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.
The results underscore the take‐home message that environmental dependence of free‐living parasites is important in predicting disease dynamics.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Phenotypic plasticity is the ability of an organism to alter its phenotype in response to environmental cues. This can be adaptive if the cues are reliable predictors of impending conditions and the ...alterations enhance the organism's ability to capitalize on those conditions. However, since traits do not exist in isolation but as part of larger interdependent systems of traits (phenotypic integration), trade‐offs between correlated plastic traits can make phenotypic plasticity non‐ or maladaptive. We examine this problem in the seasonally plastic wing melanism of a pierid (Order Lepidoptera, Family Pieridae) butterfly, Pieris rapae L. Several wing pattern traits are more melanized in colder than in warmer seasons, resulting in effective thermoregulation through solar absorption. However, other wing pattern traits, the spots, are less melanized during colder seasons than in warmer seasons. Although spot plasticity may be adaptive, reduced melanism of these spots could also be explained by resource‐based trade‐offs. Theory predicts that traits involved in resource‐based trade‐offs will be positively correlated when variation among individuals in resource acquisition is greater than variation among individuals in resource allocation strategies, and negatively correlated when variation in allocation is greater than variation in acquisition. Using data from both field studies and laboratory studies that manipulate dietary tyrosine, a melanin precursor, we show that when allocation to thermoregulatory melanism (ventral hindwing, and basal dorsal fore‐ and hindwing “shading”) varies substantially this trait is negatively correlated with spot melanism. However, when there is less variation in allocation to thermoregulatory melanism we find these traits to be positively correlated; these findings are consistent with the resource‐based trade‐off hypothesis, which may provide a non‐ or maladaptive hypothesis to explain spot plasticity. We also show that increased dietary tyrosine results in increased spot melanism under some conditions, supporting the more general idea that melanism may involve resource‐based costs.
Predictable seasonal plasticity may be adaptive. However, traits that are developmentally correlated with other plastic traits may change in predictable but non‐adaptive ways. We show patterns of butterfly wing melanism plasticity that are consistent with resource‐based trade offs and may not be adaptive.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Anthropogenic change is contributing to the rise in emerging infectious diseases, which are significantly correlated with socioeconomic, environmental and ecological factors
. Studies have shown that ...infectious disease risk is modified by changes to biodiversity
, climate change
, chemical pollution
, landscape transformations
and species introductions
. 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.
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.
The naïve host syndrome hypothesis suggests that pathogens are able to easily invade and become deadly to novel hosts because of a lack of co‐evolutionary history, whereas the local adaptation hypothesis suggests that pathogens are better able to invade local hosts because of their co‐evolutionary history, but rarely do studies on these two hypotheses cite one another or acknowledge their ostensibly mixed messages. By combining a continental‐scale, factorial, common garden experiment with a global‐scale meta‐analysis, each on the amphibian‐chytrid fungus host‐pathogen system, we show that local host‐pathogen interactions typically resulted in higher host mortality, greater infection success, and higher pathogen loads, but that there was substantial variation in novel host‐pathogen outcomes and thus moving pathogens around the planet increases the likelihood of exposure to particularly virulent pathogen strains and particularly deadly host‐pathogen combination. Therefore, we provide support for both the local adaptation and naïve host syndrome hypotheses, highlight how the two hypotheses are complementary rather than conflicting, and emphasize the need for greater integration of these hypotheses and their associated semi‐disparate literature.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
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.
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.
Survival of amphibian hosts of smaller size is reduced with exposure to an infectious fungal pathogen implicated in worldwide amphibian population declines, Batrachochytrium dendrobatidis (Bd), suggesting that small size increased susceptibility. Host condition, as measured by size, may be an important indicator of the effects of Bd.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Pathogens can have a range of effects on organisms across environmental gradients; although lethal effects may receive greater attention, sublethal impacts can have important population- and ...community-level impacts. In this laboratory study, we examined the effects of exposure to the amphibian chytrid fungus (Batrachochytrium dendrobatidis Bd) on Northern Leopard Frog (Lithobates pipiens) metamorphs that had been reared in the presence or absence of crayfish (Orconectes rusticus) predators in aquatic environments to determine whether prior predator exposure influenced the effect of Bd on terrestrial growth and survival of frogs. Although Bd exposure following metamorphosis did not impact Northern Leopard Frog survival, exposure did significantly reduce terrestrial growth, indicating that Bd exposure can have consequences that can indirectly impact populations, because size of amphibians is positively correlated with overwinter survival and fecundity. Exposure to predators during larval development, however, did not alter the impact of Bd exposure at metamorphosis on Northern Leopard Frogs. Our study suggests the Bd pathogen associated with global amphibian declines can have important sublethal impacts and play a role in population dynamics even when disease outbreaks do not occur.
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BFBNIB, IZUM, KILJ, NMLJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
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.
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.
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.
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.
National Science Foundation, National Institutes of Health.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
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