Infection patterns and new definitive host records for New Zealand gordiid hairworms (phylum Nematomorpha)

Some parasites modify the phenotype of their host in order to increase transmission to another host or to an environment suitable for reproduction. This phenomenon, known as host manipulation, is found across many parasite taxa. Freshwater hairworms are known for the behavioural changes they cause in their terrestrial arthropod hosts, increasing their likelihood of entering water to exit the host and reproduce. Understanding how infected arthropods move around in the natural environment could help uncover alterations in spatial distribution or movement induced by hairworms in their terrestrial definitive hosts. Moreover, few hairworm-host records exist for New Zealand, so any additional record could help elucidate their true host specificity. Here, we investigated whether infected terrestrial arthropods were more likely to approach streams in two subalpine communities of invertebrates, using a spatial grid of specialised pitfall traps. Although hairworm infection could not explain the movements of arthropod hosts near streams, we found several new host records for hairworms, including the first records for the recently described Gordionus maori. We also found some new host-parasite associations for mermithid nematodes. These records show that the host specificity of hairworms is quite low, suggesting that their diversity and distribution may be greater than what is currently known for New Zealand.     

Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation

One of the most fascinating examples of parasite-induced host manipulation is that of hairworms, first, because they induce a spectacular "suicide" water-seeking behavior in their terrestrial insect hosts and, second, because the emergence of the parasite is not lethal per se for the host that can live several months following parasite release. The mechanisms hairworms use to increase the encounter rate between their host and water remain, however, poorly understood. Considering the selective landscape in which nematomorph manipulation has evolved as well as previously obtained proteomics data, we predicted that crickets harboring mature hairworms would display a modified behavioral response to light. Since following parasite emergence in water, the cricket host and parasitic worm do not interact physiologically anymore, we also predicted that the host would recover from the modified behaviors. We examined the effect of hairworm infection on different behavioral responses of the host when stimulated by light to record responses from uninfected, infected, and ex-infected crickets. We showed that hairworm infection fundamentally modifies cricket behavior by inducing directed responses to light, a condition from which they mostly recover once the parasite is released. This study supports the idea that host manipulation by parasites is subtle, complex, and multidimensional.     

Can parasites synchronise the population fluctuations of sympatric tetraonids? –examining some minimum conditions

Sympatric populations of tetraonid birds tend to fluctuate in synchrony, at least on local scales. If shared parasites among sympatric populations of different tetraonid species are to operate as a local, synchronizing factor for population fluctuations at least two conditions should be met: i) the host species should share the same (or similar) parasite species, and ii) geographical location should contribute significantly more to the variation in the parasite species composition and abundance than differences among host species. We examined these conditions among subpopulations of sympatric willow ptarmigan and rock ptarmigan and found that host species shared a common pool of parasite species, and geographic location was more important than host species in determining parasite abundance across locations. There was no time lag between density oscillations in the two hosts, suggesting a symmetrical pattern of transmission and maintenance of parasites within habitats governed by the density of hosts and the environment. These findings are consistent with the idea that parasites may play a role in generating synchronous density fluctuations, but large scale experiments are needed to verify this hypothesis.     

Temperature and multiple parasites combine to alter host community structure

Predicting the effects of climate change requires understanding complex interactions among multiple abiotic and biotic factors. By influencing key interactions among host species, parasites can affect community and ecosystem structuring. Yet, our understanding of how multiple parasites and abiotic factors interact to alter ecosystem structure remains limited. To empirically test the role of temperature variation and parasites in shaping communities, we used a multigenerational mesocosm experiment composed of four sympatric freshwater crustacean species (isopods and amphipods) that share up to four parasite species. Mesocosms were assigned to one of four different treatments with contrasting seasonal temperatures (normal and elevated) and parasite exposure levels (continuous and arrested (presence or absence of parasite larvae in mesocosm)). We found that parasite exposure and water temperature had interactive effects on the host community. Continuous exposure to parasites altered the community structure and differences in water temperature altered species abundance. The abundance of the amphipod Paracalliope fluviatilis decreased substantially when experiencing continuous parasite exposure and elevated water temperatures. Elevated temperatures also led to parasite-induced mortality in another amphipod host, Paracorophium excavatum. Contrastingly, isopod hosts were affected much less, suggesting increasing temperatures in conjunction with higher parasite exposure might increase their relative abundance in the community. Changes in invertebrate host populations have implications for other species such as fish and birds that consume crustaceans as well as having impacts on ecosystem processes, such as aquatic primary production and nutrient cycling. In light of climate change predictions, parasite exposure and rise in average temperatures may have substantial impacts on communities and ecosystems, altering ecosystem structure and dynamics.     

Large-scale patterns of host use by parasites of freshwater fishes

Organisms that are abundant locally in a habitat patch are commonly observed to be frequent regionally, or among patches. In parasites, species present in high numbers in host individuals are also present in many individuals in the host population. On a larger scale, however, when host species are considered as patches, we may expect the opposite pattern because of the cost of producing mechanisms to evade the immune responses of several host species. Thus parasite species exploiting many host species may achieve lower average abundance in their hosts than parasite species exploiting fewer host species. This prediction was tested with data from 188 species of metazoan parasites of freshwater fish, using a comparative approach that controlled for study effort and phylogenetic influences. A negative correlation was found between the number of host species used by parasites and their average abundance in hosts, measured as either prevalence or intensity of infection. There was no evidence that parasite species fall into distinct categories based on abundance patterns, but rather that they fall along a continuum ranging from a generally low abundance in many host species, to a generally high abundance in few host species. These results applied to both ecto- and endoparasites. The pattern observed suggests the existence of a trade-off between how many host species a parasite can exploit and how well it does on average in those hosts.     

Evidence that flatheaded mayflies (Heptageniidae) serve as the likely paratenic host for Chordodes morgani (Nematomorpha) in Nebraska

Hairworms (Nematomorpha) have indirect life cycles that require a terrestrial arthropod definitive host and an aquatic arthropod host that serves as a paratenic host, transferring the hairworm from the aquatic to the terrestrial environment. The life cycles for most hairworms remain unknown, especially the paratenic host. The hairworm Chordodes morgani lays its eggs on sticks, which are susceptible to the activity of aquatic insects such as larvae of the flatheaded mayfly (Heptageniidae), which feed by scraping algae and detritus. To test the likelihood that scrapers serve as the paratenic host for C. morgani, we collected sticks and their accompanying invertebrates from three sites near Lincoln, NE. We noted the presence of eggs of C. morgani on each stick, placed them in labeled resealable bags, and examined the invertebrates microscopically for the presence of hairworm cysts. We predicted that scrapers found on sticks with eggs of C. morgani will harbor the highest number of cysts. To confirm that larvae of the flatheaded mayfly serve as the aquatic host, we fed field-collected specimens to three captive-reared wood roaches (Parcoblatta pensylvanica). Of the three exposed roaches, one yielded nine individuals of C. morgani 63 days after exposure. Understanding the life cycle of this horsehair worm will allow researchers to rear the species in the lab, which could become a model for parasite research.     

An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence

Epidemiological models predict a positive relationship between host population density and abundance of macroparasites. Here I lest these by a comparative study. I used data on communities of four groups of parasites inhabiting the gastrointestinal tract of mammals, nematodes of the orders Oxyurida. Ascarida. Enoplida and Spirurida. respectively. The data came from 44 mammalian species and represent examination of 16886 individual hosts. I studied average prevalence of all nematodes within an order in a host species, a measure of community level abundance, and considered the potential confounding effects of host body weight, fecundity, age at maturity and diet. Host population density was positively correlated with parasite prevalence within the order Oxyurida, where all species have direct life cycles. Considering the effects of other variables did not change this. This supports the assumption that parasite transmission rate generally is a positive function of host population density_: It also strengthens the hypothesis that host densities generally act as important determinants of species richness among directly transmitted parasites and suggests that negative influence of such parasites on host population growth rate increase with increasing host population density among host species. Within the other three nematode orders, where a substantial number of the species have indirect life cycles, no relationships between prevalence and host population density were seen, Again. considering the effects of other variables did not affect this conclusion. This suggests that host population density is a poor predictor of species richness of indirectly transmitted parasites and that effects of such parasites on host population dynamics do not scale with host densities among species of hosts.     

Female biased sex-ratio in Schistosoma mansoni after exposure to an allopatric intermediate host strain of Biomphalaria glabrata

For parasites that require multiple hosts to complete their development, the interaction with the intermediate host may have an impact on parasite transmission and development in the definitive host. The human parasite Schistosoma mansoni needs two different hosts to complete its life cycle: the freshwater snail Biomphalaria glabrata (in South America) as intermediate host and a human or rodents as final host. To investigate the influence of the host environment on life history traits in the absence of selection, we performed experimental infections of two B. glabrata strains of different geographic origin with the same clonal population of S. mansoni. One B. glabrata strain is the sympatric host and the other one the allopatric host. We measured prevalence in the snail, the cercarial infectivity, sex-ratio, immunopathology in the final host and microsatellite frequencies of individual larvae in three successive generations.     

A nematomorph parasite explains variation in terrestrial subsidies to trout streams in Japan

Nematomorph parasites alter the behavior of their orthopteran hosts, driving them to water and creating a source of food for stream salmonids. We investigated whether nematomorphs could explain variation in terrestrial subsidies across several streams. In nine study streams, orthopterans comprise much of the stomach contents of trout (46 ± 31% on average). Total mass of ingested prey per trout biomass positively correlated with the mass of orthopterans ingested, suggesting that the orthopterans enhanced absolute mass of prey consumption by the trout population. The orthopterans ingested per trout biomass positively correlated with the abundance of nematomorphs in the stream, but not with the abundance of camel crickets (the dominant hosts) around the streams. Streams in conifer plantations had fewer nematomorphs than streams in natural deciduous forests. These results provide the first quantitative evidence that a manipulative parasite can explain variation in the allochthonous energy flow through and across ecosystems.     

Patterns of interactions of a large fish-parasite network in a tropical floodplain

1.?Describing and explaining the structure of species interaction networks is of paramount importance for community ecology. Yet much has to be learned about the mechanisms responsible for major patterns, such as nestedness and modularity in different kinds of systems, of which large and diverse networks are a still underrepresented and scarcely studied fraction. 2.?We assembled information on fishes and their parasites living in a large floodplain of key ecological importance for freshwater ecosystems in the Paraná River basin in South America. The resulting fish-parasite network containing 72 and 324 species of fishes and parasites, respectively, was analysed to investigate the patterns of nestedness and modularity as related to fish and parasite features. 3.?Nestedness was found in the entire network and among endoparasites, multiple-host life cycle parasites and native hosts, but not in networks of ectoparasites, single-host life cycle parasites and non-native fishes. All networks were significantly modular. Taxonomy was the major host's attribute influencing both nestedness and modularity: more closely related host species tended to be associated with more nested parasite compositions and had greater chance of belonging to the same network module. Nevertheless, host abundance had a positive relationship with nestedness when only native host species pairs of the same network module were considered for analysis. 4.?These results highlight the importance of evolutionary history of hosts in linking patterns of nestedness and formation of modules in the network. They also show that functional attributes of parasites (i.e. parasitism mode and life cycle) and origin of host populations (i.e. natives versus non-natives) are crucial to define the relative contribution of these two network properties and their dependence on other ecological factors (e.g. host abundance), with potential implications for community dynamics and stability.     

Disease management in two sympatric Apterostigma fungus‐growing ants for controlling the parasitic fungus Escovopsis

Antagonistic interactions between host and parasites are often embedded in networks of interacting species, in which hosts may be attacked by competing parasites species, and parasites may infect more than one host species. To better understand the evolution of host defenses and parasite counterdefenses in the context of a multihost, multiparasite system, we studied two sympatric species, of congeneric fungus‐growing ants (Attini) species and their symbiotic fungal cultivars, which are attacked by multiple morphotypes of parasitic fungi in the genus, Escovopsis. To assess whether closely related ant species and their cultured fungi are evolving defenses against the same or different parasitic strains, we characterized Escovopsis that were isolated from colonies of sympatric Apterostigma dentigerum and A. pilosum. We assessed in vitro and in vivo interactions of these parasites with their hosts. While the ant cultivars are parasitized by similar Escovopsis spp., the frequency of infection by these pathogens differs between the two ant species. The ability of the host fungi to suppress Escovopsis growth, as well as ant defensive responses toward the parasites, differs depending on the parasite strain and on the host ant species.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Life cycles shape parasite evolution: comparative population genetics of salmon trematodes

Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.     

Local adaptation, resistance, and virulence in a hemiparasitic plant-host plant interaction

Abstract.— Coevolution may lead to local adaptation of parasites to their sympatric hosts. Locally adapted parasites are, on average, more infectious to sympatric hosts than to allopatric hosts of the same species or their fitness on the sympatric hosts is superior to that on allopatric hosts. We tested local adaptation of a hemiparasitic plant, Rhinanthus serotinus (Scrophulariaceae), to its host plant, the grass Agrostis capillaris . Using a reciprocal cross-infection experiment, we exposed host plants from four sites to hemiparasites originating from the same four sites in a common environment. The parasites were equally able to establish haustorial connections to sympatric and allopatric hosts, and their performance was similar on both host types. Therefore, these results do not indicate local adaptation of the parasites to their sympatric hosts. However, the parasite populations differed in average biomass and number of flowers per plant and in their effect on host biomass. These results indicate that the virulence of the parasite varied among populations, suggesting genetic variation. Theoretical models suggest that local adaptation is likely to be detected if the host and the parasite have different evolutionary potentials, different migration rates, and the parasite is highly virulent. In the interaction between R. serotinus and A. capillaris all the theoretical prerequisites for local adaptation may not be fulfilled.     

Diversity,consistency, and seasonality in parasite assemblages of two sympatric marine fish Pagrus pagrus (Linnaeus, 1758) and Pagellus bogaraveo (Brünnich, 1768) (Perciformes: Sparidae) off the coast of Algeria in the western Mediterranean Sea

Various host characteristics (i. e., feeding habits, geographic distribution) and habitat characteristics (i.e., seasonality) influence the structure of parasite assemblages. To compare the parasite assemblages of hosts representatives of two genera of the same fish family, simultaneously occupying a geographic region, and to examine if seasonal variations influence parasite occurrence and abundance, we examined the parasite assemblages of two sympatric marine fish, Pagrus pagrus (n = 308) and Pagellus bogaraveo (n = 315) off the coast of Algeria in the western Mediterranean. Specimens were collected during summer and autumn over three consecutive years (2014–2016). Parasite assemblages were high in species richness and abundance. We compiled an inventory of 40 parasite taxa, including ectoparasitic monogeneans and crustaceans, and endoparasitic trematodes, cestodes, acanthocephalans, and nematodes. Endoparasite taxa primarily consisted of adult gastro-intestinal parasites and long lived larval helminths. Information on the parasite community structure and seasonal variations in parasite populations of these two hosts from the Mediterranean is here provided. Observed patterns of composition, diversity, dominance, and similarity indicate an overall consistency in assemblage structure. Although each host species harbored distinct parasite communities, they shared a high proportion of parasite species suggesting similar use of a common local pool of parasites. However, most shared species did not contribute to structuring the assemblages. Seasonal patterns in parasite abundance were observed for both hosts, with peak prevalence, abundance, and diversity in autumn. Results suggest that, regardless of a common pool of parasites being available to sympatric species, several ecological filters over time, led to distinct, independent variations in the parasite assemblages in each species.     

Fluctuating asymmetry in an insect host: a big role for big parasites?

Parasites are expected to be associated with host developmental instability because developmentally unstable hosts may be more susceptible to, or more frequently exposed to, parasitic infections compared with developmentally stable ones, or because parasites may directly disrupt host development. In this study, we analysed the relationship between developmental stability in the weta Pleioplectron simplex (Orthoptera) and infections by hairworm and mermithid parasites. These parasites have a long development in their host and the size of adult worms exceeds the length of the host by a considerable amount (15–20 cm). For one character (femora) we found that fluctuating asymmetry was significantly higher in parasitized individuals compared with unparasitized ones, in each of two samples collected in different years. Because no relationship was observed between the level of fluctuating asymmetry and the parasite size or number, however, infection by hairworm and mermithid parasites could be more a consequence of developmental instability than a cause. For other characters (tibia, external and internal spines of femora), the level of fluctuating asymmetry between parasitized and unparasitized individuals was not significantly different. Our results are discussed in relation to ecological constraints met by hairworm and mermithid parasites to complete their life cycle.     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

Local adaptation of a holoparasitic plant,Cuscuta europaea: variation among populations

Locally adapted parasites have higher infectivity and/or fitness on sympatric than on allopatric hosts. We tested local adaptation of a holoparasitic plant, Cuscuta europaea, to its host plant, Urtica dioica. We infected hosts from five sites with holoparasites from the same five sites and measured local adaptation in terms of infectivity and parasite performance (biomass) in a reciprocal cross‐infection experiment. The virulence of the parasite did not differ between sympatric and allopatric hosts. Overall, parasites had higher infectivity on sympatric hosts but infectivity and parasite performance varied among populations. Parasites from one of the populations showed local adaptation in terms of performance, whereas parasites from one of the populations had higher infectivity on allopatric hosts compared with sympatric hosts. This among‐population variation may be explained by random variation in parasite adaptation to host populations or by time‐lagged co‐evolutionary oscillations that lead to fluctuations in the level of local adaptation.     

Parachordodes tegonotus n. sp. (Gordioidea: Nematomorpha), a hairworm parasite of ground beetles (Carabidae: Coleoptera), with a summary of gordiid parasites of carabids

A new species of hairworm, Parachordodes tegonotus n. sp. (Gordioidea: Nematomorpha) is described from three species of ground beetles (Carabidae: Coleoptera) from the state of Oregon. This is the first record of Parachordodes Camerano parasitising carabid beetles in North America. Diagnostic characters for the new species include size, colour, the nature and arrangement of the areoles, and the character, shape and extant of ornamentation on the ventral surface of the male tail. Encysted hairworm larvae found in the internal tissues of mayfly and caddisfly larvae at the type-locality were presumed to be those of P. tegonotus, indicating an indirect life-cycle involving paratenic hosts. A worldwide host list shows that some 70 species of ground beetles have been documented as developmental hosts to hairworms belonging to at least five genera, namely Gordius, Parachordodes, Dacochordodes, Gordionus and Paragordionus.