Opposing life history strategies allow grass shrimp parasites to avoid a conflict of interest.

A conflict of interest occurs when parasites manipulate the behavior of their host in contradictory ways to achieve different goals. In grass shrimp (Palaemonetes pugio), trematode parasites that use shrimp as an intermediate host cause the shrimp to be more active than usual around predators, whereas bopyrid isopod parasites that use shrimp as a final host elicit the opposite response. Since these parasites are altering the host's behavior in opposing directions, a conflict of interest would occur in co-infected shrimp. Natural selection should favor attempts to resolve this conflict through avoidance, killing, or sabotage. In a field survey of shrimp populations in four tidal creeks in the Cape Fear River, we found a significant negative association between the two parasites. Parasite abundance was negatively correlated in differently sized hosts, suggesting avoidance as a mechanism. Subsequent mortality experiments showed no evidence of early death of co-infected hosts. In behavior trials, co-infected shrimp did not show significantly different behavior from singly infected or uninfected shrimp, suggesting that neither parasite sabotages the manipulation of the other. Taken together, our results suggest that rather than sabotaging or killing one another, bopyrid and trematode parasites tend to infect differently sized hosts, thus avoiding a conflict and confirming the importance of testing assumptions in natural contexts.

Predation cues amplify the effects of parasites on the personality of a keystone grazer.

Parasites can alter species interactions either by modifying infected host behaviour or by influencing behavioural responses in uninfected individuals. Salt marsh ecosystems are characterized by a predator-prey interaction between the keystone grazer, Littoraria irrorata, and its main predator, Callinectes sapidus, both integral players in mediating the productivity of these habitats. Littoraria also acts as the first intermediate host for at least four species of digenetic trematode. Parasite infection has been shown to decrease grazing and climbing in populations of Littoraria, although effects on infected host response to predators have not been investigated. Moreover, how infection might increase or decrease among-individual variation in behaviour (i.e. animal personality) is still unknown. Here we ask how trematode infection affects the expression of boldness in the anti-predator responses of L. irrorata in both the absence and presence of a predator cue. We find that individual boldness varies substantially, and repeatability tends to increase as the number of stressors increases, with infected individuals exposed to a predator cue showing the strongest expression of behavioural types. Parasitism amplifies this effect, although the parasite itself does not appear to directly induce behavioural changes: infected snails show no evidence of decreased climbing or differences in refuge use as compared to their uninfected counterparts. Infection might therefore drive the expression of condition-dependent personality differences evident only under high-risk conditions. Group infection status strongly influenced behavioural reaction norms: uninfected individuals grouped with an infected snail were more responsive to predation risk, exhibiting increased climbing behaviour and spending less time in the water. Here parasites are influencing personality indirectly by inducing avoidance behaviours in healthy individuals, although only in high-risk environments. The potential for exposure to parasites and predators fluctuates greatly across marsh ecosystems. Given the ecological importance of this predator-prey relationship, trematode infection can act as an important, although indirect, determinant of overall salt marsh community structure, health and function.

Ecological and socioeconomic factors associated with the human burden of environmentally mediated pathogens: a global analysis.

BACKGROUND: Billions of people living in poverty are at risk of environmentally mediated infectious diseases-that is, pathogens with environmental reservoirs that affect disease persistence and control and where environmental control of pathogens can reduce human risk. The complex ecology of these diseases creates a global health problem not easily solved with medical treatment alone. METHODS: We quantified the current global disease burden caused by environmentally mediated infectious diseases and used a structural equation model to explore environmental and socioeconomic factors associated with the human burden of environmentally mediated pathogens across all countries. FINDINGS: We found that around 80% (455 of 560) of WHO-tracked pathogen species known to infect humans are environmentally mediated, causing about 40% (129 488 of 359 341 disability-adjusted life years) of contemporary infectious disease burden (global loss of 130 million years of healthy life annually). The majority of this environmentally mediated disease burden occurs in tropical countries, and the poorest countries carry the highest burdens across all latitudes. We found weak associations between disease burden and biodiversity or agricultural land use at the global scale. In contrast, the proportion of people with rural poor livelihoods in a country was a strong proximate indicator of environmentally mediated infectious disease burden. Political stability and wealth were associated with improved sanitation, better health care, and lower proportions of rural poverty, indirectly resulting in lower burdens of environmentally mediated infections. Rarely, environmentally mediated pathogens can evolve into global pandemics (eg, HIV, COVID-19) affecting even the wealthiest communities. INTERPRETATION: The high and uneven burden of environmentally mediated infections highlights the need for innovative social and ecological interventions to complement biomedical advances in the pursuit of global health and sustainability goals. FUNDING: Bill & Melinda Gates Foundation, National Institutes of Health, National Science Foundation, Alfred P. Sloan Foundation, National Institute for Mathematical and Biological Synthesis, Stanford University, and the US Defense Advanced Research Projects Agency.

Timescale reverses the relationship between host density and infection risk.

Host density shapes infection risk through two opposing phenomena. First, when infective stages are subdivided among multiple hosts, greater host densities decrease infection risk through 'safety in numbers'. Hosts, however, represent resources for parasites, and greater host availability also fuels parasite reproduction. Hence, host density increases infection risk through 'density-dependent transmission'. Theory proposes that these phenomena are not disparate outcomes but occur over different timescales. That is, higher host densities may reduce short-term infection risk, but because they support parasite reproduction, may increase long-term risk. We tested this theory in a zooplankton-disease system with laboratory experiments and field observations. Supporting theory, we found that negative density-risk relationships (safety in numbers) sometimes emerged over short timescales, but these relationships reversed to 'density-dependent transmission' within two generations. By allowing parasite numerical responses to play out, time can shift the consequences of host density, from reduced immediate risk to amplified future risk.

Evidence gaps and diversity among potential win-win solutions for conservation and human infectious disease control.

As sustainable development practitioners have worked to "ensure healthy lives and promote well-being for all" and "conserve life on land and below water", what progress has been made with win-win interventions that reduce human infectious disease burdens while advancing conservation goals? Using a systematic literature review, we identified 46 proposed solutions, which we then investigated individually using targeted literature reviews. The proposed solutions addressed diverse conservation threats and human infectious diseases, and thus, the proposed interventions varied in scale, costs, and impacts. Some potential solutions had medium-quality to high-quality evidence for previous success in achieving proposed impacts in one or both sectors. However, there were notable evidence gaps within and among solutions, highlighting opportunities for further research and adaptive implementation. Stakeholders seeking win-win interventions can explore this Review and an online database to find and tailor a relevant solution or brainstorm new solutions.

Environmental Persistence of the World's Most Burdensome Infectious and Parasitic Diseases.

Humans live in complex socio-ecological systems where we interact with parasites and pathogens that spend time in abiotic and biotic environmental reservoirs (e.g., water, air, soil, other vertebrate hosts, vectors, intermediate hosts). Through a synthesis of published literature, we reviewed the life cycles and environmental persistence of 150 parasites and pathogens tracked by the World Health Organization's Global Burden of Disease study. We used those data to derive the time spent in each component of a pathogen's life cycle, including total time spent in humans versus all environmental stages. We found that nearly all infectious organisms were "environmentally mediated" to some degree, meaning that they spend time in reservoirs and can be transmitted from those reservoirs to human hosts. Correspondingly, many infectious diseases were primarily controlled through environmental interventions (e.g., vector control, water sanitation), whereas few (14%) were primarily controlled by integrated methods (i.e., combining medical and environmental interventions). Data on critical life history attributes for most of the 150 parasites and pathogens were difficult to find and often uncertain, potentially hampering efforts to predict disease dynamics and model interactions between life cycle time scales and infection control strategies. We hope that this synthetic review and associated database serve as a resource for understanding both common patterns among parasites and pathogens and important variability and uncertainty regarding particular infectious diseases. These insights can be used to improve systems-based approaches for controlling environmentally mediated diseases of humans in an era where the environment is rapidly changing.

Monitoring the dead as an ecosystem indicator.

Dead animal biomass (carrion) is present in all terrestrial ecosystems, and its consumption, decomposition, and dispersal can have measurable effects on vertebrates, invertebrates, microbes, parasites, plants, and soil. But despite the number of studies examining the influence of carrion on food webs, there has been no attempt to identify how general ecological processes around carrion might be used as an ecosystem indicator. We suggest that knowledge of scavenging and decomposition rates, scavenger diversity, abundance, and behavior around carrion, along with assessments of vegetation, soil, microbe, and parasite presence, can be used individually or in combination to understand food web dynamics. Monitoring carrion could also assist comparisons of ecosystem processes among terrestrial landscapes and biomes. Although there is outstanding research needed to fully integrate carrion ecology and monitoring into ecosystem management, we see great potential in using carrion as an ecosystem indicator of an intact and functional food web.

The ecological consequences of a pandemic.

The COVID-19 pandemic has altered human behaviour in profound ways, prompting some to question whether the associated economic and social impacts might outweigh disease impacts. This fits into a burgeoning ecological paradigm suggesting that for both predator-prey and parasite-host interactions, non-consumptive effects (avoidance) can be orders of magnitude stronger than consumptive effects (sickness and death). Just as avoidance of predators and parasites imposes substantial costs on prey and hosts, altered behaviour to reduce the transmission of COVID-19 has impacted human fitness and wellbeing. But the effects of infectious disease avoidance do not stop there; non-consumptive effects of predators and parasites often trigger cascading indirect effects in natural systems. Similarly, shifts in human behaviour due to COVID-19 have triggered myriad indirect effects on species and the environment, which can be positive, negative or neutral. We urge researchers to recognize that the environmental impacts associated with lockdowns are indirect effects of the virus. In short, the global response to COVID-19 suggests that the non-consumptive effects of a pathogen, and resulting indirect effects, can be profound.

Concomitant Immunity and Worm Senescence May Drive Schistosomiasis Epidemiological Patterns: An Eco-Evolutionary Perspective.

In areas where human schistosomiasis is endemic, infection prevalence and egg output are known to rise rapidly through childhood, reach a peak at 8-15 years of age, and decline thereafter. A similar peak ("overshoot") followed by return to equilibrium infection levels sometimes occurs a year or less after mass drug administration. These patterns are usually assumed to be due to acquired immunity, which is induced by exposure, directed by the host's immune system, and develops slowly over the lifetime of the host. Other explanations that have been advanced previously include differential exposure of hosts, differential mortality of hosts, and progressive pathology. Here we review these explanations and offer a novel (but not mutually exclusive) explanation, namely that adult worms protect the host against larval stages for their own benefit ("concomitant immunity") and that worm fecundity declines with worm age ("reproductive senescence"). This explanation approaches schistosomiasis from an eco-evolutionary perspective, as concomitant immunity maximizes the fitness of adult worms by reducing intraspecific competition within the host. If correct, our hypothesis could have profound implications for treatment and control of human schistosomiasis. Specifically, if immunity is worm-directed, then treatment of long-standing infections comprised of old senescent worms could enable infection with new, highly fecund worms. Furthermore, our hypothesis suggests revisiting research on therapeutics that mimic the concomitant immunity-modulating activity of adult worms, while minimizing pathological consequences of their eggs. We emphasize the value of an eco-evolutionary perspective on host-parasite interactions.

Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission.

Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.

Indirect Effects Explain the Role of Parasites in Ecosystems.

Parasites are increasingly recognized as integral members of ecological communities, but their ecological effects remain less clear. Here, I propose that, to uncover the unique role of parasites, we must understand their indirect effects, which differ in important ways from those caused by predators. Similar to predators, parasites can cause density-mediated indirect effects (DMIEs) through their consumptive effects, and trait-mediated indirect effects (TMIEs) through their nonconsumptive effects; however, because they can consume a host without killing it, parasites can also trigger TMIEs through their consumptive effects. I consider the relative importance of each parasite-induced indirect interaction type and demonstrate their population-, community-, and ecosystem-level consequences. This paper contributes to recent efforts to unite predator-prey and parasite-host theory under a general consumer-resource framework.

Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos.

Environmental variation favors the evolution of phenotypic plasticity. For many species, we understand the costs and benefits of different phenotypes, but we lack a broad understanding of how plastic traits evolve across large clades. Using identical experiments conducted across North America, we examined prey responses to predator cues. We quantified five life-history traits and the magnitude of their plasticity for 23 amphibian species/populations (spanning three families and five genera) when exposed to no cues, crushed-egg cues, and predatory crayfish cues. Embryonic responses varied considerably among species and phylogenetic signal was common among the traits, whereas phylogenetic signal was rare for trait plasticities. Among trait-evolution models, the Ornstein-Uhlenbeck (OU) model provided the best fit or was essentially tied with Brownian motion. Using the best fitting model, evolutionary rates for plasticities were higher than traits for three life-history traits and lower for two. These data suggest that the evolution of life-history traits in amphibian embryos is more constrained by a species' position in the phylogeny than is the evolution of life history plasticities. The fact that an OU model of trait evolution was often a good fit to patterns of trait variation may indicate adaptive optima for traits and their plasticities.

Infectious Agents Trigger Trophic Cascades.

Most demonstrated trophic cascades originate with predators, but infectious agents can also cause top-down indirect effects in ecosystems. Here we synthesize the literature on trophic cascades initiated by infectious agents including parasitoids, pathogens, parasitic castrators, macroparasites, and trophically transmitted parasites. Like predators, infectious agents can cause density-mediated and trait-mediated indirect effects through their direct consumptive and nonconsumptive effects respectively. Unlike most predators, however, infectious agents are not fully and immediately lethal to their victims, so their consumptive effects can also trigger trait-mediated indirect effects. We find that the frequency of trophic cascades reported for different consumer types scales with consumer lethality. Furthermore, we emphasize the value of uniting predator-prey and parasite-host theory under a general consumer-resource framework.

Effect of Simultaneous Amphibian Exposure to Pesticides and an Emerging Fungal Pathogen, Batrachochytrium dendrobatidis.

Amphibian declines have been linked to numerous factors, including pesticide use and the fungal pathogen Batrachochytrium dendrobatidis (Bd). Moreover, research has suggested a link between amphibian sensitivity to Bd and pesticide exposure. We simultaneously exposed postmetamorphic American toads (Anaxyrus americanus), western toads (A. boreas), spring peepers (Pseudacris crucifer), Pacific treefrogs (P. regilla), leopard frogs (Lithobates pipiens), and Cascades frogs (Rana cascadae) to a factorial combination of two pathogen treatments (Bd+, Bd-) and four pesticide treatments (control, ethanol vehicle, herbicide mixture, and insecticide mixture) for 14 d to quantify survival and infection load. We found no interactive effects of pesticides and Bd on anuran survival and no effects of pesticides on infection load. Mortality following Bd exposure increased in spring peepers and American toads and was dependent upon snout-vent length in western toads, American toads, and Pacific treefrogs. Previous studies reported effects of early sublethal pesticide exposure on amphibian Bd sensitivity and infection load at later life stages, but we found simultaneous exposure to sublethal pesticide concentrations and Bd had no such effect on postmetamorphic juvenile anurans. Future research investigating complex interactions between pesticides and Bd should employ a variety of pesticide formulations and Bd strains and follow the effects of exposure throughout ontogeny.

Effects of nutrient supplementation on host-pathogen dynamics of the amphibian chytrid fungus: a community approach.

Anthropogenic stressors may influence hosts and their pathogens directly or may alter host-pathogen dynamics indirectly through interactions with other species. For example, in aquatic ecosystems, eutrophication may be associated with increased or decreased disease risk. Conversely, pathogens can influence community structure and function and are increasingly recognised as important members of the ecological communities in which they exist.In outdoor mesocosms, we experimentally manipulated nutrients (nitrogen and phosphorus) and the presence of a fungal pathogen, Batrachochytrium dendrobatidis (Bd), and examined the effects on Bd abundance on larval amphibian hosts (Pseudacris regilla: Hylidae), amphibian traits and community dynamics. We predicted that resource supplementation would mitigate negative effects of Bd on tadpole growth and development and that indirect effects of treatments would propagate through the community.Nutrient additions caused changes in algal growth, which benefitted tadpoles through increased mass, development and survival. Bd-exposed tadpoles metamorphosed sooner than unexposed individuals, but their mass at metamorphosis was not affected by Bd exposure. We detected additive rather than interactive effects of nutrient supplementation and Bd in this experiment.Nutrient supplementation was not a significant predictor of infection load of larval amphibians. However, a structural equation model revealed that resource supplementation and exposure of amphibians to Bd altered the structure of the aquatic community. This is the first demonstration that sublethal effects of Bd on amphibians can alter aquatic community dynamics.

Effects of Pesticide Mixtures on Host-Pathogen Dynamics of the Amphibian Chytrid Fungus.

Anthropogenic and natural stressors often interact to affect organisms. Amphibian populations are undergoing unprecedented declines and extinctions with pesticides and emerging infectious diseases implicated as causal factors. Although these factors often co-occur, their effects on amphibians are usually examined in isolation. We hypothesized that exposure of larval and metamorphic amphibians to ecologically relevant concentrations of pesticide mixtures would increase their post-metamorphic susceptibility to the fungus Batrachochytrium dendrobatidis (Bd), a pathogen that has contributed to amphibian population declines worldwide. We exposed five anuran species (Pacific treefrog, Pseudacris regilla; spring peeper, Pseudacris crucifer; Cascades frog, Rana cascadae; northern leopard frog, Lithobates pipiens; and western toad, Anaxyrus boreas) from three families to mixtures of four common insecticides (chlorpyrifos, carbaryl, permethrin, and endosulfan) or herbicides (glyphosate, acetochlor, atrazine, and 2,4-D) or a control treatment, either as tadpoles or as newly metamorphic individuals (metamorphs). Subsequently, we exposed animals to Bd or a control inoculate after metamorphosis and compared survival and Bd load. Bd exposure significantly increased mortality in Pacific treefrogs, spring peepers, and western toads, but not in Cascades frogs or northern leopard frogs. However, the effects of pesticide exposure on mortality were negligible, regardless of the timing of exposure. Bd load varied considerably across species; Pacific treefrogs, spring peepers, and western toads had the highest loads, whereas Cascades frogs and northern leopard frogs had the lowest loads. The influence of pesticide exposure on Bd load depended on the amphibian species, timing of pesticide exposure, and the particular pesticide treatment. Our results suggest that exposure to realistic pesticide concentrations has minimal effects on Bd-induced mortality, but can alter Bd load. This result could have broad implications for risk assessment of amphibians; the outcome of exposure to multiple stressors may be unpredictable and can differ between species and life stages.

Trophic dynamics in an aquatic community: interactions among primary producers, grazers, and a pathogenic fungus.

Free-living stages of parasites are consumed by a variety of predators, which might have important consequences for predators, parasites, and hosts. For example, zooplankton prey on the infectious stage of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), a pathogen responsible for amphibian population declines and extinctions worldwide. Predation on parasites is predicted to influence community structure and function, and affect disease risk, but relatively few studies have explored its consequences empirically. We investigated interactions among Rana cascadae tadpoles, zooplankton, and Bd in a fully factorial experiment in outdoor mesocosms. We measured growth, development, survival, and infection of amphibians and took weekly measurements of the abundance of zooplankton, phytoplankton (suspended algae), and periphyton (attached algae). We hypothesized that zooplankton might have positive indirect effects on tadpoles by consuming Bd zoospores and by consuming phytoplankton, thus reducing the shading of a major tadpole resource, periphyton. We also hypothesized that zooplankton would have negative effects on tadpoles, mediated by competition for algal resources. Mixed-effects models, repeated-measures ANOVAs, and a structural equation model revealed that zooplankton significantly reduced phytoplankton but had no detectable effects on Bd or periphyton. Hence, the indirect positive effects of zooplankton on tadpoles were negligible when compared to the indirect negative effect mediated by competition for phytoplankton. We conclude that examination of host-pathogen dynamics within a community context may be necessary to elucidate complex community dynamics.

Larval exposure to predator cues alters immune function and response to a fungal pathogen in post-metamorphic wood frogs.

For the past several decades, amphibian populations have been decreasing around the globe at an unprecedented rate. Batrachochytrium dendrobatidis (Bd), the fungal pathogen that causes chytridiomycosis in amphibians, is contributing to amphibian declines. Natural and anthropogenic environmental factors are hypothesized to contribute to these declines by reducing the immunocompetence of amphibian hosts, making them more susceptible to infection. Antimicrobial peptides (AMPs) produced in the granular glands of a frog's skin are thought to be a key defense against Bd infection. These peptides may be a critical immune defense during metamorphosis because many acquired immune functions are suppressed during this time. To test if stressors alter AMP production and survival of frogs exposed to Bd, we exposed wood frog (Lithobates sylvaticus) tadpoles to the presence or absence of dragonfly predator cues crossed with a single exposure to three nominal concentrations of the insecticide malathion (0, 10, or 100 parts per billion [ppb]). We then exposed a subset of post-metamorphic frogs to the presence or absence of Bd zoospores and measured frog survival. Although predator cues and malathion had no effect on survival or size at metamorphosis, predator cues increased the time to metamorphosis by 1.5 days and caused a trend of a 20% decrease in hydrophobic skin peptides. Despite this decrease in peptides determined shortly after metamorphosis, previous exposure to predator cues increased survival in both Bd-exposed and unexposed frogs several weeks after metamorphosis. These results suggest that exposing tadpoles to predator cues confers fitness benefits later in life.

The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses.

Population losses and extinctions of species are occurring at unprecedented rates, as exemplified by declines and extinctions of amphibians worldwide. However, studies of amphibian population declines generally do not address the complexity of the phenomenon or its implications for ecological communities, focusing instead on single factors affecting particular amphibian species. We argue that the causes for amphibian population declines are complex; may differ among species, populations, and life stages within a population; and are context dependent with multiple stressors interacting to drive declines. Because amphibians are key components of communities, we emphasize the importance of investigating amphibian declines at the community level. Selection pressures over evolutionary time have molded amphibian life history characteristics, such that they may remain static even in the face of strong, recent human-induced selection pressures.