Variation in Trematode Infection in Snails Associated with Land Cover and Water Chemistry in the Central Illinois River Watershed.

Parasites can affect animal populations and communities in aquatic ecosystems. However, greater understanding is needed for the distributions and drivers of parasite infection levels in many areas. This study focuses on parasite prevalence (percent infected hosts) of an important class of parasites, trematodes, in 2 species of snail first intermediate hosts (Planorbella trivolvis and Physa sp.) in the Illinois River watershed, which has been impacted by human development. We hypothesized that trematode prevalence depends on local (e.g., water chemistry) and landscape (e.g., proximity to the Illinois River and land cover) factors. To test our hypotheses, we collected at least 20 individuals of 1 or both species of snails from 28 ponds within the watershed, and we made water-quality measurements and recorded habitat characteristics at each site. We then screened the snails for infections in the laboratory and identified the trematode cercariae that emerged based on morphological and molecular techniques. We found 5 cercariae morphotypes, including important parasites of wildlife, such as Echinostoma sp. and Ribeiroia ondatrae. Our results indicate that proximity to the Illinois River and open water or wetlands was positively associated with trematode prevalence in both snail species, whereas water chemistry (higher pH, lower calcium concentration, and lower specific conductance) was associated with increased prevalence, but only in Physa. Our findings offer increased understanding of potential environmental drivers underlying trematode distributions, with implications for wildlife health.

Effects of vertical position on trematode parasitism in larval anurans.

Spatial distributions of animals can affect interactions with their natural enemies, such as parasites, and thus have important implications for host-parasite dynamics. While spatial variation in infection risk has been explored in many systems at the landscape scale, less attention has been paid to spatial structure at smaller scales. Here, we explore a hypothesized relationship between a common spatial variable, vertical position, and risk of parasite infection in a model aquatic system, larval frogs (Rana) and trematode (Digenea) parasites. Vertical position is relevant to this system given evidence that the densities of snail first intermediate hosts, tadpole second intermediate hosts, and trematode infective stages can vary with depth. To test the effects of depth on infection risk of larval frogs by trematodes, we performed two enclosure experiments, one in the laboratory and one in the field, in which larval frogs in cages just below the water surface or near the bottom of the water column were exposed to parasites. Compared with near-surface cages, mean infection load (number of cysts) in tadpoles in near-bottom cages was 83% higher after 48-h exposures in the laboratory and 730% higher after 10-day exposures in the field. Our findings thus indicate that infection risk depends on depth, which may have adaptive significance, as tadpoles have previously been shown to change vertical position in response to parasite presence. These results motivate future work examining vertical variation in infection risk and may have broader implications for host-parasite dynamics and evolution of host and parasite behavior.

The distribution of echinostome parasites in ponds and implications for larval anuran survival.

Parasites can influence host population dynamics, community composition and evolution. Prediction of these effects, however, requires an understanding of the influence of ecological context on parasite distributions and the consequences of infection for host fitness. We address these issues with an amphibian - trematode (Digenea: Echinostomatidae) host-parasite system. We initially performed a field survey of trematode infection in first (snail) and second (larval green frog, Rana clamitans) intermediate hosts over 5 years across a landscape of 23 ponds in southeastern Michigan. We then combined this study with a tadpole enclosure experiment in eight ponds. We found echinostomes in all ponds during the survey, although infection levels in both snails and amphibians differed across ponds and years. Echinostome prevalence (proportion of hosts infected) in snails also changed seasonally depending on host species, and abundance (parasites per host) in tadpoles depended on host size and prevalence in snails. The enclosure experiment demonstrated that infection varied at sites within ponds, and tadpole survival was lower in enclosures with higher echinostome abundance. The observed effects enhance our ability to predict when and where host-parasite interactions will occur and the potential fitness consequences of infection, with implications for population and community dynamics, evolution and conservation.

Cyanobacterial harmful algal blooms are a biological disturbance to Western Lake Erie bacterial communities.

Human activities are causing a global proliferation of cyanobacterial harmful algal blooms (CHABs), yet we have limited understanding of how these events affect freshwater bacterial communities. Using weekly data from western Lake Erie in 2014, we investigated how the cyanobacterial community varied over space and time, and whether the bloom affected non-cyanobacterial (nc-bacterial) diversity and composition. Cyanobacterial community composition fluctuated dynamically during the bloom, but was dominated by Microcystis and Synechococcus OTUs. The bloom's progression revealed potential impacts to nc-bacterial diversity. Nc-bacterial evenness displayed linear, unimodal, or no response to algal pigment levels, depending on the taxonomic group. In addition, the bloom coincided with a large shift in nc-bacterial community composition. These shifts could be partitioned into components predicted by pH, chlorophyll a, temperature, and water mass movements. Actinobacteria OTUs showed particularly strong correlations to bloom dynamics. AcI-C OTUs became more abundant, while acI-A and acI-B OTUs declined during the bloom, providing evidence of niche partitioning at the sub-clade level. Thus, our observations in western Lake Erie support a link between CHABs and disturbances to bacterial community diversity and composition. Additionally, the short recovery of many taxa after the bloom indicates that bacterial communities may exhibit resilience to CHABs.

Host food resource supplementation increases echinostome infection in larval anurans.

Host-parasite interactions are often influenced by environmental factors through multiple mechanisms. For example, changes in host food resources may affect multiple host traits (e.g., body size, behavior, immunocompetence), which may increase or decrease infection levels and the impact of parasites on host fitness. We often lack an understanding of which traits are most important for parasite transmission and fitness effects, posing challenges to predicting consequences of changing environmental conditions (e.g., eutrophication). Here, I examined the effects of food resources and host traits experimentally in a larval frog (Rana clamitans Latreille, 1801)-trematode parasite (Echinostoma revolutum Looss, 1899) system. I hypothesized that higher food resources reduce parasite infection and parasite effects on host growth and survival, due to increased host investment in parasite defenses, which I tested in a laboratory experiment. Contrary to my hypothesis, the results indicated that increased food levels enhanced infection in hosts, while the effect of parasites on survival did not depend on host food resources. A potential explanation for the positive effect of food level on infection was size-dependent infection rates (i.e., higher food levels increased infection through increased host growth), which is supported by a positive relationship between host body size and infection. These findings emphasize the complex relationship between host food resources and parasitism and the importance of environmental context and host traits (i.e., body size) in mediating interactions with parasites. The results also have relevance for conservation in light of rising anthropogenic impacts on aquatic systems and recent amphibian declines.

Identification of Putative Coffee Rust Mycoparasites via Single-Molecule DNA Sequencing of Infected Pustules.

The interaction of crop pests with their natural enemies is a fundament to their control. Natural enemies of fungal pathogens of crops are poorly known relative to those of insect pests, despite the diversity of fungal pathogens and their economic importance. Currently, many regions across Latin America are experiencing unprecedented epidemics of coffee rust (Hemileia vastatrix). Identification of natural enemies of coffee rust could aid in developing management strategies or in pinpointing species that could be used for biocontrol. In the present study, we characterized fungal communities associated with coffee rust lesions by single-molecule DNA sequencing of fungal rRNA gene bar codes from leaf discs (≈28 mm(2)) containing rust lesions and control discs with no rust lesions. The leaf disc communities were hyperdiverse in terms of fungi, with up to 69 operational taxonomic units (putative species) per control disc, and the diversity was only slightly reduced in rust-infected discs, with up to 63 putative species. However, geography had a greater influence on the fungal community than whether the disc was infected by coffee rust. Through comparisons between control and rust-infected leaf discs, as well as taxonomic criteria, we identified 15 putative mycoparasitic fungi. These fungi are concentrated in the fungal family Cordycipitaceae and the order Tremellales. These data emphasize the complexity of diverse fungi of unknown ecological function within a leaf that might influence plant disease epidemics or lead to the development of species for biocontrol of fungal disease.

Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival.

Parasites and predators can have complex, nonadditive effects on a shared group of victims, which can have important consequences for population dynamics. In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate (Anax) predators on the survival of larval green frogs (Rana clamitans). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. Results of the follow-up experiments suggest that increased predation susceptibility due to elevated activity levels in the presence of free-swimming parasite infective stages (i.e., an avoidance response) is the most likely mechanism responsible for the observed synergism. These results suggest a potential trade-off in susceptibility to parasites and predators, which can drive nonadditive effects that may have important consequences for natural enemy interactions in natural populations and amphibian conservation.