Search

This study surveyed gregarine parasites that infect the amphipod, Gammarus fasciatus , to investigate temporal dynamics in infracommunity structure. We sampled a population of hosts for 2 yr from the north branch of the Raritan River in New Jersey. These hosts were infected with 2 direct life cycle gregarine parasites, Rotundula gammari and Heliospora longissima. Infections were separated temporally, with the prevalence of R. gammari peaking within the amphipod population in the fall (prevalence = 78% year 1 and 97% year 2) and H. longissima peaking in early spring (prevalence = 41% year 1 and 52% year 2). Increases in host population density did not significantly correlate with the abundance of these 2 parasites. However, H. longissima abundance was positively correlated with host body weight while R. gammari showed no significant relationship. The mean body mass of amphipods infected with H. longissima was 20.7 ± 1. 2 mg, and with R. gammari 8.1 ± 0.2 mg, which suggests a sized-based infection pattern. Mixed species infections were infrequent with an overall prevalence of 4.6%. When both gregarine species co-infected the same host, the R. gammari but not the H. longissima infrapopulation size was significantly lower when compared to single-species infections, suggesting asymmetric interactions. We conclude that the observed temporal patterns of infection by the 2 parasites are driven by a seasonal change in host demographics and size-dependent infections. We argue that specificity for host developmental stages may have arisen as a mechanism to avoid overlap between these gregarine species.

Habitat is frequently implicated as a powerful determinant of community structure and species distributions, but few studies explicitly evaluate the relationship between habitat-based patterns of species' distributions and the presence or absence of trophic interactions. The complex (multi-host) life cycles of parasites are directly affected by these factors, but almost no data exist on the role of habitat in constraining parasite-host interactions at the community level. In this study the relationship(s) between species abundances, distributions and trophic interactions (including parasitism) were evaluated in the context of habitat structure (classic geomorphic designations of pools, riffles and runs) in a riverine community (Raritan River, Hunterdon County, NJ, USA). We report 121 taxa collected over a 2-year period, and compare the observed food web patterns to null model expectations. The results show that top predators are constrained to particular habitat types, and that species' distributions are biased towards pool habitats. However, our null model (which incorporates cascade model assumptions) accurately predicts the observed patterns of trophic interactions. Thus, habitat strongly dictates species distributions, and patterns of trophic interactions arise as a consequence of these distributions. Additionally, we find that hosts utilized in parasite life cycles are more overlapping in their distributions, and this pattern is more pronounced among those involved in trophic transmission. We conclude that habitat structure may be a strong predictor of parasite transmission routes, particularly within communities that occupy heterogeneous habitats.

The establishment of parasites with complex life cycles is generally thought to be regulated by free-living species richness and the stability of local ecological interactions. In this study, we test the prediction that stable host communities are prerequisite for the establishment of complex multi-host parasite life cycles. The colonization of naïve killifish, Fundulus heteroclitus, by parasites was investigated in 4 salt marsh sites that differed in time since major ecological restoration, and which provided a gradient in free-living species richness. The richness of the parasite community, and the rate at which parasite species accumulated in the killifish, were similar between the low diversity unrestored site and the two high diversity (10- and 20-year) restored marsh sites. The parasite community in the newly restored marsh (0 year) included only directly-transmitted parasite species. To explain the paradox of a low diversity, highly invaded salt marsh (unrestored) having the same parasite community as highly diverse restored marsh sites (10 and 20 yrs) we assessed qualitative community stability. We find a significant correlation between system stability and parasite species richness. These data suggest a role for local stability in parasite community assembly, and support the idea that stable trophic relationships are required for the persistence of complex parasite life cycles.

This study examined the relationship between the metazoan parasite community in a focal species, Fundulus heteroclitus , and the species richness of the free-living community. Four distinct salt marsh areas were selected in order to reflect a gradient in free-living species richness and time post-restoration (unrestored, 0, 10, and 20 yr post-restoration). A total of 960 fish was studied, with 30 collected per site in each of 8 consecutive seasons between 2005 and 2007. Species richness and abundance of birds, fish, and benthic macroinvertebrates varied significantly between sites. However, increasing richness in the free-living community was neither positively nor negatively correlated with richness in the parasite infracommunity in F. heteroclitus . These results demonstrate that the relationship between community species richness and parasite richness is not linear. The data suggest that the diversity of parasites may be more correlated with measures of community composition, such as the structure and cohesiveness of the food web, rather than with prevailing measures of biodiversity.

This study assessed the risk of larval displacement of the eastern treehole mosquito, Aedes triseriatus, and the northern house mosquito, Culex pipiens, by Aedes albopictus, the Asian tiger mosquito, during the establishment and successional stages of novel larval mosquito treehole and ground-container habitats in the state of New Jersey, U.S.A. Culex pipiens and Culex restuans were the first mosquito species to colonize ground-container habitats and were the dominant larval species throughout the study period, whereas Ae. albopictus was late to colonize ground habitats and accounted for less than 15% of weekly larval collections once established. Ae. albopictus had a much stronger community presence within treehole ovitraps; however, Ae. albopictus never reached the average larval densities of the expected primary colonizer, Ae. triseriatus. Throughout the study period, the weekly abundances of Ae. triseriatus and Ae. albopictus were positively correlated and there were no significant differences between the abundances of each species. The larval dominance of Ae. triseriatus appears to be enhanced by the presence of Toxorhynchites rutilus septentrionalis, a large predatory mosquito species. When Tx. rut. septentrionalis was present, mature larvae (3(rd) -4(th) instar) of Ae. albopictus were also present in only 16.7% of collections, whereas mature larvae of Ae. triseriatus were collected concurrently with Tx. rut. septentrionalis in 53.8% of collections. These data suggest that Ae. triseriatus is at a greater risk of displacement by Ae. albopictus than are Cx. pipiens and Cx. restuans., (© 2013 The Society for Vector Ecology.)

ABSTRACT This study looked at the influence of interannual variations in temperature and precipitation on seasonal mosquito abundances, the prevalence of West Nile virus (family Flaviviridae, genus Flavivirus, WNV) in the northeastern United States, and the capacity for local mosquito communities to maintain and transmit WNV, defined as vector community competence. Vector and virus surveillance took place within Middlesex County in New Jersey over two transmission seasons (2010 and 2011). Drought conditions during the 2010 season were associated with significant increases in the number of blood-fed Culex spp. mosquitoes collected per week, and significant increases in vector community competence, or the ability of local vector communities to transmit WNV, when compared with the wetter and milder 2011 season. These increases were associated with significantly higher weekly WNV infection rates in Culex spp. (i.e., Culex pipiens L. and Culex restuans L.) during the 2010 drought season. On a larger scale, the positive influence of drought on the amplification of WNV was also confirmed at the state level where early seasonal (June-July) increases in temperature and decreases in precipitation were strongly correlated with increases in yearly WNV infection rates over a 9-yr period (2003-2011). These data suggest that there may be clear temperature and precipitation thresholds beyond which epidemic levels of WNV transmission occur.

This review explores some of the reasons why food webs seem to contain relatively few parasite species when compared to the full diversity of free living species in the system. At present, there are few coherent food web theories to guide scientific studies on parasites, and this review posits that the methods, directions and questions in the field of food web ecology are not always congruent with parasitological inquiry. For example, topological analysis (the primary tool in food web studies) focuses on only one of six important steps in trematode life cycles, each of which requires a stable community dynamic to evolve. In addition, these transmission strategies may also utilize pathways within the food web that are not considered in traditional food web investigations. It is asserted that more effort must be focused on parasite-centric models, and a central theme is that many different approaches will be required. One promising approach is the old energetic perspective, which considers energy as the critical resource for all organisms, and the currency of all food web interactions. From the parasitological point of view, energy can be used to characterize the roles of parasites at all levels in the food web, from individuals to populations to community. The literature on parasite energetics in food webs is very sparse, but the evidence suggests that parasite species richness is low in food webs because parasites are limited by the quantity of energy available to their unique lifestyles.

This study investigated the impacts of urban wetlands and their adjacent residential environments on the transmission dynamics of West Nile virus (WNV) within the state of New Jersey (USA). A working hypothesis was that urban wetlands decrease the local prevalence of WNV through the dilution effect from increased bird diversity, and through relative reductions in the numbers of competent avian host and mosquito species commonly associated with WNV. Surveys of mosquito and bird communities were undertaken at six urban wetlands and their adjacent residential environments over two seasons (2009, 2010). The community compositions of both avian and mosquito species differed significantly across habitats, and over relatively short geographical distances. Residential areas contained significantly higher proportions of WNV-competent mosquito species (31.25±5.3 %; e.g. Culex pipiens and Culex restuans) , and WNV-competent avian host species (62.8±2.3 %, e.g. House Sparrow and American Robin) when compared to adjacent urban wetlands (13.5±2.1 %; 35.4±2.1 % respectively). Correspondingly, WNV infection rates within local Culex spp. populations indicate that WNV was more prevalent within residential areas (28.53/1000) compared to wetlands (16.77/1000). Large urban wetlands (>100 ha) produced significantly lower weekly WNV infection rates in local Culex spp. (6.67±2.84/1000) compared to small (<15 ha) wet-lands (22.57±6.23/1000). Avian species richness was also influenced by patch size. Large urban wetlands contained significantly more species than small wetland patches. These results confirm that the community compositions of mosquito and avian hosts are important drivers in WNV infections, and that the ecological conditions that favor transmission are more strongly associated with urban residential environments than with adjacent urban wetlands.

Several studies have suggested that the fitness of a parasite can be directly impacted by the quality of its host. In such cases, selective pressures could act to funnel parasites towards the highest-quality hosts in a population. The results of this study demonstrate that snail host quality is strongly correlated with spatial patterning in trematode infections and that habitat type is the underlying driver for both of these variables. Two trematodes (Himasthla quissetensis and Zoogonus rubellus) with very different life cycles assume the same spatial infection pattern in populations of the first intermediate host (Ilyanassa obsoleta) in coastal marsh habitats. Infected snails are disproportionately recovered from intertidal panne habitats, which offer more hospitable environs for snails than do adjacent habitats (intertidal creeks, coastal flats, and subtidal creeks), in terms of protection from turbulence and wave action, as well as the availability of food stuffs. Snails in intertidal panne habitats are of higher quality when assessed in terms of average size-specific mass, growth rate, and fecundity. In mark-recapture experiments, snails frequently dispersed into intertidal pannes but were never observed leaving them. In addition, field experiments demonstrate that snails confined to intertidal panne habitats are disproportionately infected by both trematode species, relative to conspecifics confined to adjacent habitats. Laboratory experiments show that infected snails suffer significant energetic losses and consume more than uninfected conspecifics, suggesting that infected snails in intertidal pannes may survive better than in adjacent habitats. We speculate that 1 possible mechanism for the observed patterns is that the life cycles of both trematode species allows them to contact the highest-quality snails in this marsh ecosystem.

Background: Parasites significantly alter topological metrics describing food web structure, yet few studies have explored the relationship between food web topology and parasite diversity., Methods/principal Findings: This study uses quantitative metrics describing network structure to investigate the relationship between the topology of the host food web and parasite diversity. Food webs were constructed for four restored brackish marshes that vary in species diversity, time post restoration and levels of parasitism. Our results show that the topology of the food web in each brackish marsh is highly nested, with clusters of generalists forming a distinct modular structure. The most consistent predictors of parasite diversity within a host were: trophic generality, and eigenvector centrality. These metrics indicate that parasites preferentially colonise host species that are highly connected, and within modules of tightly interacting species in the food web network., Conclusions/significance: These results suggest that highly connected free-living species within the food web may represent stable trophic relationships that allow for the persistence of complex parasite life cycles. Our data demonstrate that the structure of host food webs can have a significant effect on the establishment of parasites, and on the potential for evolution of complex parasite life cycles.

This review examines the historical origins of food web theory and explores the reasons why parasites have traditionally been left out of food web studies. Current paradigms may still be an impediment because, despite several attempts, it remains virtually impossible to retrofit parasites into food web theory in any satisfactory manner. It seems clear that parasitologists must return to first principles to solve how best to incorporate parasites into ecological food webs, and a first step in changing paradigms will be to include parasites in the classic ecological patterns that inform food web theory. The limitations of current food web models are discussed with respect to their logistic exclusion of parasites, and the traditional matrix approach in food web studies is critically examined. The well-known energetic perspective on ecosystem organization is presented as a viable alternative to the matrix approach because it provides an intellectually powerful theoretical paradigm for generating testable hypotheses on true food web structure. This review proposes that to make significant contributions to the food web debate, parasitologists must work from the standpoint of natural history to elucidate patterns of biomass, species abundance, and interaction strengths in real food webs, and these will provide the basis for more realistic models that incorporate parasite dynamics into the overall functional dynamics of the whole web. A general conclusion is that only by quantifying the effects of parasites in terms of energy flows (or biomass) will we be able to correctly place parasites into food webs.

The presence or absence of parasites within host populations is the result of a complex of factors, both biotic and abiotic. This study uses a non-parametric classification tree approach to evaluate the relative importance of key abiotic and biotic drivers controlling the presence/absence of parasites with complex life cycles in a sentinel, the common killifish Fundulus heteroclitus. Parasite communities were classified from 480 individuals representing 15 fish from 4 distinct marsh sites in each of 4 consecutive seasons between 2006 and 2007. Abiotic parameters were recorded at continuous water monitoring stations located at each of the 4 sites. Classification trees identified the presence of benthic invertebrate species (Gammarus sp. and Littorina sp.) as the most important variables in determining parasite presence: secondary splitters were dominated by abiotic variables including conductance, pH and temperature. Seventy percent of hosts were successfully classified into the correct category (infected/uninfected) based on only these criteria. The presence of competent definitive hosts was not considered to be an important explanatory variable. These data suggest that the most important determinant of the presence of these parasite populations in the common killifish is the availability of diverse communities of benthic invertebrates.

Relatively few published food webs have included parasites, and in this study we examined the animal community in a stream across eight contiguous seasons to test how inclusion of helminth parasites alters the topology or structure of the food web. Food webs constructed for each season and analyzed using common binary matrix measures show that species richness, linkage density, and the number of observed and possible links increased when parasites were included as individual species nodes. With parasite-parasite and predator-parasite links omitted, measures of community complexity, such as connectance (C), generally increased over multiple seasons. However, relative nestedness (n*) decreased when parasites were included, which may be a result of low resolution of basal resources inflating specialist-to-specialist links. Overall, adding parasites resulted in moderate changes in food web measures when compared to those of four other published food webs representing different ecosystems. In addition, including parasites in the food web revealed consistent pathways of energy flow, and the association of parasite life histories along these pathways suggest stable evolutionary groups of interacting species within the community.

Changes to host behaviour as a consequence of infection are common in many parasite-host associations, but their effects on the functional role hosts play within ecosystems are rarely quantified. This study reports that helminth parasites significantly decrease consumption of detritus by their isopod hosts in laboratory experiments. Natural host and parasite densities across eight contiguous seasons were used to estimate effects on the amount of stream detritus-energy processed. Extrapolations using mass-specific processing rates from laboratory results to field patterns suggest that the effects of the parasites occur year round but the greatest impact on the amount of detritus processed by isopods occurs in the autumn when the bulk of leaf detritus enters the stream, and when parasite prevalence in the isopod population is high. Parasites have a lesser impact on the amount of detritus processed in spring and summer when isopods are most abundant, when parasite prevalence is not high, and when fish predation on isopods is high. These results support the idea that parasites can affect the availability of resources critical to other species by altering behaviours related to the functional role hosts play in ecosystems, and suggest that seasonality may be an important factor to consider in the dynamics of these parasite-host interactions.

The composition and diversity of metazoan parasite communities in naturally depauperate ecosystems are rarely studied. This study describes the composition of helminth endoparasite communities infecting fish that are part of naturally acidic stream ecosystems in the coastal-plains region of the State of New Jersey (USA) known as the Pinelands, and compares the diversity of parasites between six streams that differ in anthropogenic disturbance. A total of 514 fish were examined representing 6 species native but restricted to the Pinelands region, 5 species native and widespread throughout the region and State, and 6 species introduced to the Pinelands and State. Fish (prevalence: 78%) were infected with 18 helminth endoparasite species. In most streams, prevalence of infection, mean abundance, and total number of individuals for the 5 most common parasites were higher in pirate perch, a native fish species. The diversity of helminth endoparasite communities measured as species richness and Shannon index was higher in degraded streams, and especially in native or introduced fish at these sites. Parasite diversity was positively correlated with anthropogenic disturbance, which was measured by water pH, water conductance, and the proportion of agricultural and developed land surrounding streams. Helminth community composition included parasites intimately tied to trophic interactions in food webs, and disturbance to these ecosystems results in changes to these communities. Understanding structure and function of animal communities from these naturally depauperate ecosystems is important before continued anthropogenic changes result in the extirpation or extinction of their unique fauna.

This study demonstrates that infective-stage larvae of 2 trichostrongyle ruminant gastrointestinal nematodes, Haemonchus contortus and Trichostrongylus colubriformis, can enter into anhydrobiotic states when completely desiccated. Larvae of control trichostrongyle species, Heligmosomoides polygyrus and Nippostrongylus brasiliensis, that infect mice were unable to survive desiccation or to enter into anhydrobiosis. Ruminant larvae were able to survive up to 7 desiccation/rehydration cycles, and, during anhydrobiosis, metabolic activity was decreased and survival of the larvae was prolonged both in the laboratory and in the field. Relative humidity had no effect on ruminant larval survival after anhydrobiosis compared with controls. Temperature had a significant effect, 85.8 +/- 2.3% of larvae in anhydrobiosis could survive low temperatures (0 C) that killed all control larvae. Metabolic activity, measured by changes in lipid content and CO2 respiration, was significantly lower in larvae that entered anhydrobiosis compared with controls (P < 0.05). In field experiments using open-meshed chambers under ambient environmental conditions, larvae in anhydrobiosis had significantly higher survival rates in the field compared with controls (P < 0.05) during summer and winter trials. These data suggest that anhydrobiosis in ruminant larvae promotes survival at freezing temperatures, decreases metabolic activity, and prolongs survival under natural field conditions.

This paper considers how fixed behaviours may play a role in post-larval migrations of Entobdella soleae. A general argument is that a shift away from the paradigm of orientation is required to elucidate the mechanisms that parasites use to navigate on the surface of their hosts. Some migrations may rely on fixed behaviours (genetically programmed stereotyped behaviours) that often evolve under predictable environmental conditions with reliable signals. In turbulent and stochastic free-living environments, homeostatic hosts present very predictable topological substrates and physico-chemical characteristics to their parasites. Over the course of evolution on these predictable host substrates, adaptive behaviours in the parasites can become fixed. Examples of endoparasite migration behaviour, particularly that of the common liver fluke, Fasciola hepatica, will be used to develop an approach based on the perceptual worlds of migrating parasites. An important conclusion is that multi-disciplinary approaches, firmly rooted in an understanding of each parasite's natural history, are requisite to successful interpretation of migration behaviours on the host.

The gastrointestinal nematode Nippostrongylus brasiliensis is thought to feed on host ingesta, and it is generally thought that the presence of ingesta determines the distribution of this parasite within the host intestine. However, these assertions have not been supported by direct evidence. The purpose of this study was to test the hypothesis that N. brasiliensis worms are preferentially found in regions of the host small intestine containing ingesta. The relationship between worm and ingesta distribution was investigated using mice infected with N. brasiliensis and killed on day 8 postinfection at 0130, 0730, 1330, or 1930 hr. There was an inverse relationship between worm and ingesta distributions, and the worms were distributed significantly more anteriad in the intestine than host ingesta, at all times during the 24 hr. To determine what the worms fed on, host ingesta, tissue, and blood were differentially labeled with the fluorescent dyes rhodamine B and Fluoresbrite. The results of this study suggest that N. brasiliensis feeds on the host's intestinal wall, and that habitat distribution of this parasite within the small intestine is not directly related to the presence of luminal ingesta.

Microparasite virulence (the potential to cause harm in the host) is thought to be regulated by a direct trade-off with pathogen transmission potential, but it is unclear whether similar trade-offs occur in macroparasites (helminths). In this analysis, the transmission potentials of 5 nematode species (order Strongylida), known to differ in their virulence, were estimated using an index based on egg production and larval survivability. Virulence estimates were based on the minimum number of worms that cause host death. In nematode species where mature adults cause pathology (trichonematidic development), there is a direct relationship between virulence and transmission, suggesting that high virulence is related to parasite fitness in these worms. However, in nematodes where the juvenile stages produce pathology during migration and development (strongylidic development), virulence is not correlated with transmission. These data suggest that trade-offs between transmission and virulence in nematode parasites are not analogous for all species and may depend on the developmental strategy and mechanism of pathogenicity of the parasites.

Infective larvae (L3) of Strongylus vulgaris have limited energy stores for host finding and for infection. For transmission to occur, the larvae must have sufficient energy to (a) migrate onto grass, where they are ingested by their equine host (host finding), and (b) penetrate into the host gut. This study is designed to test the hypothesis that L3 larvae of S. vulgaris partition their energy stores between locomotory activity (used in host finding) and infection activity (penetration). Chronic locomotory activity was stimulated by incubating S. vulgaris L3 larvae at a constant temperature (38 C). After 8 days of treatment, locomotory activity ceased (exhaustion). Exhausted L3 larvae had significantly decreased total lipid when compared to controls (P < 0.05), but there was no decrease in levels of protein of carbohydrate. Lipids of S. vulgaris L3 larvae are comprised of 9 fatty acids, some of which are depleted in exhausted worms (14:0, 14:1, 16:0, 16:1, 18:1, 18:2), whereas others (18:0, 20:4, 24:0) remain unchanged. These data suggest that specific fatty acids provide the energy source for locomotory activity in S. vulgaris. Exhausted L3 larvae were also less able to penetrate host cecal tissue in in vitro penetration assays when compared to controls (P < 0.05), suggesting that the depletion of individual fatty acids during locomotory activity also reduced infectivity. These data do not support the hypothesis that S. vulgaris L3 larvae partition their energy stores between host-finding and infection activities. A comparison of lipid storage profiles in the L3 larvae of 4 nematode species with similar transmission strategies (S. vulgaris, Strongylus edentatus, Strongylus equinus, and Haemonchus contortus) revealed similarities in the fatty acid composition of these species. These data suggest a relationship between transmission patterns and energy storage strategies in the L3 larvae of nematode parasites of vertebrates.

Heligmosomoides polygyrus is a gastrointestinal nematode whose adult distribution is restricted to the duodenal region in the small intestine of the mouse. This study tests the hypothesis that the habitat of these parasitic worms is influenced by fixed (architectural) cues in the small intestine of the vertebrate host, and that H. polygyrus adults will select microhabitats containing the longest villi. H polygyrus adults attach by coiling around the villi, and longer villi may provide greater attachment resources. In addition, these parasites feed on the epithelial cells covering the villi and thus, longer villi may also provide more food resources. Using histological methods, this study identified a gradient of villus length in the small intestine of the mouse where the longest villi were found in the duodenum and shortest in the ileum. Several non-surgical and surgical treatments were used to differentially alter the overall lengths of the villi. These treatments produced a significant negative correlation between villus length and worm distribution, with the worms selecting regions with the relatively longest villi in the small intestine. Attachment and feeding sites are crucial resources for this parasite, and these data suggest that villus length may be a reliable indicator of resource quality, and that decisions on habitat suitability by H. polygyrus adults may depend on this single, topological variable.

Habitat selection may be the basis of some of the most exciting questions in behavioural ecology today, but parasites are being excluded from this debate. Parasites are not aberrant; they form a large proportion of the diversity of life on earth, and one estimate suggests that parasitism is more common than all other feeding strategies combined. We still do not understand the adaptive value of habitat selection behaviours in these organisms, even though the literature is full of examples of parasites migrating and navigating through hosts to their specific habitats. Parasites must make the same decisions that every animal has to make regarding food acquisition, shelter and reproduction. However, we cannot even make reasonable guesses on the habitat selection strategies and critical resources that influence their decision-making. The purpose of this review is to provide examples of experiments and methods of incorporating critical resources into the ecological analyses of habitat selection by gastrointestinal parasites. Information on parasite resources is simply not available for most parasites, and these ideas might stimulate and guide future research. In addition, parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasite populations are simple, and habitats of endoparasites can be precisely altered by surgical methods. Few tests of habitat selection theory have been attempted in free-living environments because of the difficulty of assessing the correlations between environmental variations and organismal success in real-world situations, but this is not a problem with parasites because their habitats are replicated exactly in each host.

Grooming behavior may play a part in the transmission of the gastrointestinal nematode, Heligomosomoides polygyrus in the mouse host. After infective larvae are placed on individually housed mice, significantly higher numbers of adult worms were recovered from the small intestine of mice that were allowed to self-groom when compared to infection levels in mice that had been fitted with Elizabethan collars to prevent self-grooming. Larvae placed on a single mouse housed with 3 other untreated mice resulted in all mice in the group becoming infected, suggesting that allogrooming may also be important in parasite transmission. A significantly higher percentage of larvae nictate on rough surfaces such as damp peat moss substrate when compared to smooth surfaces such as 0.5% agarose. Mice exposed to larvae placed on peat moss substrate have significantly higher infection levels when compared to mice exposed to larvae on a 0.5% agarose substratum, suggesting that natural transmission of infective L3 larvae in mice may be dependent on a substratum type that allows nictation behavior. A significantly higher percentage of worms were attracted to mouse urine and mouse and rat epidermal lipids when compared to deionized water controls in an in vitro preference assay, suggesting an attraction to host-specific signals. These results support the hypothesis that transmission of this parasite is an active process involving movement of the infective larvae of H. polygyrus into the host's active space where they are ingested during grooming behavior.

Mesenchyme cells and their processes are found in the cerebral ganglia of the parasitic flatworm, Fasciola hepatica. The mesenchyme cell processes are found in two specialized associations within the ganglion: (i) as lamellae-like multilayer sheaths encircling the cerebral ganglia and separating it from the surrounding parenchyma cells, and (ii) invaginated into the surface of large diameter ('giant') nerve processes to form trophospongium-like relationships. Based on morphological criteria, these mesenchyme cells resemble general invertebrate glial cells suggesting that the mesenchyme cells of these flatworms may represent the earliest glial-like cell.

The aim of this study was to identify the food resources of Heligmosomoides polygyrus, a gastrointestinal nematode of mice. Gastrointestinal nematodes obtain food from 1 of 3 compartments: host ingesta, blood, or intestinal tissue. A method was developed to label these compartments differentially in the living host using 2 fluorescent marker dyes and to record in situ feeding activity of the parasite. Fluoresbrite is a yellow-green fluorescent dye bound to small-diameter beads that are membrane impermeable. Thus, it is restricted to the bloodstream when introduced there, or it remains in the ingesta when fed to the host. Rhodamine B, a red fluorescent dye, is membrane permeable and stains tissue cytoplasm. These dyes were fed to or injected into the bloodstream of the host. Following treatment, the worms were removed, and the contents of the worm intestines were examined by fluorescent microscopy. Worm intestinal contents only fluoresced with rhodamine B dye. These results suggest that H. polygyrus adults feed on tissue in the living host and not on host ingesta or blood.

Helminth parasites of vertebrates usually select very specific regions or habitats in their hosts, and this is often preceded by a tortuous migration through various host organs. However, the proximate mechanisms of migration and habitat selection have remained enigmatic despite considerable effort by parasitologists. In this paper a new approach to studying helminth behaviour in the host is proposed. The core idea is that behaviour strategies must be considered from the perspective of the parasites and their perceptions of their environment. A guiding principle is that the environmental features to which an animal responds, and the actions which are required for responding to the environment, form a fundamental unit of behaviour. Thus, we can deduce an animal's behavioural strategy from the details of its response to environmental signals and from its sensory capabilities. The evidence presented suggests that helminth behaviours in the host often occur as fixed (or modal) action patterns which are usually seen in response to constant, or predictable environmental features. Thus, a working hypothesis is that the mechanisms of physiological and biochemical homeostasis within the host provide an extremely predictable environment for the parasite. Under these conditions, a parasite needs to perceive only small subsets of the total information available from the environment to respond appropriately. Studies on sensory and nervous systems of these organisms are critical to understanding parasite perception, but there are formidable technical obstacles that prevent easy access to parasite nervous systems. Therefore, a multidisciplinary approach, using ideas from parasitology, ecology, evolutionary biology and neuroethology, is considered requisite for reconstructing the parasites' behaviour strategies. It is suggested that future directions should pursue integration of studies on sensory physiology with the behavioural ecology of these organisms.

The localization of FMRFamide-related peptide (FaRP) immunoreactivity was determined during different stages of development of the rat tapeworm Hymenolepis diminuta. In the adult worm (14 days old), FaRP immunostaining was most intense in the scolex and concentrated in the central nervous system (cerebral ganglia and transverse commissures) and around the lips of the suckers. In the strobila, medial and lateral longitudinal nerve cords (LNCs) and ladder-like connecting commissures were the only tissue stained. Immunoreactivity in the medial LNCs of the adult tapeworms extended only to and included proglottides containing developing testis and seminal receptacle but disappeared in proglottides in which primordial ovaries were first detected. Radioimmunoassay confirmed that FaRPs were concentrated in the scolex/neck region of the adult worm (3.9 +/- 1.5 pmol mg protein-1), whereas the lowest concentrations (0.2 +/- 0.19 pmol mg protein-1) were recovered from the regions of the strobila containing shelled eggs. The pattern of FaRP immunoreactivity observed in 5- and 7-day-old worms was similar to that seen in adult worms, but in 2- and 3-day-old worms the pattern of immunoreactivity observed in the cerebral ganglia, transverse commissures, and LNCs differed significantly as compared with that seen in older worms. These results indicate differential utilization and/or roles for FaRPs during development and suggest both central and sensory roles in this tapeworm.

The aim of this study was to determine if intestinal contractions were important in the migration behaviour of the rat tapeworm Hymenolepis diminuta. The objectives were to investigate the intestinal motility responses of the host to a meal which initiates worm migration, and the worms' responses to an artificial peristaltic contraction. A 1 g glucose meal elicited a significant orad migration by H. diminuta in the small intestine of the rat host when compared to water-fed controls (P less than 0.05). The glucose meal also significantly increased the transit rate, and thus, frequency of intestinal contractions in the small intestine of the rat, when compared to water-fed controls (P less than 0.05). Application of a circumintestinal ligature (6.3 g) (simulating an intestinal peristaltic contraction) resulted in significant worm migration when the ligature was applied in regions containing the worm's strobila as compared to controls where loose ligatures were tied in regions containing the strobila, or to controls where tight ligatures were tied ahead of the worm's strobila. These results suggest that H. diminuta migrates in an orad direction in response to the mechanical pressure produced by intestinal contractions induced by host feeding. It is concluded that contractions of the small intestine are an important cue in the migration behaviour of this cestode.

Hymenolepis diminuta propels itself with unidirectional peristaltic-like waveforms. When intact adult H. diminuta are placed in a thermal gradient, with the anterior proglottids hot relative to the posterior proglottids, the worms migrate up the gradient toward the hot side. When the anterior is cold, relative to the posterior, the worms moved slightly or little. These behaviors in a thermal gradient represent true thermokinetic responses for an organism with undirectional locomotion. Removal of the scolex, containing the worm's cerebral ganglia, did not significantly alter these thermal responses. These data suggest that the peripheral nervous system is capable of integrating sensory input over the length of the strobila and coordinating locomotory behavior, in the absence of the central nervous system.

Hymenolepis diminuta migrates up the small intestine in response to feeding the host 1 g of glucose. Locomotion during migration may result from fixed patterns of retrograde peristaltic-like waves in the strobila of the tapeworm which propel the organism against the normal expulsive forces in the small intestine. The peristaltic-like locomotory waves occur in a gradient along the strobila with a frequency of 24.9 +/- 0.9 cycles/min in the anterior segments of the worm, decreasing linearly to 6.6 +/- 1.4 cycles/min in the posterior segments of the worm. Chemical signals, isolated from the small intestine of fed hosts, which stimulate migration behaviour in vivo do not alter the behaviour of the scolex or strobila in vitro. Removal of the scolex containing the cerebral ganglia does not alter the frequency or pattern of locomotory activity in the strobila. After the worm is cut into pieces, each region generates the pattern of locomotory activity that is appropriate for that region. These data suggest that the peripheral nervous system, and not the central nervous system, is responsible for the coordination of the fixed patterns of locomotory activity in these tapeworms.

Adult female worms recovered from the jejunum of rats infected per os with 1000 larvae of Trichinella spiralis were significantly more fecund (peak jejunal fecundity = 35.7 +/- 3.1 newborn larvae per female) than females recovered from the terminal ileum (9.3 +/- 4.1 larvae per female) in the same infections. The majority of the adult worms were established in those sections of the small intestines that produced the most fecund females (r = 0.92; P less than 0.05). Worm fecundity is believed to be location-specific because adult females that were surgically implanted into the jejunum were significantly more fecund that were implanted into only the ileum. It is concluded that the physico-chemical conditions of the anterior small intestines are optimal for the parasites' reproductive fitness and this exerts a strong selective pressure on habitat selection behavior.

How do liver worms find the liver? Why are heartworms always found in the heart? Attempts to answer these questions have invariably yielded inconclusive results. A major problem has been the use of models or hypotheses derived from studies of free-living organisms. The parasite's environment is distinct from free-living environments in several fundamental ways and these differences will impact on the evolution of parasite behaviours. In this article, Michael Sukhdeo outlines a hypothesis for habitat selection behavior of helminths that is based on the specific environmental conditions within the host.

During ontogenetic development in the definitive host, the cerebral ganglia of the parasitic flatworm Fasciola hepatica lose their cell rind integrity and develop specialized nerve processes. The organization and cytological features of the central nervous system were examined during three developmental stages in the parasitic life cycle of F. hepatica to determine when the changes occur. The cerebral ganglion cell bodies of migrating juvenile worms (5 days post-infection) are organized into a one-cell-thick rind that surrounds a central neuropile composed of small unmyelinated nerve processes (less than 3 microns in diameter). In young, sexually-immature adult worms (30 days post-infection), the cell bodies of the ganglia are no longer organized into a complete or tight cell rind around the ganglia. In addition, large diameter ('giant') unmyelinated nerve processes (greater than 12 microns) are found in the neuropile area. These giant nerve processes are also found in the transverse commissure and the longitudinal nerve cords. In mature adult worms (4-6 months post-infection), the rind of nerve cell bodies has completely disappeared and cell bodies are scattered around and within the neuropile. More than half of the volume of the mature adult neuropile is composed of giant nerve processes. The three developmental stages of the parasite that were used in this study differ significantly in their sizes, behaviours and microhabitat locations in the host. The results suggest that the organizational and morphological changes in the ganglia reflect selective adaptations to changes in the parasitic microenvironment.

The behavioral repertoire of the infective stage of Fasciola hepatica was qualitatively characterized. During activation, a primary activity was the emptying of the ceca by peristaltic-like contractions. Emergence behavior comprised coordinated patterns of body movement and sucker activity specifically directed at disruption of the ventral plug. The stimulus specificity of the emergence response for glycine-conjugated cholic acid and the log dose-effect relationship of this response with glycocholic acid suggested a receptor-mediated sensory recognition. Extracts from the duodenum (departure organ) and the liver (arrival site) significantly affected the rate of locomotion and the orientation of the migratory stage. The evidence for orientation in the migrating stages is unequivocal, but the mechanisms by which they orient are unclear.

An ultrastructural study of the organization and fine structure of the nervous system of the parasitic flatworm Fasciola hepatica was undertaken. The brain consists of paired cerebral ganglia, located just posterior to the oral sucker, that are connected by a transverse commissure which crosses over the dorsal surface of the pharynx. The cell bodies of the cerebral ganglia are not organized into a clearly defined rind around the neuropile but are loosely scattered around and within the neuropile area. The neuropile consists of two morphologically distinct types of unmyelinated nerve processes. The small nerve processes, with smooth cell membranes, are less than 2 micron in diameter, whereas the "giant" processes are greater than 12 micron in diameter and have extensively invaginated cell membranes. Giant processes make up the bulk of the nerve fibers in the transverse commissure and longitudinal nerve cords. Four morphological types of vesicles are present in the small processes; small clear vesicles (which were found associated with synapses), spheroidal and ellipsoidal dense vesicles, and dense-core vesicles. Two types of synapses are found in the neuropile: simple synapses characterized by pre- and postsynaptic membrane densities, clusters of small clear vesicles, and a clear synaptic cleft; and wedge-shaped synapses or divergent diads each having one presynaptic process synapsing onto two postsynaptic processes. Synaptic contacts were observed only between small processes; no synapses were observed on the cell bodies or on giant processes.

Female CDI mice were inoculated with 10, 50, 100, 250, or 500 larvae of Heligmosomoides polygyrus. At Days 7, 9, and 12 after infection, the anterior third of the small intestine was perfused using an in vivo technique. The distribution of worms in the mouse intestine was determined after 7, 9, and 12 days. All worms that were recovered were from the proximal half of the small intestine. When compared to uninfected controls, there was a significant increase (+56%) in glucose absorption of the small intestine at Day 7 after infection with inocula of 50 and 100 larvae; at Day 9, glucose absorption was significantly increased with a 10-larvae inoculum. A decrease in glucose absorption occurred at Days 7 and 9 after infection with a 500-larvae inoculum. Net water absorption was significantly increased (+183%) with the 50- and 100-larvae inocula at Day 7, but was significantly reduced at Day 9 after infection with the 50-, 100-, 250-, and 500-larvae inocula. Both Cl- and Na+ absorption were significantly increased with the 50-, 100-, and 250-larvae inocula at Day 7 after infection; at 9 and 12 days, there was significant net secretion of both ions. In control mice, there was net secretion of K+, while with the 50-, 100-, and 250-larvae inocula on Day 7 there was significant net absorption of K+ ions.(ABSTRACT TRUNCATED AT 250 WORDS)

The effects of pharmacological concentrations of several gastrointestinal hormones on the rate of sucker activity and the frequency and the amplitude of spontaneous longitudinal muscle contractions have been examined in adult Fasciola hepatica. Caerulein and serum decrease the rate of oral sucker activity; motilin decreases and CCK-PZ increases ventral sucker activity when compared to controls. Caerulein, serum and motilin significantly inhibit the frequency of contractions while bile, caerulein and motilin decrease the amplitude of contractions. These results suggest that F. hepatica can recognize and respond to certain gastrointestinal hormones and there may be adaptive value in these behavioural responses.

Consistent in vitro behavioral patterns were found in the scolex and strobila of adult Hymenolepis diminuta. These patterns were measured with a force transducer and the behavior analyzed with a slow motion closed circuit T.V. Varying concentrations of serotonin (5-HT), acetylcholine (Ach), histamine and somatostatin, in the range of 10(-3) to 10(-9) M, were tested for their influence on the rhythmic patterns of behavior. High concentrations of 5-HT and of Ach decreased scolex motility. While 5-HT significantly increased motility in the anterior-, mid- and posterior regions of the strobila at 10(-3) M, Ach inhibited motility in all 3 regions of the strobila at the same concentrations. At high concentrations, somatostatin had a smaller stimulatory effect on worm motility in the anterior and mid-regions; histamine only significantly affected worm motility in the posterior region of the strobila. Depending on concentration, the action of 5-HT, Ach and histamine can be reversed, particularly in the anterior and posterior regions of the strobila. The in vivo assay for worm migrational responses suggests that the action of the neuromuscular stimulators and inhibitors on worm migration is indirect.

The rate of production of locomotory cycles in juvenile Fasciola hepatica was significantly decreased following treatment with conjugated chenodeoxycholic acids and significantly increased following treatment with dehydrocholic acid or whole bovine bile. Deoxycholic acid caused death and lysis of the parasites in less than 30 min. These results suggest that bile components act as a specific stimulus for a fixed action pattern (the locomotory cycle) in this parasite.

The head region of the trematode parasite Fasciola hepatica contains 3.47 +/- 0.42 pmol/mg wet wt. of serotonin as measured by high-performance liquid chromatography coupled to electrochemical detection. The head region includes the cerebral ganglia, the transverse commissure and associated nervous tissue that innervates the musculature of the oral sucker, pharynx and body wall. Tissue from the tail, which contains little nervous innervation, has approximately 20 times less serotonin (0.18 +/- 0.01 pmol/mg wet wt.). Immunohistochemistry was used to identify serotonin-like immunoreactive cells. Bipolar and multipolar cell bodies in the cerebral ganglia show serotonin-like immunoreactivity. Also evident are serotonin-like immunoreactive processes in the neuropile and in the transverse commissure that connects the ganglia, and immunoreactive peripheral bipolar cell bodies innervating the musculature of the pharynx and body wall. The cell bodies containing serotonin are organized in bilateral symmetry with homologous cell bodies and processes represented in each ganglion and on both sides of the pharynx.

Histological examination of the small intestine of mice infected with Heligmosomoides polygyrus indicates that the final site of the larvae is in the circular muscle layer of the muscularis externa of the anterior small intestine. The larvae become embedded in the muscle between the first and third days after infection and are subsequently sequestered by a localized leucocytic response. There is no evidence of a true cyst. Histological evidence suggests that the larvae actively feed on the tissues of the host during their development.

Acetylcholinesterase activity was found in the cell bodies and extracellularly in the neuropile of the cerebral ganglia of the adult trematode parasite, Fasciola hepatica. Within neuronal cell bodies of the cerebral ganglion, acetylcholinesterase reaction product was found in the endoplasmic reticulum, in the cisternae of the Golgi apparatus, and in secretory vesicles near the inner (releasing face) cisternae. Acetylcholinesterase reaction product was not seen intracellularly within any nerve processes. The reaction product was found around the somatic cell membranes and in the extracellular space between closely apposed nerve processes in the neuropile. Acetylcholinesterase reaction product was associated with synaptic endings that contained clear spheroidal synaptic vesicles, and the reaction product was localized at the site of synaptic contact between the zone of apposition of the pre- and postsynaptic terminals. This intracellular and extracellular distribution of the enzyme is consistent with its function as the degrading enzyme in cholinergic transmission.