Gregory J. Sandland

Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas)

Intensity-dependent development of Ornithodiplostomum ptychocheilus metacercariae was studied in fathead minnows (Pimephales promelas) exposed to 0, 20, or 120 cercariae. Subsamples of hosts were necropsied at 2-wk intervals to monitor parasite recruitment, growth, and time to encystment. The complex development of metacercariae within the cranium of minnows involved growth, encystment, and consolidation phases, each of which were affected by intensity. At the end of the growth phase, metacercariae from low-dose fish were 20% longer than those from high-dose fish and the latter took 2–4 wk longer to encyst. At the end of the postencystment consolidation phase (6–8 wk postinfection), the size of metacercariae decreased by approximately 50%. The rate of consolidation was slower in high-dose fish. Our results show that time, intensity, and temperature affect development of O. ptychocheilus. Because metacercariae development and differentiation are linked to infectivity, events occurring in intermediate hosts can potentially impact the structure and size of trematode suprapopulations.

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.

POPULATION DYNAMICS OF ORNITHODIPLOSTOMUM PTYCHOCHEILUS METACERCARIAE IN FATHEAD MINNOWS (PIMEPHALES PROMELAS) FROM FOUR NORTHERN-ALBERTA LAKES

Annual, seasonal, and interlake variation in prevalence and intensity of Ornithodiplostomum ptychocheilus (Faust) metacercariae was assessed in populations of fathead minnows (Pimephales promelas) collected from 4 lakes in north-central Alberta. Mean metacercariae intensity in young-of-the-year minnows varied extensively (5–123 metacercariae/host) among year, month, and lakes. In 2 of the lakes, prevalence always reached 100%, and mean intensity always peaked in September or October. The high spatial and annual variation in metacercarial recruitment was partly attributable to variation in host size, but variation in water depth, temperature, snail densities, and bird visitation likely also played a role. A laboratory experiment demonstrated that host and metacercariae survival was intensity-independent during a period of simulated winter. Thus, metacercariae recruited in the fall survive until the following spring.

PARASITE-INDUCED VARIATION IN HOST MORPHOLOGY: BRAIN-ENCYSTING TREMATODES IN FATHEAD MINNOWS

Metacercariae of the trematode Ornithodiplostomum ptychocheilus cause a conspicuous enlargement of the cranium of juvenile fathead minnows (Pimephales promelas). Minnows sampled from 2 naturally infected ponds in northern Alberta, Canada, had 12% higher and 7% wider craniums compared to fish from an adjacent, uninfected pond. We tested the prediction that cranial distortion was caused by encystment of metacercariae on the brains of slow-growing minnows in a factorial experiment. Juvenile fish were either exposed once to 120 cercariae or 3 times to 40 cercariae; they were then fed either a low- or high-quantity diet for 8 wk. Results showed that after controlling for host size, cranial heights were affected by infection regime and host diet but not by the infection × diet interaction. Cranial distortion was most prominent in minnows exposed once to cercariae, showing that the rapid, simultaneous growth of metacercariae interfered with the normal development of the cranium. Thus, the expression of the parasite-induced phenotype was context dependent, the result of factors associated with the dynamics of cercariae transmission and host growth rate.

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 parasites life cycle can influence the intensities and sex ratios of worms in subsequent hosts.

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.

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.

Differential patterns of infection and life-history expression in native and invasive hosts exposed to a trematode parasite

Non-indigenous species (NIS) are well-recognized as threats to biodiversity worldwide. Yet the interaction between NIS and disease emergence in native habitats remains poorly understood. Bithynia tentaculata is an invasive aquatic snail which is now found in the Upper Mississippi River (UMR). A key concern with this snail is that it harbors trematode parasites (such as Sphaeridiotrema spp.) that have been associated with waterfowl mortality in the region. In this study, we used a combination of field collections and laboratory experiments to better understand the roles that infection competency and host life-history responses play in disease transmission in the UMR. Results from the field and laboratory showed that B. tentaculata infected with Sphaeridiotrema spp. grew to a larger size than uninfected individuals. Although infection was not observed in a number of native species, results from this study suggest that they may still suffer exposure costs (such as reduced growth). Moreover, variability in infection competency between NIS and native snails may dilute or amplify host infection risk. This study reinforces the importance of considering both host life-history responses and competency in systems involving NIS, and provides insight into the factors potentially modulating waterfowl disease in the UMR.

Context-dependent life-history variation in a pond snail (Lymnaea elodes) exposed to desiccation and a sterilizing parasite

Abstract: In this study we used a combination of field monitoring and laboratory experimentation to investigate the effects of desiccation and Echinostoma revolutum infection on life-history traits of the pond snail, Lymnaea elodes. Field-collected snails demonstrated a sharp decline in survivorship within 8 weeks of pond drying. Results from a corresponding laboratory experiment, where snails were exposed to parasites prior to aestivation, demonstrated that desiccation played a more important role in snail survival than E. revolutum infection. However, infection influenced host growth patterns as aestivated-infected snails were significantly larger at the end of the experiment relative to aestivated controls. In a second laboratory experiment, exposure after a period of aestivation resulted in higher levels of infection compared to snails that were continuously hydrated. Moreover, exposed-uninfected snails demonstrated higher mortality than either control or infected snails regardless of aestivation treatment. Results from this work 1) demonstrate the importance of incorporating multiple variables into life-history studies and 2) provide insight into the factors underlying host-parasite dynamics in the field.

Infection Patterns in Invasive and Native Snail Hosts Exposed to a Parasite Associated with Waterfowl Mortality in the Upper Mississippi River, USA

Abstract 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.