Introduction

Hairworms (also called horse hairworms) (Gordioidea: Nematomorpha) and mermithid nematodes (Mermithidae: Nematoda) are worldwide, enigmatic obligate parasites that have been little studied, mainly because of their general rareness, difficulty in rearing under laboratory conditions, and lack of economic importance. These 2 groups are often confused with one another since the mature forms are elongate, narrow worms, with invertebrates, especially insects, as developmental hosts. In fact, as shown here, some host species support the development of both hairworms and mermithids, although rarely in the same individual. Immature hairworms are white and usually die if removed from their hosts. They turn black or various shades of brown when mature and then leave the host. Mermithid nematodes are normally white or cream colored in both the immature and mature stages; however females of the genus Mermis can appear brown when gravid with eggs.

Little is known about the host diversity of these parasites. Hosts of most of the 18 described species of North American hairworms are unknown (Poinar & Chandler 2004). No mermithids are previously known from stenopelmatids (Poinar 1975). The present study identifies orthopteran hosts of hairworms and mermithids collected from sites throughout central and western United States and much of Mexico. Host groups involved members of the Orthoptera: Stenopelmatidae, Gryllidae and Tettigoniidae.

Methods

Orthopterans for this study were field collected and laboratory maintained for studies (see, e.g., Weissman 2001a,b) on communication and biology used in taxonomic investigations. Over the past 25 y, more than 2500 Jerusalem crickets (Stenopelmatus spp.), almost 5000 field crickets (Gryllus spp.) and several hundred decticine katydids have been so treated, providing an unparalleled variety of potential host data. Because worm-infected individuals typically do not molt or sing, yet appear healthy and active, hosts are unintentionally retained alive until their parasites mature and emerge.

Methods for preserving and preparing specimens for optical microscopic examination are reported elsewhere (Poinar 2001, Smith 2001). Generic and specific identification are based on keys presented in Poinar & Chandler 2004, with reference to earlier descriptions by Montgomery (1898a, 1898b, 1907), Ward & Whipple (1918), and Leidy (1851, 1856). All specimens are preserved in alcohol and deposited at the California Academy of Sciences, San Francisco, CA. Localities where host orthopterans were collected are tabulated in Tables 1, 2, and 3, with specific collection data presented in the Appendix.

Results

Thirty six identifiable hosts were parasitized, most multiple. Of these, 19 were hairworms associated with some 11, mostly undescribed, species of Stenopelmatus (Table 1), 6 were hairworms from 4 species of Gryllus and 2 decticine katydid genera (Table 2), and 11 were mermithid nematodes associated with 5 species of Stenopelmatus, Capnobotes fuliginosus (Thomas) and a Gryllus sp. (Table 3).

Discussion

Hairworms normally emerge from their hosts as adults and possess diagnostic characters for identification to species. Mermithid nematodes, in contrast, emerge as postparasitic juveniles and must undergo a final molt in the environment to reach the adult stage. This final molt may take weeks and since most specimens are fixed immediately upon exit from their hosts, the adult is not available. Since all of the basic diagnostic characters in mermithids occur in the adults, postparasitic juveniles cannot be confidently identified beyond family level. Many of our specimens probably represent new species.

Most if not all hairworms (as well as some mermithid species) utilize both a paratenic host (a host where encystment but no development occurs) as well as a developmental host, in their life cycle. In the present study, all of the hosts are developmental hosts, where the parasite grows to maturity in the body cavity.

The present study contributes significantly to our knowledge of orthopteran hosts of North American hairworms and mermithid nematodes. Up to the present, there have been no published records of mermithids infesting members of the Stenopelmatidae (Poinar 1975). Here, we report mermithids from 5 species of Stenopelmatus. No mermithids had been reported previously from members of the decticine genus Capnobotes. However, the mermithids Mermis subnigrescens Cobb and Agamermis decaudata Cobb, Steiner & Christie have been reported from other members of the Tettigoniidae (Poinar 1975). Only one location [Charmlee State Park, Los Angeles Co., CA, (S89–92 in Table 1 and S01-12 in Table 3)] in the present study contained a host species infected with both hairworms and mermithids: but not in the same individual.

Thus far, hairworm parasites of stenopelmatids and related anostostomatids are known from North America, New Zealand and Australia (Poinar 1991, Wharton et al. 2001). Our knowledge is not complete enough to determine if any hairworm species is restricted to members of these families. However, on the basis of these results and what has been reported previously, it appears that certain species of North American hairworms definitely prefer Orthoptera as hosts.

One of these is Gordius robustus Leidy. In 1856, Leidy reported infections in the tettigoniid Xiphidium nemorale Scudder (now Conocephalus nemoralis). Later, May (1919) found the tettigoniids Orchelimum nigripes Scudder, O. vulgare Harris and Scudderia furcata Brunner to be infected by G. robustus. Thorne (1940) studied this hairworm in the decticine katydid Anabrus simplex Haldeman, and Cappucci (1977) reported G. robustus from the stenopelmatid Stenopelmatus longispina Brunner. The present report (see Table 2) is the first case of this hairworm species infecting members of the decticine katydid genus Steiroxys and a Gryllus sp.

A second North American orthopteran hairworm is Paragordius varius Leidy. Ward & Whipple (1918) mentioned the gryllids Acheta abbreviata Serville (now Gryllus pennsylvanicus Burmeister) and Nemobius fasciatus De Geer as developmental hosts for P. varius. We confirm here that crickets may be a preferred host of P. varius as we also found them in 3 species of Gryllus (Table 2).

A third hairworm species that appears to prefer Orthoptera is Neochordodes occidentalis (Montgomery). The only previous report of a host of this species is by Ward & Whipple (1918) who state that an acridid grasshopper was parasitized. The present study reports the first case of this hairworm parasitizing members of the genus Stenopelmatus (5 species) (Table 1) and the decticine katydid genus Pediodectes (Table 2).

Our records of the hairworm Parachordodes platycephalus Montgomery from 2 species of Stenopelmatus (Table 1), are interesting since members of that genus normally develop in predatory beetles, especially members of the family Carabidae (Poinar et al. 2004).

A previous study dealing with hairworm parasites of Anostostomatidae showed that an obligate paratenic host is involved in the life cycle (Poinar 1991). This paratenic host is usually an aquatic insect, especially a mayfly (Ephemeroptera) or caddisfly (Trichoptera). The larvae of these insects ingest hairworm eggs or first stage larvae from the stream bed. The ingested eggs hatch, and the larvae proceed to bore through the insect midgut and encyst in various tissues in the hemocoel. They do not grow or develop in this location, but simply enter a dormant stage that can be carried through the pupal and into the adult stages of the insect. Hosts become infected when they eat one of these insects containing hairworm cysts. The cysts are quite durable and it is possible for infection to occur even if the paratenic host is dying or already dead. In the orthopteran gut, the hairworm larva leaves the cyst, penetrates the gut wall and enters the body cavity where it grows. When mature, hairworms somehow alter their host's behavior, causing them to seek a water source (most hosts do not live far from some supply of water, whether a permanent or temporary stream, pond, puddle or even a water trough). Upon emerging from the host, the hairworms enter the water, mate, and the female oviposits strings or masses of eggs in the aquatic habitat. Since they kill their hosts at the time of, or soon after, emergence, hairworms can be a significant mortality factor and were the major parasite of New Zealand wetas (Poinar 1991). In the present study, we found that hairworm-parasitized stenopelmatids usually did not molt. A notable exception was a nymph from S92–146 that molted several times over the 16-month period she was in captivity, only to ultimately die upon emergence of the hairworm. There may be other abnormalities in parasitized hosts, especially in relation to sexual behavior. Our paucity of worm records from Mexico, despite much collecting, probably reflects the few stenopelmatids recovered.