Mermithid Nematodes: Physiological Relationships with their Insect Hosts

This paper assesses our state of knowledge of physiological processes involved in the relationships between insects and their mermithid nematode parasites. Three major components of the host-parasite relationship(s) are reviewed: effects of mermithids on host physiology, effects of host physiology on mermithids, and the physiology of the nematodes themselves. Mermithids induce an array of changes in host physiology, and the effects on host metabolism and endocrinology are discussed at some length. Few studies have been done to ascertain the effects of the host on the parasites from a physiological standpoint. Whereas host immunity mechanisms against mermithids have been described at the ultrastructural level, the physiological basis of such responses is not known. Mermithids are atypical nematodes, both structurally and physiologically. In the absence of a functional gut, nutrients are absorbed across the outer cuticle and stored in a trophosome. The transcuticular mode of feeding, storage within the trophosome, and metabolism of storage products are discussed. The usefulness of physiological information toward expediting in vitro culture of these nematodes is discussed, and problems that need to be addressed are defined.     

Mermithid Parasitism of Black Flies (Diptera: Simuliidae)

Mermithid nematodes are common parasites of black flies and play a significant role in the natural regulation of these medically important insects. Infection levels tend to he moderate and perennial, with epizootics rare and highly localized. Mermithid parasitism almost invariably results in the death of the black fly, and thus considerable attention has focused on the potential of these nematodes as biocontrol agents. Early instar black fly larvae appear most susceptible to infection, and integumental penetration hy mermithid preparasites is the only known mode of entry. Postparasitic nematodes typically emerge before host pupation. However, carryover of parasitism into adult simuliids is an important mechanism for local dispersal and recolonization of upstream areas. Following emergence, the mermithids molt to the adult stage. Copulation ensues, the females then laying eggs which eventually give rise to the next generation of infective preparasites. The number of described species is conservatively estimated at 35-40, with most species within the genera Mesomermis, Gastromermis, and Isomermis. The taxonomy of this group of mermithids is a challenging and little explored area. Host-specificity statements, therefore, must be made cautiously because of these systematic problems and others within the Simuliidae. In most instances, temporal and spatial factors limit the host range of these mermithids among simuliid species. Differential susceptibilities anmng larvae concurrently present within the same microhabitat probably reflect varying degrees of host attractiveness and behavioral-physiological resistance. Effects of parasitism on the host may include prevention of metamorphosis, sterility, intersexual development, and behavior modification. Evaluation of the technical feasibility of mermithid control of black flies has been stymied by the limitations of current inoculum-production technology. Continued advances in in vivo and in vitro culture methods are required to accelerate the research process.     

Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda: Talitridae)

Talitrid amphipods spend their days burrowed in sand to avoid predators as well as desiccation and heat stress, although other factors may influence burrowing depth. We investigated the potential role of mermithid nematode parasites in determining burrowing depth in the amphipod Talorchestia quoyana. Mermithids grow as parasites inside amphipods until they reach adulthood, when they must emerge from their host into moist sand to complete their life cycle and reproduce. When allowed to burrow to a depth of their choice in experimental situations, large amphipods burrowed deeper than small ones. In addition, deep-burrowing amphipods were more likely to be infected by mermithid nematodes, and harboured longer worms, on average, than amphipods that burrowed close to the sand surface. This last result is not an artefact of the larger size of deep-burrowing amphipods: the increase in worm length with increasing depth was found after statistical correction for host size. In other words, amphipods that burrowed deeper harboured longer worms than expected based on their body size, whereas those that stayed near the surface of the sand column harboured worms shorter than one would expect based on host size. This implies that the greater burrowing depth of infected amphipods is a consequence, and not a cause, of infection. These results emphasize the importance of parasitism as a determinant of the small-scale spatial distribution of their hosts.     

Heydenius dominicus n. sp. (Nematoda: Mermithidae), a Fossil Parasite from the Dominican Republic

Heydenius dominicus n. sp. is described as a new species of fossil mermithid nematode from Dominican Republic amber. The species is represented by two specimens of parasitic juveniles that left their insect host and became embedded in the resin. The nematodes are associated with an adult male limoniid (Diptera: Limoniidae) and an adult female mosquito (Diptera: Culicidae). The parasites are thought to have emerged from the mosquito host. This is the first report of a fossil mermithid from a Neotropical area.     

Occurrence of five distinct clades of mermithid nematodes (Nematoda: Mermithidae) infecting black fly larvae (Diptera: Simuliidae) in tropical streams in Malaysia

Mermithids are the most common parasites of black flies and are associated with host feminization and sterilization in infected hosts. However, information on the species / lineage of black fly mermithids in Southeast Asia, including Malaysia requires further elucidation. In this study, mermithids were obtained from black fly larvae collected from 138 freshwater stream sites across East and West Malaysia. A molecular approach based on nuclear-encoded 18S ribosomal RNA (18S rRNA) gene was used to identify the species identity / lineage of 77 nematodes successfully extracted and sequenced from the specimens collected. Maximum likelihood and neighbor-joining phylogenetic analyses demonstrated five distinct mermithid lineages. Four species delimitation analyses: automated simultaneous analysis phylogenetics (ASAP), maximum likelihood Poisson tree processes with Bayesian inferences (bPTP_ML), generalized mixed yule coalescent (GMYC) and single rate Poisson tree processes (PTP) were applied to delimit the species boundaries of mermithid lineages in this data set along with genetic distance analysis. Data analysis supports five distinct lineages or operational taxonomic units for mermithids in the present study, with two requiring further investigation as they may represent intraspecific variation or closely related taxa. One mermithid lineage was similar to that previously observed in Simulium nigrogilvum from Thailand. Co-infection with two mermithids of different lineages was observed in one larva of Simulium trangense. This study represents an important first step towards exploring other aspects of host – parasite interactions in black fly mermithids.     

Fungal and oomycete parasites of Chironomidae,Ceratopogonidae and Simuliidae (Culicomorpha,Diptera)

Members of the families Chironomidae (chironomids or non-biting midges), Ceratopogonidae (ceratopogonids or biting midges) and Simuliidae (simulids or blackflies) are ubiquitous dipterans of the infraorder Culicomorpha. They are extremely diversified in ecological strategies. Their larvae play major roles in aquatic food webs as detritivores or predators, whereas their adults can be general predators (Chironomidae), hemolymphagous or hematophagous predators (Ceratopogonidae and Simuliidae) or pollinators. Both larval and adult stages are commonly infected by bacteria, viruses, protists, nematodes, true fungi and oomycetes. These phylogenetically diverse assemblages of microorganisms can simultaneously infect multiple species of chironomids, ceratopogonids and simulids, and each host may become trophically interrelated with other hosts by sharing their parasites. Here, we review the information on fungal and oomycete parasites of these dipteran groups with special reference to the natural regulation of host populations, the impact of parasitism in food webs, and the potential of these parasites as biocontrol agents.     

Nematode endoparasites do not codiversify with their stick insect hosts

Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.     

Heydenius araneus n.sp. (Nematoda: Mermithidae), a parasite of a fossil spider, with an examination of helminths from extant spiders (Arachnida: Araneae)

Abstract. A mermithid, a parasite of a spider (Araneae: Thomisidae) in Baltic amber (40 mya), is described as Heydenius araneus n.sp. (Nematoda: Mermithidae) and represents the first fossil record of a nematode parasite of an arachnid. After a critical examination of reports of naturally occurring helminths of extant spiders, I conclude that although mermithid parasitism is well established in this host group, previous reports of hairworm parasites of spiders are "nomina dubia," putative records, or refer to mermithid nematodes.     

Parasitism of bark scorpion Centruroides exilicauda (Scorpiones: Buthidae) by entomopathogenic nematodes (Rhabditida: Steinernematidae; Heterorhabditidae)

In laboratory bioassays, Steinernema glaseri Steiner, Steinernema riobrave Cabanillas, Poinar & Raulston, Heterorhabditis bacteriophora Poinar, and Heterorhabditis marelatus Liu & Berry were capable of infecting and killing the bark scorpion, Centruroides exilicauda (Wood). Steinernema feltiae (Filipjev) and Steinernema carpocapsae (Weiser) failed to infect C. exilicauda at 22 degrees C. S. glaseri, H. marelatus, and H. bacteriophora caused significant mortality at 22 degrees C, indicating the potential role of these parasites as a biocontrol option. Efficacy of S. glaseri and H. bacteriophora was reduced in an assay conducted at 25 degrees C. Only S. glaseri was able to reproduce in the target host. Dissection of scorpions at the end of the experimental periods revealed inactive juvenile S. riobrave, H. marelatus, and H. bacteriophora nematodes. Both mermithid and oxyurid nematodes have been documented as nematode parasites of scorpions, but rhabditids have not been reported until now. Field studies are warranted to assess the usefulness of entomopathogenic nematodes as biocontrol agents of bark scorpions.     

Effects of the mermithid nematode Ovomermis sinensis on the hemocytes of its host Helicoverpa armigera

Little is known about the mechanism by which mermithid nematodes avoid encapsulation responses of insect hosts. In this study, we investigated the influence of the mermithid nematode Ovomermis sinensis on host Helicoverpa armigera hemocyte number, encapsulation activity, spreading behavior and cytoskeleton. Parasitism by O. sinensis caused a significant increase in the total hemocyte counts (THC) and plasmatocyte numbers of H. armigera. However, in vivo encapsulation assays revealed that hemocyte encapsulation abilities of H. armigera were suppressed by O. sinensis. Moreover, parasitism by O. sinensis changed the spreading behavior and cytoskeletons of the host hemocytes. The results suggested that O. sinensis could actively suppress the hemocyte immune response of its host, possibly by destroying the host hemocyte cytoskeleton. This is the first report of a possible mechanism by which mermithid nematodes suppress encapsulation responses of insect hosts.     

Parasitoid-induced behavioral alterations of Aedes aegypti mosquito larvae infected with mermithid nematodes (Nematoda: Mermithidae).

A wide range of parasites are known to cause behavioral changes in their hosts and parasitized insects are especially amenable to the study of such changes. The majority of studies addressing parasite-induced behavioral alterations have focused on parasites with complex life cycles and the adaptive nature of such changes. Behavioral changes caused by parasitoids, single-host parasites that kill their host upon emergence, have been studied less and the adaptive nature of these changes is likely to be different than those in complex life cycles. I investigated behavioral alterations in Aedes aegypti mosquito larvae infected with parasitoid nematodes (family Mermithidae). I conducted several experiments in which I tested the following hypotheses: 1) Mermithid nematodes induce behavioral changes in mosquito larvae and the changes are density dependent. 2) Different species of mermithid nematodes induce similar changes in mosquito larvae behavior. 3) Behavioral alterations vary with mermithid developmental stage. 4) Mosquito larvae infected with mermithid nematodes behave similarly to uninfected food-deprived mosquito larvae. I found that 4th instar Ae. aegypti infected with Romanomermis culicivorax or Strelkovimermis spiculatus exhibited resting behaviors significantly more often than uninfected controls but that intensity of infection did not affect activity levels. In earlier instars, infected mosquito larvae were more active than uninfected control larvae in some behaviors associated with feeding. There was no significant difference between infected and uninfected food-deprived mosquitoes in nine of the ten behaviors observed. The decrease in activity of late instar Ae. aegypti larvae infected with mermithids may be a parasitoid adaptation that reduces the risk of predation and thus increases host and parasitoid survival. The increase in feeding activity in earlier instars as well as the similarity between uninfected food-deprived and infected Ae. aegypti behavior may indicate that these behaviors are adaptive for the parasitoid, increasing nutritional acquisition for successful parasitoid development.     

Insect immune responses to nematode parasites

Host innate immunity plays a central role in detecting and eliminating microbial pathogenic infections in both vertebrate and invertebrate animals. Entomopathogenic or insect pathogenic nematodes are of particular importance for the control of insect pests and vectors of pathogens, while insect-borne nematodes cause serious diseases in humans. Recent work has begun to use the power of insect models to investigate host-nematode interactions and uncover host antiparasitic immune reactions. This review describes recent findings on innate immune evasion strategies of parasitic nematodes and host cellular and humoral responses to the infection. Such information can be used to model diseases caused by human parasitic nematodes and provide clues indicating directions for research into the interplay between vector insects and their invading tropical parasites.     

Bird hosts, blood parasites and their vectors--associations uncovered by molecular analyses of blackfly blood meals

The level of host specificity of blood-sucking invertebrates may have both ecological and evolutionary implications for the parasites they are transmitting. We used blood meals from wild-caught blackflies for molecular identification of parasites and hosts to examine patterns of host specificity and how these may affect the transmission of avian blood parasites of the genus Leucocytozoon . We found that five different species of ornithophilic blackflies preferred different species of birds when taking their blood meals. Of the blackflies that contained avian blood meals, 62% were infected with Leucocytozoon parasites, consisting of 15 different parasite lineages. For the blackfly species, there was a significant association between the host width (measured as the genetic differentiation between the used hosts) and the genetic similarity of the parasites in their blood meals. The absence of similar parasite in blood meals from blackflies with different host preferences is interpreted as a result of the vector–host associations. The observed associations between blackfly species and host species are therefore likely to hinder parasites to be transmitted between different host-groups, resulting in ecologically driven associations between certain parasite lineages and hosts species.     

中华卵索线虫的体外培养

在研究中华卵索线虫的体外培养方法的同时,对其在不同培养基中的生长发育情况进行了观察。结果表明：以培养基TC－199加20％热灭活胎牛血清的培养效果较为理想,大多数线虫可存活3个月,最大虫体长55．1mm,宽204．13um,其发育程度大致与该种索线虫在宿主粘虫体内寄生8－9天的情况相近,培养期间观察到2次蜕皮;第一次蜕皮在卵内,第二次在培养6－8天之后,口针消失,虫体内滋养物体发育明显,尾部附器已经形成,没有观察到生殖原基的发育。     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

Mermithid nematode infections and drift in the mayfly Deleatidium spp. (Ephemeroptera).

Alterations in host phenotype induced by parasitic infection are often interpreted as either host or parasite adaptations, depending on which of the two appears to benefit. Mermithid nematodes typically castrate their insect hosts and, therefore, any change in host behavior has no further fitness consequences for the host; the adaptive value of the modified behavior must be assessed with respect to parasite fitness only. In a New Zealand stream, mermithid-infected nymphs of mayflies in the genus Deleatidium were disproportionately represented in drift samples compared with benthic samples, suggesting that infection by mermithids results in an increased tendency to drift. Drifting mayflies face a higher predation risk from trout, and the mermithid nematodes they harbor die if ingested by a fish. The change in mayfly behavior induced by mermithids thus appears to have negative fitness effects for the parasite, and one possible explanation for this phenomenon is that it is a nonadaptive, pathological side effect of infection.     

Trematodes and nematodes parasitizing the benthic insect community of an Andean Patagonian stream,with emphasis on plagiorchiid metacercariae

In freshwater systems, parasitological studies have mainly been carried out on vertebrates and molluscs, but little is known about parasites of aquatic insects. We describe the trematodes and nematodes parasitizing the benthic insects of an Andean Patagonian stream and the presence of parasites in the terrestrial adult stages. Members of 3 of 20 insect taxa were found to be parasitized by larval nematodes, and members of six taxa harbored metacercariae of digeneans. In benthic samples, chironomids, simuliids (Order Diptera), and baetids (Order Ephemeroptera) harbored mermithid larvae (Nematoda). The stonefly Antarctoperla michaelseni (Order Plecoptera), the caddisfly Smicridea annulicornis (Order Trichoptera), a watersnipe fly (Order Diptera: Athericidae), and three species of leptophlebiid mayflies (Order Ephemeroptera) were parasitized by encysted plagiorchiid metacercariae (Order Plagiorchiida). Most metacercariae were found in the three species of mayflies with prevalences ranging 15–63% and mean intensities ranging 1.2–4.9. Prevalence declined from summer to early winter, probably because of the emergence of infected nymphs and the recruitment of uninfected new cohorts. The imagos had live metacercariae with higher prevalences and intensities of infection than nymphs. We suggest that these plagiorchiids have an allogenic life cycle, involving a terrestrial definitive host.     

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.     

Mating and Sexual Communication by Steinernema carpocapsae (Nemata: Steinernematidae)

Entomopathogenic nematodes are lethal insect parasites that reproduce exclusively inside their hosts in nature. Infection decisions made by the free-living infective-stage juveniles have an impact on reproductive success, but it is likely that mating decisions are made by adults while inside their host. We investigated sexual communication between male and female adult stages of Steinernema carpocapsae (Rhabditida: Steinernematidae) to assess whether mating is chemically mediated during the adult stage or results from incidental encounters between adults inside the insect host. To assess chemical communication, we measured the behavioral response of adult male S. carpocapsae to several different potential sources of chemical information. Male S. carpocapsae responded to virgin females only and were not influenced by mated conspecific females, conspecific males, or heterospecific females. These results show that species-specific communication takes place between adult entomopathogenic nematodes within the host cadaver just prior to mating.     

Role of mermithid nematodes in biological control of mosquitoes

Mermithid nematodes have been reported from at least 63 species of mosquitoes from all over the world, but until recently they have received little attention. Such nematodes are prime candidates as biological control agents because they have adapted to the life cycle of the host; are host specific; produce high levels of parasitism; kill the hosts; are easily handled; have a high reproductive potential; are free swimming and can be disseminated easily in the infective stage; and can be used in an inundative or inoculative manner to control mosquitoes. Nevertheless, with the exception of one mermithid species, little is known about factors that influence parasitism in mosquitoes. Also, only one species of mermithid has been successfully mass cultured to date. The exception is the mermithid Reesimermis nielseni. With this mermithid, high levels of parasitism can be obtained in natural populations of mosquitoes at reasonable dosages; preparasitic nematodes can be applied easily by using many of the standard techniques used to apply insecticides; and R. nielseni can establish itself in many of the sites in which it is released. The same potentials exist for mermithids of other aquatic insects.