Why do parasites exhibit reverse latitudinal diversity gradients? Testing the roles of host diversity, habitat and climate.

AIM: The latitudinal diversity gradient (LDG) - in which species richness decreases from the equator toward the poles - is among the most fundamental distributional patterns in ecology. Despite the expectation that the diversity of parasites tracks that of their hosts, available evidence suggests that many parasites exhibit reverse latitudinal gradients or no pattern, yet the rarity of large-scale datasets on host-parasite interactions calls into question the robustness of such trends. Here, we collected parasitological data from a host group of conservation importance - lentic-breeding amphibians - to characterize the form and direction of relationships among latitude, parasite richness, and parasite load. LOCATION: The contiguous USA. TIME PERIOD: 2000 to 2014. MAJOR TAXA STUDIED: Lentic-breeding frogs and toads and their helminth parasites. METHODS: We collected information on parasite richness and infection load for 846 amphibian populations representing 31 species. We combined these data with environmental and biological data to test for LDGs and potential mechanisms. RESULTS: Both parasite richness and abundance increased across 20 degrees of latitude - a reverse LDG. For parasite richness, this pattern was partially explained by latitudinal increases in wetland area, landcover diversity, and the richness of waterbirds - which function as definitive hosts for many amphibian parasites. Host body size also correlated positively with latitude and helminth richness, potentially reflecting increased habitat availability, greater host longevity, or a persistent phylogenetic signal. Parasite abundance associated positively with wetland area and landcover diversity, but negatively with amphibian taxonomic richness. Longitude exhibited non-linear relationships with parasite abundance and richness, which we suggest stem from large-scale variation in host availability (e.g., migratory bird flyways). MAIN CONCLUSIONS: With growing interest in the distribution of parasites and pathogens, these results highlight the importance of inverse latitudinal gradients while emphasizing the explanatory influence of host body size, habitat availability, and host diversity.

What factors explain the geographical range of mammalian parasites?

Free-living species vary substantially in the extent of their spatial distributions. However, distributions of parasitic species have not been comprehensively compared in this context. We investigated which factors most influence the geographical extent of mammal parasites. Using the Global Mammal Parasite Database we analysed 17 818 individual geospatial records on 1806 parasite species (encompassing viruses, bacteria, protozoa, arthropods and helminths) that infect 396 carnivore, ungulate and primate host species. As a measure of the geographical extent of each parasite species we quantified the number and area of world ecoregions occupied by each. To evaluate the importance of variables influencing the summed area of ecoregions occupied by a parasite species, we used Bayesian network analysis of a subset ( n = 866) of the parasites in our database that had at least two host species and complete information on parasite traits. We found that parasites that covered more geographical area had a greater number of host species, higher average phylogenetic relatedness between host species and more sampling effort. Host and parasite taxonomic groups had weak and indirect effects on parasite ecoregion area; parasite transmission mode had virtually no effect. Mechanistically, a greater number of host species probably increases both the collective abundance and habitat breadth of hosts, providing more opportunities for a parasite to have an expansive range. Furthermore, even though mammals are one of the best-studied animal classes, the ecoregion area occupied by their parasites is strongly sensitive to sampling effort, implying mammal parasites are undersampled. Overall, our results support that parasite geographical extent is largely controlled by host characteristics, many of which are subsumed within host taxonomic identity.

Continental-extent patterns in amphibian malformations linked to parasites, chemical contaminants, and their interactions.

Widespread observations of malformed amphibians across North America have generated both concern and controversy. Debates over the causes of such malformations-which can affect >50% of animals in a population-have continued, likely due to involvement of multiple causal factors. Here, we used a 13-year dataset encompassing 53,880 frogs and toads from 422 wetlands and 42 states in the conterminous USA to test hypotheses relating abnormalities and four categories of potential drivers: (i) chemical contaminants, (ii) land use practices, (iii) parasite infection, and (iv) targeted interactions between parasites and pesticides. Using a hierarchically nested, competing-model approach, we further examined how these associations varied spatially among geographic regions. Although malformations were rare overall (average = 1.6%), we identified 96 hotspot sites with 5%-25% abnormal individuals. Using the full dataset of 934 collections (without data on parasite infection), malformation frequency was best predicted by the presence of oil and gas wells within the watershed. Among collections also examined for parasite infection (n = 154), average parasite load and its interaction with pesticide application positively predicted malformations: wetlands with a greater abundance of the trematode Ribeiroia ondatrae were more likely to have malformed amphibians, but these effects were strongest when pesticide application was also high, consistent with prior experimental research. Importantly, however, the influence of these factors also varied regionally, helping explain divergent results from previous studies at local scales; parasite infection was more influential in the West and Northeast, whereas pesticide application and oil/gas wells correlated with abnormalities in the Northeast, Southeast, and western regions of the USA. These results, based on the largest systematic sampling of amphibian malformations, suggest that increased observations of abnormal amphibians are associated with both parasite infection and chemical contaminants, but that their relative importance and interaction strength varied with the spatial extent of the analysis.

Global Mammal Parasite Database version 2.0.

Illuminating the ecological and evolutionary dynamics of parasites is one of the most pressing issues facing modern science, and is critical for basic science, the global economy, and human health. Extremely important to this effort are data on the disease-causing organisms of wild animal hosts (including viruses, bacteria, protozoa, helminths, arthropods, and fungi). Here we present an updated version of the Global Mammal Parasite Database, a database of the parasites of wild ungulates (artiodactyls and perissodactyls), carnivores, and primates, and make it available for download as complete flat files. The updated database has more than 24,000 entries in the main data file alone, representing data from over 2700 literature sources. We include data on sampling method and sample sizes when reported, as well as both "reported" and "corrected" (i.e., standardized) binomials for each host and parasite species. Also included are current higher taxonomies and data on transmission modes used by the majority of species of parasites in the database. In the associated metadata we describe the methods used to identify sources and extract data from the primary literature, how entries were checked for errors, methods used to georeference entries, and how host and parasite taxonomies were standardized across the database. We also provide definitions of the data fields in each of the four files that users can download.

Habitat heterogeneity drives the host-diversity-begets-parasite-diversity relationship: evidence from experimental and field studies.

Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free-living species. Our analyses revealed that parasite diversity increased consistently with host diversity due to habitat (i.e. host) heterogeneity, with secondary contributions from parasite colonisation and host abundance. Results of the experiment, in which host diversity was manipulated while parasite colonisation and host abundance were fixed, further reinforced this conclusion. Finally, the coefficient of host diversity on parasite diversity increased with spatial grain, which was driven by differences in their species-area curves: while host richness quickly saturated, parasite richness continued to increase with neighbourhood size. These results offer mechanistic insights into drivers of parasite diversity and provide a hierarchical framework for multi-scale disease research.

Effects of individual, community, and landscape drivers on the dynamics of a wildland forest epidemic.

The challenges posed by observing host-pathogen-environment interactions across large geographic extents and over meaningful time scales limit our ability to understand and manage wildland epidemics. We conducted a landscape-scale, longitudinal study designed to analyze the dynamics of sudden oak death (an emerging forest disease caused by Phytophthora ramorum) across hierarchical levels of ecological interactions, from individual hosts up to the community and across the broader landscape. From 2004 to 2011, we annually assessed disease status of 732 coast live oak, 271 black oak, and 122 canyon live oak trees in 202 plots across a 275-km2 landscape in central California. The number of infected oak stems steadily increased during the eight-year study period. A survival analysis modeling framework was used to examine which level of ecological heterogeneity best predicted infection risk of susceptible oak species, considering variability at the level of individuals (species identity, stem size), the community (host density, inoculum load, and species richness), and the landscape (seasonal climate variability, habitat connectivity, and topographic gradients). After accounting for unobserved risk shared among oaks in the same plot, survival models incorporating heterogeneity across all three levels better predicted oak infection than did models focusing on only one level. We show that larger oak trees (especially coast live oak) were more susceptible, and that interannual variability in inoculum production by the highly infectious reservoir host, California bay laurel, more strongly influenced disease risk than simply the density of this important host. Concurrently, warmer and wetter rainy-season conditions in consecutive years intensified infection risk, presumably by creating a longer period of inoculum build-up and increased probability of pathogen spillover from bay laurel to oaks. Despite the presence of many alternate host species, we found evidence of pathogen dilution, where less competent hosts in species-rich communities reduce pathogen transmission and overall risk of oak infection. These results identify key parameters driving the dynamics of emerging infectious disease in California woodlands, while demonstrating how multiple levels of ecological heterogeneity jointly determine epidemic trajectories in wildland settings.

Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems.

A central challenge to studying emerging infectious diseases (EIDs) is a landscape dilemma: Our best empirical understanding of disease dynamics occurs at local scales, whereas pathogen invasions and management occur over broad spatial extents. The burgeoning field of landscape epidemiology integrates concepts and approaches from disease ecology with the macroscale lens of landscape ecology, enabling examination of disease across spatiotemporal scales in complex environmental settings. We review the state of the field and describe analytical frontiers that show promise for advancement, focusing on natural and human-altered ecosystems. Concepts fundamental to practicing landscape epidemiology are discussed, including spatial scale, static versus dynamic modeling, spatially implicit versus explicit approaches, selection of ecologically meaningful variables, and inference versus prediction. We highlight studies that have advanced the field by incorporating multiscale analyses, landscape connectivity, and dynamic modeling. Future research directions include understanding disease as a component of interacting ecological disturbances, scaling up the ecological impacts of disease, and examining disease dynamics as a coupled human-natural system.

Forest species diversity reduces disease risk in a generalist plant pathogen invasion.

Empirical evidence suggests that biodiversity loss can increase disease transmission, yet our understanding of the 'diversity-disease hypothesis' for generalist pathogens in natural ecosystems is limited. We used a landscape epidemiological approach to examine two scenarios regarding diversity effects on the emerging plant pathogen Phytophthora ramorum across a broad, heterogeneous ecoregion: (1) an amplification effect exists where disease risk is greater in areas with higher plant diversity due to the pathogen's wide host range, or (2) a dilution effect where risk is reduced with increasing diversity due to lower competency of alternative hosts. We found evidence for pathogen dilution, whereby disease risk was lower in sites with higher species diversity, after accounting for potentially confounding effects of host density and landscape heterogeneity. Our results suggest that although nearly all plants in the ecosystem are hosts, alternative hosts may dilute disease transmission by competent hosts, thereby buffering forest health from infectious disease.