Sarah A. Budischak

Effects of malathion on embryonic development and latent susceptibility to trematode parasites in ranid tadpoles

We investigated the effects of embryonic exposure to the widely used organophosphate malathion (15-600 micro/L) on the early development and latent susceptibility of pickerel frog (Rana palustris) tadpoles to the trematode parasite Echinostoma trivolvis. The latent effects of contaminant exposure are rarely examined but could have important implications for individual survival and population viability. Malathion decreased hatching success by 6.5% and viability rates by 17% at 600 microg/L, which is a lower concentration than previously documented for anuran embryos. Incidence of malformations increased from 0.5% in controls to 11.2% in the 600-microg/L malathion treatment. The primary malformations documented in the two highest pesticide concentrations were ventralization and axial shortening. After seven weeks of development in water with no malathion, tadpoles previously exposed as embryos for only 96 h to 60 and 600 microg/L malathion suffered increased parasite encystment rates when compared to controls. Our research identifies embryonic development as a sensitive window for establishing latent susceptibility to infection in later developmental stages.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Natural History of Terrapene carolina (Box Turtles) in an Urbanized Landscape

Abstract Urbanization and other anthropogenic factors are often implicated in turtle population declines, yet limited research on the natural history of turtles in urban areas has been conducted. To assess the effects of urbanization and to help develop proper conservation strategies for Terrapene c. carolina (Eastern Box Turtles), we conducted a mark-recapture study in the vicinity of Davidson, NC, from 1999 to 2004. We made 354 turtle captures, 42 of which were recapture events. We evaluated meristic characters, body condition, activity patterns, population structure, and growth rates, and then examined relationships among these variables and the amount of anthropogenically-modified habitat within 100 m of each turtles collection location. Males and females had different patterns of seasonal activity and body condition indices. Growth rates decreased with turtle age and varied between developed and forested habitats. More turtles over the age of 20 were found in areas with extensive forest cover than in areas that were developed. Although box turtles may persist in urbanized landscapes and may grow more quickly there, they suffer higher mortality in these habitats compared to forested landscapes.

Direct and indirect costs of co-infection in the wild: Linking gastrointestinal parasite communities, host hematology, and immune function.

Graphical abstract Highlights ► Costs of GI parasite infection are detectable with hematological indices. ► With aggregate parasite data, costs of infection were detected in male buffalo. ► Species-specific parasite data revealed hidden costs in female buffalo. ► Hematological data revealed costs not evident with standard body condition data. ► Parasite species richness and identity are important for measuring infection costs.

A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts

Most hosts are concurrently or sequentially infected with multiple parasites; thus, fully understanding interactions between individual parasite species and their hosts depends on accurate characterization of the parasite community. For parasitic nematodes, noninvasive methods for obtaining quantitative, species‐specific infection data in wildlife are often unreliable. Consequently, characterization of gastrointestinal nematode communities of wild hosts has largely relied on lethal sampling to isolate and enumerate adult worms directly from the tissues of dead hosts. The necessity of lethal sampling severely restricts the host species that can be studied, the adequacy of sample sizes to assess diversity, the geographic scope of collections and the research questions that can be addressed. Focusing on gastrointestinal nematodes of wild African buffalo, we evaluated whether accurate characterization of nematode communities could be made using a noninvasive technique that combined conventional parasitological approaches with molecular barcoding. To establish the reliability of this new method, we compared estimates of gastrointestinal nematode abundance, prevalence, richness and community composition derived from lethal sampling with estimates derived from our noninvasive approach. Our noninvasive technique accurately estimated total and species‐specific worm abundances, as well as worm prevalence and community composition when compared to the lethal sampling method. Importantly, the rate of parasite species discovery was similar for both methods, and only a modest number of barcoded larvae (n = 10) were needed to capture key aspects of parasite community composition. Overall, this new noninvasive strategy offers numerous advantages over lethal sampling methods for studying nematode–host interactions in wildlife and can readily be applied to a range of study systems.

Resource limitation alters the consequences of co-infection for both hosts and parasites

Most animals are concurrently infected with multiple parasite species and live in environments with fluctuating resource availability. Resource limitation can influence host immune responses and the degree of competition between co-infecting parasites, yet its effects on individual health and pathogen transmission have not been studied for co-infected hosts. To test how resource limitation affects immune trade-offs and co-infection outcomes, we conducted a factorial experiment using laboratory mice. Mice were given a standard or low protein diet, dosed with two species of helminths (alone and in combination), and then challenged with a microparasite. Using a community ecology trophic framework, we found that co-infection influenced parasite survival and reproduction via host immunity, but the magnitude and direction of responses depended on resources and the combination of co-infecting parasites. Our findings highlight that resources and their consequence for host defenses are a key context that shapes the magnitude and direction of parasite interactions.

Counterbalancing effects of maternal mercury exposure during different stages of early ontogeny in American toads.

Maternal transfer of environmental contaminants is a disadvantageous parental effect which can have long-lasting implications for offspring fitness. We investigated the effects of mercury (Hg) on the reproductive success of female amphibians and the subsequent effects of maternal transfer on the development of their offspring. American toads (Bufo americanus) maternally transferred Hg to their eggs, and there was a negative relationship between Hg concentrations and the percentage of viable hatchlings produced in clutches. However, when we continued to monitor larvae that successfully hatched, we found 21% greater metamorphic success in larvae from Hg-exposed mothers compared to reference larvae. The negative effect in the embryonic stage and positive effect in the larval stage counterbalanced one another, ultimately resulting in no difference in predicted terrestrial recruitment, regardless of maternal Hg exposure. Our findings demonstrate that maternal effects on survival manifesting at different stages in ontogeny have the potential to produce complicated outcomes.

Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population

Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.

Experimental insight into the process of parasite community assembly

Community assembly is a fundamental process that has long been a central focus in ecology. Extending community assembly theory to communities of co-infecting parasites, we used a gastrointestinal nematode removal experiment in free-ranging African buffalo to examine the community assembly patterns and processes. We first asked whether reassembled communities differ from undisturbed communities by comparing anthelmintic-treated and control hosts. Next, we examined the temporal dynamics of assembly using a cross-section of communities that reassembled for different periods of time since last experimental removal. Next, we tested for evidence of assembly processes that might drive such reassembly patterns: environmental filtering based on host traits (i.e. habitat patches), interspecific interactions, priority effects and chance dispersal from the environmental pool of infective stages (i.e. the regional species pool). On average, reassembled parasite communities had lower abundance, but were more diverse and even, and these patterns varied tightly with reassembly time. Over time, the communities within treated hosts progressively resembled controls as diversity and evenness decreased, while total abundance increased. Notably, experimental removal allowed us to attribute observed differences in abundance, diversity and evenness to the process of community assembly. During early reassembly, parasite accumulation was biased towards a subordinate species and, by excluding stochastic assembly processes (i.e. chance dispersal and priority effects), we were able to determine that early assembly is deterministic. Later in the reassembly process, we established that host traits, as well as stochastic dispersal from the environmental pool of infective stages, can affect the community composition. Overall, our results suggest that there is a high degree of resiliency and environmental dependence to the worm communities of buffalo. More generally, our data show that both deterministic and stochastic processes may play a role in the assembly of parasite communities of wild hosts, but their relative importance may vary temporally. Consequently, the best strategy for managing reassembling parasite communities may also need to shift over time.