Jeremy M. Cohen

Biodiversity inhibits parasites: Broad evidence for the dilution effect

Significance The dilution effect hypothesis suggests that diverse ecological communities limit disease spread via several mechanisms. Therefore, biodiversity losses could worsen epidemics that harm humans and wildlife. However, there is contentious debate over whether the hypothesis applies broadly, especially for parasites that infect humans. We address this fundamental question with a formal meta-analysis of >200 assessments relating biodiversity to disease in >60 host–parasite systems. We find overwhelming evidence of dilution, which is independent of host density, study design, and type and specialization of parasites. A second analysis identified similar effects of diversity in plant–herbivore systems. Thus, biodiversity generally decreases parasitism and herbivory. Consequently, human-induced declines in biodiversity could increase human and wildlife diseases and decrease crop and forest production. Infectious diseases of humans, wildlife, and domesticated species are increasing worldwide, driving the need to understand the mechanisms that shape outbreaks. Simultaneously, human activities are drastically reducing biodiversity. These concurrent patterns have prompted repeated suggestions that biodiversity and disease are linked. For example, the dilution effect hypothesis posits that these patterns are causally related; diverse host communities inhibit the spread of parasites via several mechanisms, such as by regulating populations of susceptible hosts or interfering with parasite transmission. However, the generality of the dilution effect hypothesis remains controversial, especially for zoonotic diseases of humans. Here we provide broad evidence that host diversity inhibits parasite abundance using a meta-analysis of 202 effect sizes on 61 parasite species. The magnitude of these effects was independent of host density, study design, and type and specialization of parasites, indicating that dilution was robust across all ecological contexts examined. However, the magnitude of dilution was more closely related to the frequency, rather than density, of focal host species. Importantly, observational studies overwhelmingly documented dilution effects, and there was also significant evidence for dilution effects of zoonotic parasites of humans. Thus, dilution effects occur commonly in nature, and they may modulate human disease risk. A second analysis identified similar effects of diversity in plant–herbivore systems. Thus, although there can be exceptions, our results indicate that biodiversity generally decreases parasitism and herbivory. Consequently, anthropogenic declines in biodiversity could increase human and wildlife diseases and decrease crop and forest production.

Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models

Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18–34°C with maximal transmission occurring in a range from 26–29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones.

Spatial scale modulates the strength of ecological processes driving disease distributions

Significance For four decades, ecologists have hypothesized that biotic interactions predominantly control species’ distributions at local scales, whereas abiotic factors operate more at regional scales. Here, we demonstrate that the drivers of three emerging diseases (amphibian chytridiomycosis, West Nile virus, and Lyme disease) in the United States support the predictions of this fundamental hypothesis. Humans are contributing to biodiversity loss, changes in dispersal patterns, and global climate change at an unprecedented rate. Our results highlight that common single-scale analyses can misestimate the impact that humans are having on biodiversity, disease, and the environment. Humans are altering the distribution of species by changing the climate and disrupting biotic interactions and dispersal. A fundamental hypothesis in spatial ecology suggests that these effects are scale dependent; biotic interactions should shape distributions at local scales, whereas climate should dominate at regional scales. If so, common single-scale analyses might misestimate the impacts of anthropogenic modifications on biodiversity and the environment. However, large-scale datasets necessary to test these hypotheses have not been available until recently. Here we conduct a cross-continental, cross-scale (almost five orders of magnitude) analysis of the influence of biotic and abiotic processes and human population density on the distribution of three emerging pathogens: the amphibian chytrid fungus implicated in worldwide amphibian declines and West Nile virus and the bacterium that causes Lyme disease (Borrelia burgdorferi), which are responsible for ongoing human health crises. In all three systems, we show that biotic factors were significant predictors of pathogen distributions in multiple regression models only at local scales (∼102–103 km2), whereas climate and human population density always were significant only at relatively larger, regional scales (usually >104 km2). Spatial autocorrelation analyses revealed that biotic factors were more variable at smaller scales, whereas climatic factors were more variable at larger scales, as is consistent with the prediction that factors should be important at the scales at which they vary the most. Finally, no single scale could detect the importance of all three categories of processes. These results highlight that common single-scale analyses can misrepresent the true impact of anthropogenic modifications on biodiversity and the environment.

Local Adaptation in Community Perception: How Background Impacts Judgments of Neighborhood Safety

When observing an unfamiliar neighborhood, people use indicators of physical disorder to judge the local community (i.e., community perception), associating them with crime and weak relationships between neighbors. The authors argue that these judgments depend on people’s definition of disorder, which is adapted to their local community. This is tested with an experiment. Undergraduate students from across New York State rated the collective efficacy (i.e., social quality) of neighborhoods from a single city using images of physical structures. Participants reported which features they attended to when making these judgments. Participants were categorized as being from New York City (NYC), NYC suburbs, or the less densely populated upstate region. Images were from an upstate city. Those from NYC attended more to pavement than others. Ratings by those from upstate were most accurate and positive. These results supported the initial hypotheses and suggested that community perception combines heuristics and familiarity to make inferences.

A global synthesis of animal phenological responses to climate change

Shifts in phenology are already resulting in disruptions to the timing of migration and breeding, and asynchronies between interacting species1–5. Recent syntheses have concluded that trophic level1, latitude6 and how phenological responses are measured7 are key to determining the strength of phenological responses to climate change. However, researchers still lack a comprehensive framework that can predict responses to climate change globally and across diverse taxa. Here, we synthesize hundreds of published time series of animal phenology from across the planet to show that temperature primarily drives phenological responses at mid-latitudes, with precipitation becoming important at lower latitudes, probably reflecting factors that drive seasonality in each region. Phylogeny and body size are associated with the strength of phenological shifts, suggesting emerging asynchronies between interacting species that differ in body size, such as hosts and parasites and predators and prey. Finally, although there are many compelling biological explanations for spring phenological delays, some examples of delays are associated with short annual records that are prone to sampling error. Our findings arm biologists with predictions concerning which climatic variables and organismal traits drive phenological shifts.A synthesis of animal phenology shows that temperature primarily drives mid-latitude responses, with precipitation important at lower latitudes. Phylogeny and body size are associated with the strength of phenological shifts.

Temperature determines Zika, dengue and chikungunya transmission potential in the Americas

Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand virus transmission ecology for Aedes aegypti and Ae. albopictus mosquitoes. An estimated 3.9 billion people in 120 countries are at risk for these diseases. Temperature defines the fundamental potential for vector-borne disease transmission, yet the potential for transmission in sub-tropical and temperate regions remains uncertain. Using mechanistic transmission models fit to mosquito and virus physiology data and validated with human case data, we show that mean temperature accurately bounds transmission risk for Zika, chikungunya, and dengue in the Americas. Transmission occurs between 18-34 degrees C and peaks at 29 degrees C for Ae. aegypti (between 11-28 degrees C with a peak at 26 degrees C for Ae. albopictus). As predicted, high relative incidence of Zika, dengue, and chikungunya in humans occurs between 23-32 degrees C, peaks at 27-29 degrees C, and is very low outside the predicted range. As a proxy for infrastructure and vector control effort, economic reliance on tourism explains some departures from areas otherwise suitable for high rates of transmission. Nonetheless, the temperature-based models alone provide fundamental eco-physiological measures of transmission potential. Tropical and subtropical regions are suitable for extended seasonal or year-round transmission by Ae. aegypti and Ae. albopictus. By contrast, potential transmission in temperate areas is constrained to at most three months per year even if vectors are present (which is currently not the case for large parts of the US). Such brief transmission windows limit the likelihood and potential extent of epidemics following disease introduction in temperate zones.Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18-34°C with maximal transmission occurring in a range from 26-29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones. Author Summary Understanding the drivers of recent Zika, dengue, and chikungunya epidemics is a major public health priority. Temperature may play an important role because it affects mosquito transmission, affecting mosquito development, survival, reproduction, and biting rates as well as the rate at which they acquire and transmit viruses. Here, we measure the impact of temperature on transmission by two of the most common mosquito vector species for these viruses, Aedes aegypti and Ae. albopictus. We integrate data from several laboratory experiments into a mathematical model of temperature-dependent transmission, and find that transmission peaks at 26-29°C and can occur between 18-34°C. Statistically comparing model predictions with recent observed human cases of dengue, chikungunya, and Zika across the Americas suggests an important role for temperature, and supports model predictions. Using the model, we predict that most of the tropics and subtropics are suitable for transmission in many or all months of the year, but that temperate areas like most of the United States are only suitable for transmission for a few months during the summer (even if the mosquito vector is present).

Reply to Salkeld et al.: Diversity-disease patterns are robust to study design, selection criteria, and publication bias

Recently, we provided broad evidence for a negative association between community diversity and the abundance of human and wildlife parasites (1), supporting the dilution effect hypothesis (2). Salkeld et al. (3) point out that our meta-analysis reached a different conclusion than their previous meta-analysis on the dilution effect (4), which focused solely on 13 effect sizes from six species of human parasites. Salkeld et al. (3) argue that their smaller sample size is justified because only field studies capture the ecological realism necessary to test the dilution effect hypothesis. However, field studies can have confounding variables that can generate false-positive or false-negative relationships between diversity and disease. Although laboratory studies often more confidently capture cause–effect relationships, they can be contrived. Hence, given these costs and benefits of field and laboratory studies, we included both in our meta-analysis and found that each strongly supported the dilution effect hypothesis. Nevertheless, we reanalyzed the data in our publicly available dataset using the inclusion criteria (i.e., field studies on human parasites at certain scales) of Salkeld et al. (4) and, once again, found a significant negative relationship between biodiversity and the abundance of human parasites (random effects meta-analysis: n = 22 effect sizes and 12 species as a random effect, mean Hedges’ d = −0.75, P = 0.018). Hence, the difference between the marginally nonsignificant finding in the meta-analysis of Salkeld et al. (mean Fisher’s Z = −0.23, 95% confidence interval: −0.470 to 0.008) (4) and our significant finding can be explained by the increased statistical power associated with the inclusion of nine more recent studies on six human parasites. These results further support the robustness of the negative relationship between biodiversity and infectious disease using our dataset.

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.

A global synthesis of phenological responses to climate change

Phenology, or the timing of seasonal activities, is shifting with climate change, resulting in disruptions to the timing of migration and breeding and in emerging asynchronies between interacting species1-5. Recent syntheses have concluded that trophic level1, latitude6, and how phenological responses are measured7 are key to determining the strength of phenological responses to climate change. However, despite these insights, researchers still lack a comprehensive framework that can predict responses to climate change globally and across diverse taxa. For example, little is known about whether phenological shifts are driven by different climatic factors across regions or which ecologically important species characteristics (e.g., body size) predict the strength of phenological responses. Here, we address these questions by synthesizing hundreds of published time series of animal phenology from across the planet. We find that temperature drives phenological responses at mid-latitudes, but precipitation is more important at lower latitudes, likely because these climate factors often drive seasonality in each of these regions. Body size is also negatively associated with the strength of phenological shift, suggesting emerging asynchronies between interacting species that differ in size, such as hosts and ectoparasites and predators and prey. Finally, although there are many compelling biological explanations for spring phenological delays, some examples of delays are associated with short annual records prone to sampling error. As climate change intensifies, our findings arm biologists with predictions concerning which climatic variables and organismal traits drive phenological shifts.

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.