Evaluating the Life-History Responses of Adult Invasive (Bithynia tentaculata) and Native (Physa gyrina) Snails Exposed to a Cu-Based Pesticide (EarthTec® QZ).

The faucet snail, Bithynia tentaculata, is an invasive snail that facilitates outbreaks of waterfowl disease in the Upper Mississippi River of the United States. In response, there is interest in identifying strategies that mitigate its population and spread. In this study we assessed the effects of a copper (Cu) molluscicide, EarthTec® QZ, at three concentrations (0, 0.1 and 0.6 mg/L Cu) on adult B. tentaculata and a coexisting native species, Physa gyrina. We found that in the 0.6 mg/L Cu treatment, ~ 68% of B. tentaculata snails remained alive after a 4-day exposure whereas all P. gyrina snails died. In contrast, a majority of both snail species remained alive and active after 4 days in the control and 0.1 mg/L Cu treatments. Although B. tentaculata demonstrated higher survivorship, it bioaccumulated more Cu than P. gyrina. Additionally, examination of B. tentaculata individuals revealed that females tended to exhibit higher mortality than males.

Patterns of Sphaeridiotrema pseudoglobulus infection in sympatric and allopatric hosts (Bithynia tentaculata) originating from widely separated sites across the USA.

In circumstances where populations of invasive species occur across variable landscapes, interactions among invaders, their parasites, and the surrounding environment may establish local coevolutionary trajectories for the participants. This can generate variable infection patterns when parasites interact with sympatric versus allopatric hosts. Identifying the potential for such patterns within an invasive-species framework is important for better predicting local infection outcomes and their subsequent impacts on the surrounding native community. To begin addressing this question, we exposed an invasive snail (Bithynia tentaculata) from two widely separated sites across the USA (Wisconsin and Montana) to the digenean parasite, Sphaeridiotrema pseudoglobulus, collected from Wisconsin. Parasite exposures generated high infection prevalences in both sympatric and allopatric snails. Furthermore, host survival, host growth, the proportion of patent snails, and the timing of patency did not differ between sympatric and allopatric combinations. Moreover, passaging parasites through snails of different origins had no effect on transmission success to subsequent hosts in the life cycle. However, the number of parasites emerging from snails and the pattern of their release varied based on snail origin. These latter observations suggest the potential for local adaptation in this system, but subsequent research is required to further substantiate this as a key factor underlying infection patterns in the association between S. pseudoglobulus and B. tentaculata.

Infection patterns of trematodes across size classes of an invasive snail species using field and laboratory studies.

In the Upper Mississippi River Region, invasive faucet snails (Bithynia tentaculata) and their trematode parasites have been implicated in more than 182 000 waterfowl deaths since 1996. Estimating transmission potential depends on accurate assessments of susceptible host population size. However, little is known about the mechanisms underlying snail-host susceptibility in this system. Prior field studies suggest that very small, likely young, faucet snails are less suitable secondary intermediate hosts. Here, we test whether the patterns observed in the field are because small snails (1) are refractory to infection by cercariae, (2) die from infection and are removed from sampled populations, and/or (3) are not preferred by cercariae. Our own field collections were consistent with the observation that smaller faucet snails exhibit lower metacercarial infection prevalence and abundance than larger snails. However, laboratory-based experiments show that smaller snails were actually more susceptible to infection than larger snails. Moreover, the smallest snail size class had significantly higher mortality than larger snails following infection, which may explain their reduced infection levels observed in the field. Our study demonstrates the importance of pairing field and laboratory studies to better understand mechanisms underlying patterns of infection.

A Pilot Evaluation of the Toxicity of EarthTec® QZ on Invasive (Bithynia tentaculata) and Native (Physa gyrina) Snail Species from the Upper Mississippi River.

We used a comparative approach to investigate the effects of a copper-based pesticide (EarthTec® QZ) on embryos of an invasive snail (Bithynia tentaculata) and a native snail (Physa gyrina). Embryos were exposed to one of three treatments: control (0 mg/L Cu2+), low-dose (0.1 mg/L Cu2+), or high-dose (0.6 mg/L Cu2+), which reflect manufacturer-recommended low and medium 4-day molluscicide treatment concentrations. Exposure to 0.6 mg/L Cu2+ over 4 days generated 100% mortality in both invasive and native snail embryos; however, reducing the exposure time from 4 to 1 day resulted in 100% mortality in B. tentaculata but some hatching (7%) in P. gyrina. In contrast, embryos of both species exposed to 0.1 mg/L Cu2+ treatment for 4 days showed almost 100% survivorship. Further manipulations of Cu2+ concentrations and exposure times may yield regimes that maximize mortality in B. tentaculata while minimizing negative impacts on native species.

Using a Summer REU to Help Develop the Next Generation of Mathematical Ecologists.

Understanding the complexities of environmental issues requires individuals to bring together ideas and data from different disciplines, including ecology and mathematics. With funding from the national science foundation (NSF), scientists from the University of Wisconsin-La Crosse and the US geological survey held a research experience for undergraduates (REU) program in the summer of 2016. The goals of the program were to expose students to open problems in the area of mathematical ecology, motivate students to pursue STEM-related positions, and to prepare students for research within interdisciplinary, collaborative settings. Based on backgrounds and interests, eight students were selected to participate in one of two research projects: wind energy and wildlife conservation or the establishment and spread of waterfowl diseases. Each research program was overseen by a mathematician and a biologist. Regardless of the research focus, the program first began with formal lectures to provide students with foundational knowledge followed by student-driven research projects. Throughout this period, student teams worked in close association with their mentors to create, parameterize and evaluate ecological models to better understand their systems of interest. Students then disseminated their results at local, regional, and international meetings and through publications (one in press and one in progress). Direct and indirect measures of student development revealed that our REU program fostered a deep appreciation for and understanding of mathematical ecology. Finally, the program allowed students to gain experiences working with individuals with different backgrounds and perspectives. Taken together, this REU program allowed us to successfully excite, motivate and prepare students for future positions in the area of mathematical biology, and because of this it can be used as a model for interdisciplinary programs at other institutions.

Nutrient availability modulates both host and parasite life histories in a snail-trematode interaction.

Host nutrient availability can have important life history consequences for hosts and their parasites. The responses of each participant within the association can vary extensively across host-parasite systems. In this paper, we outline the life history responses of the aquatic snail Biomphalaria glabrata and its trematode parasite Echinostoma caproni during host nutrient restriction. The onset of host starvation had rapid and strong effects on snail reproduction, significantly reducing egg output in control snails and eliminating egg production in infected individuals. The combination of E. caproni infection and nutrient restriction also had a dramatic effect on B. glabrata survival, with starved infected snails dying at a faster rate than hosts from any other treatment. In terms of parasite reproduction, host nutrient restriction did not influence the quantity of parasite larvae produced after starvation onset but did influence parasite quality, reducing both larval swimming time and overall longevity. Together these results demonstrate that nutrient restriction can strongly influence both host and parasite life histories, and therefore should be considered in future studies attempting to understand patterns of disease in host populations.

Infection patterns in invasive and native snail hosts exposed to a parasite associated with waterfowl mortality in the upper Mississippi River, USA.

Bithynia tentaculata is an aquatic invasive snail first detected in the upper Mississippi River (UMR) in 2002. The snail harbors a number of parasitic trematode species, including Sphaeridiotrema pseudoglobulus, that have been implicated in waterfowl mortality in the region. We assessed the capacity of S. pseudoglobulus cercariae to infect B. tentaculata and native snails found in the UMR. Four snail species (one invasive and three native) were individually exposed to S. pseudoglobulus larvae and all were successfully infected. A subsequent experiment examining infection patterns in invasive and native hosts exposed singly or in mixed treatments revealed no difference in parasite establishment among snail species. Our results add to our understanding of S. pseudoglobulus transmission and provide insight into processes underlying waterfowl disease in the UMR.

Interactions among virulence, coinfection and drug resistance in a complex life-cycle parasite.

Motivated by relatively recent empirical studies on Schistosoma mansoni, we use a mathematical model to investigate the impacts of drug treatment of the definitive human host and coinfection of the intermediate snail host by multiple parasite strains on the evolution of parasites' drug resistance. Through the examination of evolutionarily stable strategies (ESS) of parasites, our study suggests that higher levels of drug treatment rates (which usually tend to promote monomorphism as the evolutionary equilibrium) favor parasite strains that have a higher level of drug resistance. Our study also shows that whether coinfection of intermediate hosts affects the levels of drug resistance at ESS points and their stability depends on the assumptions on the cost of parasites paid for drug resistance, coinfection functions and parasites' reproduction within coinfected hosts. This calls for more empirical studies on the parasite.

Evolution of host resistance to parasite infection in the snail-schistosome-human system.

The evolutionary strategies that emerge within populations can be dictated by numerous factors, including interactions with other species. In this paper, we explore the consequences of such a scenario using a host-parasite system of human concern. By analyzing the dynamical behaviors of a mathematical model we investigate the evolutionary outcomes resulting from interactions between Schistosoma mansoni and its snail and human hosts. The model includes two types of snail hosts representing resident and mutant types. Using this approach, we focus on establishing evolutionary stable strategies under conditions where snail hosts express different life-histories and when drug treatment is applied to an age-structured population of human hosts. Results from this work demonstrate that the evolutionary trajectories of host-parasite interactions can be varied, and at times, counter-intuitive, based on parasite virulence, host resistance, and drug treatment.

Effects of host outcrossing on the interaction between an aquatic snail and its locally adapted parasite.

In this study, we investigated the interaction between host outcrossing and infection in the Biomphalaria glabrata-Schistosoma mansoni system. Snails collected from three susceptible isofemale lines were mated with either siblings or snails recently derived from a field site in Brazil. Resulting inbred and outcrossed progeny were then exposed to S. mansoni larvae and monitored for a 10-week period. Interestingly, all snails exhibited equal susceptibility whether they were the result of inbreeding or outcrossing. However, further examination of both host and parasite life-history traits uncovered significant differences between the groups. In uninfected snails, outcrossed progeny tended to exhibit greater fitness relative to inbred progeny. When snails were parasitized, these differences were magnified in certain life-history traits, particularly host reproduction and survival. As an extension of the work, we also investigated virulence within this host-parasite system. Estimates of parasite reproduction and host size were combined to generate a novel "exploitation index," and these indices were regressed with host survivorship. As predicted, there was a significant and negative correlation between the variables, but this was restricted to a single snail line. Results from this study demonstrate that infection outcomes (as measured by prevalence) may not differ between inbred and outcrossed hosts. However, outcrossing may enhance snail fitness through life-history trait expression.

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni.

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite's life cycle can influence the intensities and sex ratios of worms in subsequent hosts.

Evolutionary implications for interactions between multiple strains of host and parasite.

The interaction between multiple parasite strains within different host types may influence the evolutionary trajectories of parasites. In this article, we formulate a deterministic model with two strains of parasites and two host types in order to investigate how heterogeneities in parasite virulence and host life-history may affect the persistence and spread of diseases in natural systems. We compute the reproductive number of strain i (R(i)) independently, as well as the (conditional) "invasion" reproductive number for strains i (R(i)(j), j not equal i) when strain j is at a positive equilibrium. We show that the disease-free equilibrium is locally asymptotically stable if R(i)<1 for both strains and is unstable if R(i)>1 for one stain. We establish the criterion R(i)(j)>1 for strain i to invade strain j. Subthreshold coexistence driven by coinfection is possible even when R(i) of one strain is below 1. We identify conditions that determine the evolution of parasite specialism or generalism based on the life-history strategies employed by hosts, and investigate how host strains may influence parasite persistence.

Interplay between host genetic variation and parasite transmission in the Biomphalaria glabrata-Schistosoma mansoni system.

Genetic variability is often predicted to enhance host fitness in the face of parasitism, yet this idea is rarely tested in an experimental setting, particularly with animal hosts. To assess this question, we used a relatively resistant line of snail hosts (Biomphalaria glabrata) to generate inbred and outcrossed progeny that were then either exposed or sham-exposed to the trematode parasite, Schistosoma mansoni. Results showed no difference in prevalence between the groups; however, large differences appeared in other host life history traits, particularly reproduction. Outcrossed progeny produced large numbers of eggs relative to inbred progeny especially in the face of infection. Furthermore, eggs produced by outcrossed snails took less time to hatch and exhibited greater hatching success compared to their inbred counterparts. Parasite reproduction demonstrated the opposite trend, with fewer parasites emerging from outcrossed snails compared to inbred individuals. This work shows that the introduction of genetic variation into inbred snail populations can have important implications for the viability of host populations and disease transmission.

Interspecific antagonism and virulence in hosts exposed to two parasite species.

Co-infection of host organisms by multiple parasite species has evolutionary consequences for all participants in the symbiosis. In this study, we co-exposed aquatic-snails (Biomphalaria glabrata) to two of their trematode parasites, Schistosoma mansoni and Echinostoma caproni. In co-exposed snails, E. caproni prevalence was 63% compared to only 23% for S. mansoni. Co-exposed E. caproni-infected snails exhibited reduced fecundity, higher mortality, and higher parasite reproduction (higher virulence) compared to hosts exposed to echinostomes alone. Conversely, co-exposed S. mansoni-infected snails released fewer parasites and produced greater numbers of eggs compared to hosts exposed to S. mansoni alone. These results suggest that co-exposure not only influences the establishment (presence or absence) of particular parasite species, but also impacts host life history, parasite reproduction, and the virulence of the interaction.

Combined effects of a herbicide (atrazine) and predation on the life history of a pond snail, Physa gyrina.

We investigated the combined effects of chronic pesticide exposure and predation on the life-history traits of Physa gyrina. Results show that atrazine and predation can impact snail immune function, reproduction, and survival. This work emphasizes the need to assess sublethal life-history responses to multiple stressors over biologically relevant timescales.

Multi-species interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata).

This study assessed the effects of a commensal, Chaetogaster limnaei limnaei, and a parasitic trematode, Schistosoma mansoni, on infection patterns and life-history responses in the aquatic snail Biomphalaria glabrata. Prevalence of infection was significantly higher in snails that were devoid of C. limnaei limnaei relative to those that were colonized by the commensal, indicating that the oligochaete may protect the host from trematode infection. This finding appeared to be the direct result of the commensal as opposed to indirect stimulation of the immune system, as hemocyte numbers did not differ between C. limnaei limnaei-colonized and noncolonized snails. Snail growth and reproduction were affected by the presence of C. limnaei limnaei and exposure to S. mansoni. Two-way ANOVA revealed a significant effect of both C. limnaei limnaei presence and trematode exposure on B. glabrata growth over the 5-wk study with C. limnaei limnaei-colonized and parasite-infected snails demonstrating the greatest growth. Snails exposed, but uninfected, by S. mansoni demonstrated the lowest growth regardless of commensal colonization. Chaetogaster limnaei limnaei colonization had no effect on egg production, but S. mansoni-infected snails produced significantly more eggs than individuals from other treatment groups. Survival remained over 85% in all treatment groups. The ecological implications of these results are discussed.

Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails.

Resource allocation strategies may be influenced by both biotic and abiotic factors. The purpose of this study was to investigate the effects of both parasitism and diet quality on the growth, reproduction, and survival of the pond snail, Lymnaea elodes. In addition, we assessed parasite growth and reproduction. High-protein (high diet) or low-protein diets (low diet) were fed to juvenile L. elodes snails that were either exposed or sham-exposed to the castrating trematode, Echinostoma revolutum. Host growth was assessed weekly; reproduction and survival were recorded every 2-3 days. We estimated parasite development as the time to parasite release from the host (patency), and parasite reproduction as the number of larvae shed from infected snails at two time points. Diet and infection status had significant effects on snail growth. Infected snails produced few eggs and tended to grow to larger sizes than uninfected snails regardless of diet. In contrast, exposed-uninfected individuals displayed diet-dependent patterns of growth and reproduction. On the high-protein diet, uninfected and exposed-uninfected snails exhibited similar patterns of growth and reproduction, whereas in the low-diet treatment, exposed-uninfected snails exhibited reduced growth and delayed reproduction relative to uninfected individuals. Survival differed among treatments in the latter stages of the study with infected snails exhibiting reduced survival relative to snails from other treatments. Moreover, infected low-diet snails exhibited lower survival than infected high-diet snails. Parasite development and reproduction did not appear to be directly influenced by the quality of host diet. Results from this study suggest that energy allocation patterns are context-dependent in juvenile snails, influenced by parasite exposure and diet quality. Furthermore, parasite reproduction appears to depend more on host size than on the quality of host diet.