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Civitello, D. J.

Publications and source records attributed to Civitello, D. J..

12 recordsLinked to original sources

From protection to amplification: Imperfect chytridiomycosis prophylaxis increases infections in wild amphibians

Wildlife vaccination could become a powerful strategy to mitigate disease-induced biodiversity losses, yet many vaccines for wildlife diseases provide only limited protection. Notably, tools to control the fungal pathogen Batrachochytrium dendrobatidis (Bd) are urgently needed for amphibian conservation. Laboratory experiments have demonstrated that prophylactic exposure to Bd metabolites increases host resistance, significantly reducing infection intensity in amphibians subsequently challenged with live Bd. Because Bd metabolites are non-infectious and applied topically, this treatment has potential to be administered to waterbodies to vaccinate and protect amphibians. We developed an agent-based model that indicated imperfect vaccination could reduce or amplify Bd infections at the population level, depending on degree of enhanced resistance or tolerance. Utilizing a Before-After-Control-Impact design with ten years of data, we conducted an ecosystem-level trial where we applied low levels of Bd metabolites or a sham control treatment to ponds in California and subsequently quantified Bd prevalence and infection intensity in metamorphosing Pacific chorus frogs (Pseudacris regilla). Unexpectedly, infection intensity was significantly greater in treated ponds relative to control ponds following metabolite addition. Additional model simulations indicated that this could occur via two mechanisms: (1) if treatment greatly increased tolerance alone or in combination with smaller increases in resistance, or (2) if a deleterious environmental interaction caused the treatment to increase susceptibility, rather than promote resistance. Future research is needed to determine whether tolerance or environmental factors drove heightened Bd infection intensities in this field trial to identify contexts in which this treatment can be used as a conservation tool. Significance statementAlthough wildlife vaccination is increasingly explored as a strategy to mitigate disease-induced population declines, many available vaccines provide limited protection, requiring careful consideration to design successful conservation campaigns. Here, we use both an eco-epidemiological model and field manipulation experiment to assess the effectiveness of an imperfect prophylactic treatment (akin to a prototype vaccine) for chytridiomycosis, a disease implicated in the massive decline of amphibian biodiversity worldwide. We unexpectedly found that prophylaxis-treated ponds had higher pathogen loads relative to control populations and models suggest this could result from enhanced tolerance or an adverse environmental interaction.

ecology↗

Apparent failure and cryptic success of disease control via intermediate host population reduction: Density dependence in copepods has implications for Guinea worm disease transmission

All populations experience density dependence, lest they grow infinitely. However, elucidating what forms of density dependence act most strongly for a given species remains incredibly challenging. Identifying the mechanisms that regulate population density is particularly relevant to pest control, which often causes high mortality, reducing population density but enabling recovery when survivors are freed from intraspecific competition and density dependent vital rates (e.g., birth, death, and maturation rates). Understanding these demographic responses is critical for effective pest management, especially when specific life stages of pests differ in the harm they cause. Guinea worm disease (GWD) is a neglected tropical disease with an obligate copepod intermediate host, and importantly, only large-bodied copepods can be infected with GW parasites. GW disease has been the target of control for several decades, with main management strategies including the use of a chemical larvicide, Abate, which is applied to water bodies to cull copepod populations. Despite the wide application of Abate in GW endemic countries, little is known about long-term copepod population dynamics in response to Abate. Thus, we evaluated this mortality-based management of intermediate copepod hosts to control GW transmission, combining mathematical models with a population dynamics experiment designed to mimic Abate pesticide control methods across a range of intensities. Despite initial reductions in both total and stage specific population densities, copepod populations recovered so rapidly that control appeared to fail, enabled by extremely fast maturation rates in low-density populations. Much to our surprise, model simulations of GW transmission showed that although total and stage-specific densities rebounded, infectious adult copepods --the proximate cause of infections--were strongly suppressed, indicating cryptic success. This effect was enabled by the 15-day developmental period of GW larvae within copepods, which blocks the accumulation of infectious copepods between interventions. Ultimately, this study highlights the importance of understanding mechanisms of density dependence when designing and optimizing pest control interventions, as well as interpreting counterintuitive consequences of interventions.

ecology↗

Mapping of snail intermediate host habitat reveals variability in schistosome and nonschistosome trematode transmission in endemic settings

BackgroundThere is growing recognition that mass drug administration must be complemented with environmental interventions to interrupt schistosomiasis transmission. Accurate mapping of snails and schistosome parasite distribution is critical to identify foci of human exposure and prioritize sites for interventions. MethodologyWe conducted longitudinal environmental surveys of snails and schistosomes in 467 waterbodies across 86 villages in northwestern Tanzania to describe spatial and temporal variation in snail and schistosome parasites presence and identify relevant underlying predictors. We conducted time constrained net sampling of Bulinus snails from vegetation, sediments, and floating objects and then examined all collected snails for patent infections. Principal findingsA total of 43,272 Bulinus snails were collected across the three visits to each waterbody spanning November 2020 - August 2021, and we conducted statistical analyses on the latter two visits with more in-depth surveys (25,052 snails). We found patent schistosome infections in 0.87% of snails, 9.8% of waterbodies, and 31% of villages in all six districts. Variance decomposition indicated that variation among waterbodies was associated with variation in snail presence and the prevalence of schistosomes and nonschistosome parasites, whereas variation among villages and districts was not. Snail presence was highest in March-May a period of heavy rains, but otherwise not associated with waterbody characteristics. Waterbodies permitting cattle use had significantly higher prevalence of schistosomes than those permitting only human use. Nonschistosome parasites were more prevalent in June to September the dry season but were not associated with other waterbody characteristics. Waterbody permanence and distance to the nearest primary school were not associated with snails or parasites. Conclusions/significanceThis study revealed substantial variation in snails, schistosome and nonschistosome abundance at local (waterbody) scales, and it suggests links between community-driven water use decisions and schistosome transmission. The identification of local drivers of snail and schistosome abundance level and transmission factors at waterbody scale can complement studies across larger scales to shed light on transmission hotspots and guide the development of targeted interventions for schistosomiasis control. Author summaryCurrently there is increasing need to supplement mass drug administration with environmental interventions by identifying potential sites for human exposure to disrupt schistosomiasis transmission. Here we focus on environmental surveys to determine leading factors for presence and sequential variation in snails and schistosomes. Using a timed sampling strategy, snail vectors were collected and examined for infections. We screened snails collected from November 2020 to August 2021 and found variation among waterbodies in snail presence and infections of schistosomes and nonschistosome parasites. This variation was not observed at village and district levels. High abundance of snails was observed in March to May during heavy rainfall but not connected with waterbody distinctiveness. Waterbodies used by cattle had higher prevalence of schistosomes compared to waterbodies used by humans alone. Nonschistosomes were higher in June to September the dry season but not related to waterbody characteristics. Although chemotherapy reduces schistosomiasis burden, our results suggest that identification of transmission sites at waterbody scale could aid development of targeted interventions for schistosomiasis control.

ecology↗

Spatiotemporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogenous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing dormancy for up to seven months yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, parasite survival within snails is greatly diminished. We conducted a year-round investigation of seasonal snail-schistosome dynamics in 109 ponds of variable ephemerality in Tanzania. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and cercariae release, though of lower magnitude in the fully desiccating ponds than non-desiccating ponds. Second, we evaluated total yearly prevalence across a gradient of an ephemerality, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

ecology↗

Global change drivers and the risk of infectious disease

Anthropogenic change is contributing to the rise in emerging infectious diseases, but it remains unclear which global change drivers most increase disease and under what contexts. We amassed a dataset from the literature that includes 1,832 observations of infectious disease responses to global change drivers across 1,202 host-parasite combinations. We found that biodiversity loss, climate change, and introduced species were associated with increases in disease-related endpoints or harm (i.e., enemy release for introduced species), whereas urbanization was associated with decreases in disease endpoints. Natural biodiversity gradients, deforestation, forest fragmentation, and most classes of chemical contaminants had non-significant effects on these endpoints. Overall, these results were consistent across human and non-human diseases. Context-dependent effects of the global change drivers on disease were common and are discussed. These findings will help better target disease management and surveillance efforts towards global change drivers that increase disease. One-Sentence SummaryHere we quantify which global change drivers increase infectious diseases the most to better target global disease management and surveillance efforts.

ecology↗

Functional similarity, not phylogenetic relatedness, predicts the relative strength of competition

Predicting the outcome and strength of species interactions is a central goal of community ecology. Researchers have proposed that outcomes of species interactions (competitive exclusion and coexistence) are a function of both phylogenetic relatedness and functional similarity. Studies relating phylogenetic distance to competition strength have shown conflicting results. Work investigating the role of phylogenetic relatedness and functional similarity in driving competitive outcomes has been limited in terms of the breadth of taxa and ecological contexts examined, which makes the generality of these studies unclear. Consequently, we gathered 1,748 pairwise competition effect sizes from 269 species and 424 unique species pairs with divergence times ranging from 1.14 to 1,275 million years and used meta-regression and model selection approaches to investigate the importance of phylogenetic relatedness and functional similarity to competition across ecological contexts. We revealed that functional similarity, but not phylogenetic relatedness, predicted the relative strength of interspecific competition (defined as the strength of interspecific competition relative to intraspecific competition). Further, we found that the presence of predators, certain habitats, increasing density of competitors, and decreasing spatial grain of experiments were all associated with more intense interspecific competition relative to intraspecific competition. Our results demonstrate that functional similarity, not phylogenetic relatedness, may explain patterns of competition-associated community assembly, highlighting the value of trait-based approaches in clarifying biotic assembly dynamics.

ecology↗

Environmental persistence but not per capita transmission rates of a chytrid fungus determines infection prevalence

AO_SCPLOWBSTRACTC_SCPLOWUnderstanding local-scale variability in disease dynamics can be important for informing strategies for surveillance and management. For example, the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd), which is implicated in population declines and species extinctions of amphibians, causes spatially variable epizootics and extirpations of its hosts. Outbreak heterogeneity could be driven by differential survival of zoospores, the free-living infectious life stage of Bd, or the persistence of dead zoospores and/or its metabolites in water, which could induce resistance among hosts. To gain a mechanistic understanding of the potential for variation in local transmission dynamics of Bd, we conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition, and per-capita transmission rate vary among water sources. We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd zoospores, rather than differences in per-capita transmission rates. Specifically, zoospore mortality rates varied significantly among pond water treatments and were lower in artificial spring water compared to pond water sources. These results suggest that variation in Bd infection dynamics could be a function of differences in exposure of hosts to live Bd. In contrast to the persistence of live zoospores, we found that rates of decomposition of dead zoospores did not vary among water sources. These results may suggest that exposure of hosts to dead Bd or its metabolites, which have been shown to induce acquired resistance, might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the drivers of variable epizootics of Bd could lead to increases in the effectiveness of surveillance and management strategies.

ecology↗

Reducing disease and producing food: Effects of 13 agrochemicals on snail biomass and human schistosomes

Agrochemical use is predicted to increase 2-5 fold by 2050 to meet food demand. Evidence suggests that agrochemical pollution could increase snails that transmit the disease schistosomiasis to 250 million people, but most agrochemicals remain unexamined. Here we quantify the relative effects of fertilizer, six insecticides, and six herbicides on snail genera responsible for 90% of global schistosomiasis cases. We identified fertilizers and 4 of 6 insecticides as high risk for increasing snail biomass by increasing snail resources (vegetative habitat and periphytic food) and reducing snail predators, respectively. Herbicides generally had negative effects on snails by reducing vegetative habitat, with two herbicides increasing snails in the absence of aquatic vegetation. Parasite production, which reflects human infection risk, scaled positively to snail biomass. Our findings suggest that fertilizers and insecticides are more likely to increase human schistosomiasis than herbicides and revealed several low risk agrochemicals that might increase crop production without increasing schistosomiasis.

ecology↗

A meta-analysis reveals temperature, dose, life stage, and taxonomy influence host susceptibility to a fungal parasite

Complex ecological relationships, such as host-parasite interactions, are often modeled with laboratory experiments. However, some experimental laboratory conditions, such as temperature or infection dose, are regularly chosen based on convenience or convention and it is unclear how these decisions systematically affect experimental outcomes. Here, we conducted a meta-analysis of 58 laboratory studies that exposed amphibians to the pathogenic fungus Batrachochytrium dendrobatidis (Bd) to better understand how laboratory temperature, host life stage, infection dose, and host species affect host mortality. We found that host mortality was driven by thermal mismatches: hosts native to cooler environments experienced greater Bd-induced mortality at relatively warm experimental temperatures and vice versa. We also found that Bd dose positively predicted Bd-induced host mortality and that the superfamilies Bufonoidea and Hyloidea were especially susceptible to Bd. Finally, the effect of Bd on host mortality varied across host life stages, with larval amphibians experiencing lower risk of Bd-induced mortality than adults or metamorphs. Metamorphs were especially susceptible and experienced mortality when inoculated with much smaller Bd doses than the average dose used by researchers. Our results suggest that when designing experiments on species interactions, researchers should carefully consider the experimental temperature, and inoculum dose, and life stage and taxonomy of the host species.

ecology↗

Thermal mismatches explain how climate change and infectious disease drove widespread amphibian extinctions

Global temperatures and infectious disease outbreaks are simultaneously increasing, but linking climate change and infectious disease to modern extinctions remains difficult. The thermal mismatch hypothesis predicts that hosts should be vulnerable to disease at temperatures where the performance gap between themselves and parasites is greatest. This framework could be used to identify species at risk from a combination of climate change and disease because it suggests that extinctions should occur when climatic conditions shift from historical baselines. We conducted laboratory experiments and analyses of recent extinctions in the amphibian genus Atelopus to show that species from the coldest environments experienced the greatest disease susceptibility and extinction risk when temperatures rapidly warmed, confirming predictions of the thermal mismatch hypothesis. Our work provides evidence that a modern mass extinction was likely driven by an interaction between climate change and infectious disease.

ecology↗

Agrochemical pollution increases risk of human exposure to schistosome parasites

Roughly 10% of the global population is at risk of schistosomiasis, a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries1-3. Increased prevalence, infection intensity, and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion, such as dam construction, which has resulted in increased snail habitat1,4-6. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife7-9 and a projected 2- to 5-fold increase in global agrochemical use by 205010 that will disproportionately occur in schistosome-endemic regions. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, the common herbicide atrazine, and the common insecticide chlorpyrifos, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat (fertilizer and atrazine) and decreasing densities of snail predators (chlorpyrifos). Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomiasis. Hence, the rapid agricultural changes occurring in schistosome-endemic regions11,12 that are driving increased agrochemical use and pollution could potentially increase the burden of schistosomiasis in these areas. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing13,14.

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Towards a Global Framework for Estimating Acclimation and Thermal Breadth that Predicts Risk from Climate Change

Thermal breadth, the range of body temperatures over which organisms perform well, and thermal acclimation, the ability to alter optimal performance temperature and critical thermal maximum or minimum with changing temperatures, reflect the capacity of organisms to respond to temperature variability and are thus crucial traits for coping with climate change. Although there are theoretical frameworks for predicting thermal breadths and acclimation, the predictions of these models have not been tested across taxa, latitudes, body sizes, traits, habitats, and methodological factors. Here, we address this knowledge gap using simulation modeling and empirical analyses of >2,000 acclimation strengths from >500 species using four datasets of ectotherms. After accounting for important statistical interactions, covariates, and experimental artifacts, we reveal that i) acclimation rate scales positively with body size contributing to a negative association between body size and thermal breadth across species and ii) acclimation capacity increases with body size, seasonality, and latitude (to mid-latitudinal regions) and is regularly underestimated for most organisms. Contrary to suggestions that plasticity theory and empirical work on thermal acclimation are incongruent, these findings are consistent with theory on phenotypic plasticity. We further validated our framework by demonstrating that it could predict global extinction risk to amphibian biodiversity from climate change.

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