment into the terrestrial life stage when exposure occurs at metamorphosis. Malathion did not impact survival, but a 12-h exposure at metamorphosis significantly reduced terrestrial growth. Toads that were exposed to both Bd and malathion showed a nonsignificant trend toward the smallest growth compared with other treatments. The present study suggests that Bd may pose a threat to American toads even though population declines have not been observed for this species; in addition, the presence of both the insecticide malathion and Bd could reduce terrestrial growth, which could have implications for lifetime fitness and suggests that environmental factors could play a role in pathogen impacts in nature.

Effects of pesticide exposure and the amphibian chytrid fungus on gray treefrog (Hyla chrysoscelis) metamorphosis.

Pesticides are detectable in most aquatic habitats and have the potential to alter host-pathogen interactions. The amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), has been associated with amphibian declines around the world. However, Bd-associated declines are more prominent in some areas, despite nearly global distribution of Bd, suggesting other factors contribute to disease outbreaks. In a laboratory study, the authors examined the effects of 6 different isolates of Bd in the presence or absence of a pesticide (the insecticide carbaryl or the fungicide copper sulfate) to recently hatched Cope's gray treefrog (Hyla chrysoscelis) tadpoles reared through metamorphosis. The authors found the presence or absence of pesticides differentially altered the mass at metamorphosis of tadpoles exposed to different Bd isolates, suggesting that isolate could influence metamorphosis but not in ways expected based on origin of the isolate. Pesticide exposure had the strongest impact on metamorphosis of all treatment combinations. Whereas copper sulfate exposure reduced the length of the larval period, carbaryl exposure had apparent positive effects by increasing mass at metamorphosis and lengthening larval period, which adds to evidence that carbaryl can stimulate development in counterintuitive ways. The present study provides limited support to the hypothesis that pesticides can alter the response of tadpoles to isolates of Bd and that the insecticide carbaryl can alter developmental decisions.