Mermithid Peresitism of Bleck (Diptere: Simuliidee) ~ Daniel P. Molloy 2 Abstract: Mermithid are common parasites of black flies and play a significant role in the natural regulation of these medically important . Infection levels tend to he moderate and perennial, with epizootics rare and highly localized. Mermithid almost invariably results in the death of the black , and thus considerable attention has focused on the potential of these nematodes as biocontrol agents. Early instar 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. Folhtwing 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 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. Key words: Mermithidae, bionotnics, systematics, host specificity, host-parasite relationship, biological control, Mesomermis, Gastromer- mis, Isomermis.

"On coming downstairs on Aug. 16th, I natural regulation (4,38,59). Infection levels saw a small Dipteron (Simulium ornatum) tend to be moderate (3-15%) and peren- on the windowpane, and this seemed nial, with epizootics rare and highly lo- to enjoy its usual activity until a drop of calized (12,26,28,53,56). Nevertheless, mer- benzine proved fatal. I then mounted it on mithids have occasionally been reported to a slip of cardboard, when what seemed a cause drastic population reductions (38,60). huge cabbage-green snake-like creature sud- Although recorded from black fly popu- denly crept forth from its abdomen." (55). lations throughout the world, mermithid The above is one of the earliest and most parasites appear to have sporadic local dis- colorful descriptions of mermithid para- tributions--a condition due in part to their sitism of black flies. The Mermithidae para- limited dispersal capabilities. For example, sitize a wide variety of invertebrates. In the surveys conducted in Newfoundland (15) class Insecta at least 17 orders, including and Wisconsin (3) found that only 30 and more than 100 families, have been recorded 23% of the streams, respectively, contained as hosts (39). Welch (59) cited at least 153 mermithid-parasitized black flies. reports of mermithid parasitism of black Because infection almost invariably re- flies; at least another 50 have appeared since sults in host death, considerable attention his 1964 review. has been focused on these parasites as po- Mermithids are common parasites of tential black fly biocontrol agents (23,48). simuliids and play a significant role in their In Central America and Africa, black flies are intermediate hosts and vectors of Onchocerca volvulus, a filarioid Received for publication 12 December 1980, which causes human onchocerciasis--a vision XSymposium paper presented at the annual meeting of the Society of Nematologists, New Orleans, Louisiana, Au- impairing disease estimated to afflict more gust 1980. Published by permission of the Director, New than 20 million people. Since present con- York State Museum, State Education Department, Journal Series No. 321. trol efforts rely solely on chemical larvicides, 2Senior Scientist. Biological Survey, New York State the development of biological agents for Museum, State Education Department, Albany, NY 12230. Continuing financial support from the National Institutes incorporation into an integrated control of Health (AI-15605) is gratefully acknowledged. The program is needed. Mermithids are leading author thanks J. R. Finney and R. R. Gaugler for critical review of the manuscript. candidates for such a role. 250 Mermithids and Black Flies: Molloy 251

BIONOMICS However, per os entry (ingestion of either an egg or juvenile) should not be ruled out, The infective stage is the newly hatched, since it has been reported for mermithids preparasitic nematode, and all evidence in- parasitic in other insects (11,41). Others dicates that early instar black flies are most (38,54,60) have suggested that some black susceptible to invasion (9,17,31,60). Mer- fly mermithids enter their hosts by penetra- mithid life cycles are synchronized with tion of the gut wall, but conclusive evidence those of their hosts, preparasite hatch oc- curring during periods when susceptible of this mode of entry has not been offered. The juvenile derives its nourishment larval instars are present (12,16,60). from the host's hemolymph. Transcuticular The mode of penetration is unknown nutrient uptake through the nematode's for almost all mermithid species parasitic in body wall has been demonstrated for mer- black flies. The two exceptions are Iso- mithid parasites of grasshoppers (49,50), and mermis lairdi (33) and Mesomermis (= a recent uhrastructural study of the black Neomesornermis) flurnenalis sensu lato (2, fly parasite Gastromermis boophthorae has 31). Preparasites of I. lairdi are captured by provided evidence that transcuticular up- the cephalic fans of feeding black flies and penetrate the larval cuticle in the cephalic take also occurs in this mermithid (7). region. Preparasites of M. flumenalis s. l. When the nematode has completed its crawl on the streambed in search of hosts development within the abdomen o£ the (31). In a successful attack, a M. flumenalis black fly, it emerges to resume a free-living preparasite typically attaches itself to the existence. Postparasitic emergence typically thoracic region of the black fly larva, out of occurs during the larval stage of the black reach of the larva's mandibles, and coils fly, usually at the time uninfected flies in tightly around the larva. The black fly the population are pupating. The peak moves in quick jerking motions, opening emergence of male mermithids often pre- and closing its mandibles in a vain attempt ceeds that of the females (5). Emergence to grasp the nematode. The integument is generally occurs through the intersegmental soon pierced by the stylet, and within a few areas of the larval abdomen, but penetration minutes the preparasite uncoils and passes of the gut wall and exit through natural into the larva's hemocoel. During this pe- openings have also been observed. The riod and for several minutes thereafter, the length of a postparasite is 1-4 times that of its host, the length varying inversely with black fly appears to be paralyzed, with the number of mermithids per host. its body often in a contorted position. Al- though normal movement and feeding Although development of some mer- gradually resume within an hour after pene- mithids appears to occur solely within larval tration, this temporary paralysis eliminates simuliids (30), pupation and emergence of further defensive tactics by a larva and infected black flies has frequently been re- ensures successful penetration by the pre- ported (12,29,37,47,51). Parasitism of adult parasite. In laboratory trials (Molloy, un- simuliids is advantageous to mermithid published data) such defenseless, paralyzed populations, since it provides a mechanism larvae were observed to be easily attacked for dispersal of these nematodes to neigh- and penetrated by other preparasites in the boring streams and allows recolonization of vicinity. Wiilker (63) reported a similar upstream areas (black flies migrate upstream "paralysis" in chironomid larvae attacked to oviposit) (59). by Gastromermis rosea and suggested that After host emergence, the postparasites the paralysis was induced by injection of a molt to adults, mate, and lay eggs to pro- substance into the host's hemocoel by the duce a new generation of preparasites; these preparasite. Wiilker's hypothesis is plausi- free-living stages in the life cycle occur ble, and it is here suggested that the pre- within the streambed. Immediately after parasite's penetration glands might be the emergence, many postparasites lose their source of such a muscle-paralyzing fluid. hold on substrates and are carried down- It is likely that preparasite penetration stream. Infection loci, however, are likely of the integument is a common mode of maintained in upstream areas by those post- entry for mermithids parasitic in black flies. parasites which are capable of crawling di- 252 Journal o I Nematology, Volume 13, No. 3, July 1981 rectly down into the streambed. ness in moving water and that it did not Data on the periodicity of molt, mating, develop normally in those few black fly oviposition, and egg hatch are available for larvae that it did successfully invade (21), Gastromermis viridis, I. wisconsinensis (38), interest in its biocontrol potential quickly M. flumenalis s. l. (14), and I. lairdi (33). faded. Although multivoltine merimithids are It is difficult to accurately assess the known from black flies in England (Curran, specificity of black fly mermithids because personal communication) all five species de- of systematic problems within the parasite scribed from North American black flies and the host groups. Host-list tables give (30,40,58) are thought to be univoltine. the impression that black fly mermithids Tropical species (e.g., 1. lairdi) appear mul- have a broad host range and that individual tivoltine. black fly species serve as hosts for a wide range of mermithids. Both impressions are SYSTEMATICS misleading. For example, although M. Mesomermis, Gastromermis, and Iso- [lumenalis is listed as a parasite of 13 black mermis spp. are the most common mer- fly species (28,53), it is likely that at least mithids parasitic in black flies. Other genera three mermithid species (M. [tumenalis that have been observed to infect simuliids sensu strictu, M. camdenensis, and an un- include Limnomermis, Hydromermis, and described Mesomermis sp. infecting Pro- Spiculimermis. There are approximately simulium spp.) were involved in these rec- 35-40 widely recognized species including ords. The identification of the host species the recently described M. camdenensis (30), in many records likewise may be inaccurate, M. paradisus (41), M. guatemalae (44), M. since it has been demonstrated that a large travisi (57), M. iaponicus (42), 1. benevolus number of species complexes exist in the (43), I. vulvachila (44), and G. cloacachilus Simuliidae. Thus, considering these sys- (44). tematic problems, host specificity statements The lack of clear-cut, distinguishing have to be made cautiously. We do know, morphological features at the species level however, from field observations and lab- makes the taxonomy of the Mermithidae oratory tests that black fly species are dif- challenging. The systematic position of M. ferentially susceptible to mermithid infec- [tumenalis is a prime example. Although tion. For example, a complete lack of infec- this species was originally described from a tion in S. tuberosum was noted in streams Simulium sp. (58), a mermithid of similar where high levels of mermithid infection naorphology parasitizing Prosimulium spp. were present in S. vittatum (38). Colbo and has also been widely referred to as "M. Porter (12) reported 19% and 0% mer- flumenalis.'" Only recently have sufficient mithid infection in P. mixture and biological-ecological data (6,12) been avail- Stegopterna mutata larvae, respectively, able to indicate a lack of conspecificity be- even though early instars of both species tween these Simulium- and Prosimulium- were present in the same microhabitats emerging mermithids. in Newfoundland. Similarly, significantly higher rates of infection were achieved in S. verecundum than in S. vittatum larvae in HOST SPECIFICITY a New York field trial with M. [tumenalis Black fly mermithids are not known as s. l. (32). This trial also demonstrated that parasites of any other stream fauna. More- cross-generic infection by a mermithid spe- over, mermithids which are naturally para- cies was possible, since the mermithids used sitic in other insects have not been found in the test had been field-collected from in field-collected black flies. The mosquito Prosimulium larvae. mermithid, Romanomermis culicivorax, In most instances, temporal and spatial which had been demonstrated in the lab- factors (e.g., asynchronous life cycles, dif- oratory to infect black flies (20), was pro- fering geographical and habitat prefer- posed as a black fly biocontrol agent (27). ences) limit the host range of mermithid However, after it was demonstrated that parasites. However, when larvae of two or this mermithid had markedly little invasive- more black fly species are present together, Mermithids and Black Flies: Molloy 253 differential host attraction or behavioral male genitalia; parasitism of genetically fe- and physiological resistance may account male individuals, while it induces altera- for differential rates of parasitism (36). Be- tions in their internal and external adult havioral resistance occurs when black fly morphology, does not result in major inter- larvae put up an active defense to attacking sexual traits (45,61,62). preparasites. In moving water, S. vittatum The above pattern of intersexual devel- larvae are capable of grasping and mortally opment may also occur among black flies wounding host-searching M. flumenalis s. l. which, like mosquitoes and chironomids, preparasites (Molloy, unpublished obser- are nematocerous Diptera. Mokry and Fin- witions). Resistance based on the physio- ney (29) and Colbo and Porter (12) re- logical response of the host does not appear ported finding only "female" adults in- to play a significant role in the differential fected with mermithids. They observed susceptibility of mermithid infection in that their results were atypical, since other black tiles. Nothing is presently known studies (24,37,38) had reported mermithid about host attraction and the kinds of infection in both males and females. Colbo stimuli that may be involved. and Porter (12) suggested that parasitized male flies may have been killed prior to HOST-PARASITE RELATIONSHIPS pupation. However, one might suggest that Mermithid parasitism causes serious as with mosquitoes and chironomids, all morphological and physiological disturb- intersexual black flies are genetically male ances in the larval fly, as shown by the host's and that in certain simuliid-mermithid as- abdominal distortion, discolored integu- sociations (e.g., as present in the New- ment, and depleted fat body (38,54,59). Ar- foundland studies) mermithid parasitism of rested development of pupal and adult his- male larvae results in their intersexual de- toblasts is common in parasitized larvae and velopment. Thus, in the Newfoundland can prevent metamorphosis. Condon and studies, all parasitized male flies would have Gordon (13) suggested that inhibition of appeared as female phenotypes. Morpholog- pupation associated with parasitism is prob- ical and cytological determination of the ably a consequence of severe nutrient de- sex of parasitized and nonparasitized flies, pletion rather than an active manipulation following Rempel et al. (45), would test of the black fly's hormonal system by the this hypothesis. parasite. However, parasitized flies that do Mermithid parasitism also modifies adult pupate and emerge are usually sterile due behavior. Parasitized males have been ob- to incomplete development of their gonads served to attach to oviposition substrates (3,37,38,51). Moreover, Hocking and Picker- (38) and simulate oviposition (12). Grunin ing (25) reported degeneration of the nerv- (24) observed mermithids emerging from ous and digestive systems in parasitized male Prosimulium which were flying over adult S. venustum. Ovarian development streams. The mock ovipositional behavior was inhibited in 99% of infected adult of these adults increases the likelihood that Simulium damnosum, and these flies lived an emerging mermithid will be deposited in only half as long as nonparasitized females an upstream area. It would be interesting to (34). examine if intersexual development of Intersexual adult black flies can result genetically male flies further reinforces this from mermithid parasitism, and Rubtsov oviposition behavior. (46) suggests that a disturbance to the fly's The sex of mermithids developing within endocrine system is responsible. Intersexual an insect usually depends upon the inten- development in chironomids and mos- sity of infection, with the proportion of quitoes only occurs in genetically male in- males to females increasing with the num- dividuals (10), and nematode parasitism of ber of nematodes per host; mermithids para- these flies is a known cause of this condition sitic in black flies are not an exception. A (22). Genetically male Chironomus an- single mermithid in a black fly is almost in- thracimus and C. rempelIi larvae parasitized variably a female, while superparasitized by mermithids uniformly develop into hosts usually produce males (15,18). Sexual phenotypically female adults possessing determination in I. lairdi may be atypical, 254 Journal of Nematology, Volume 13, No. 3, July 1981 however, since male adult S. damnosum s. l. Recent studies are somewhat encouraging. typically contain only male mermithids (35). Significant advances have been made toward tile establishment of continuous laboratory BIOCONTROL POTENTIAL colonies of black flies (8,52), thus making Mermithids parasitic in black flies have in vivo production of black fly mermithids several characteristics that make them ideal potentially feasible. Considerable progress biocontrol agents. Their host range appears has also occurred in the area of in vitro limited to simuliids; they kill or sterilize culturing of mermithids (19). In the short their hosts; and, being natural parasites of term it is more likely that an in vivo-pro- black flies, they have good potential for ducetl mermithid colony will be available; permanent establishment, thereby giving the establishment of in vitro production is long-term control following a single appli- a more challenging research area, but one cation. which may ultimately prove to be a more economical method of inoculum produc- Encouraged by steady progress in the development of the mermithid, Romano- tion. Although emphasis here is placed on the mermis culicivorax, as a mosquito control pressing need for comprehensive laboratory agent (36), hope ran high in the early 1970s and field trials, other aspects of research on that the biocontrol potential of black fly mermithid parasitism of black flies should mermithids could be systematically ex- not be neglected. Further taxonomic studies ploited (1). Field-oriented research focused on both host and parasite groups are neces- on host-parasite interrelationships and pro- sary if species are to be accurately identified. vided baseline data on the biology and ecol- Studies such as host-parasite life cycle syn- ogy of host and parasite. However, the tech- chrony, host specificity, and the environ- nical feasibility of using mermithids in a mental parameters affecting the free-living black fly control program has yet to be ade- stages of these mermitbids are needed to quately addressed. The control potential of better define the factors influencing the these parasites is most readily evaluated prevalence and intensity of parasitism. through comprehensive laboratory and field trials, in which the effects of mermithid treatments on black flies are carefully quan- LITERATURE CITED tified. Few such tests have been conducted 1. Ammymous. 1972. Preventing onchocerciasis to date (31,32,33) due to difficulty of ob- through blackfly control. International Development taining inoculum, Since laboratory colonies Research Centre, Ottawa, Canada, IDRC-006e. of black tly mermithids are not yet avail- 2. Anonymous. 1973. Third biannual report. Re- search Unit on Vector Pathology. Memorial Uni- able, all inoculum must be produced from versity of Newfoundland. nematodes which have emerged from field- 3. Anderson, J. R., and G. R. DeFoliart. 1962. collected flies. This is an expensive pro- Nematode parasitism of black fly (Diptera: Sirnuli- cedure, and one which is highly dependent idae) larvae in Wisconsin. Ann. Entomol. Soc. Am. on the seasonal and local availability of 55:542-546. 4. Anderson, J. R., and R. J. Dicke. 1960. Ecol- infected black fly populations. ogy of the immature stages of some Wisconsin black Only one field trial with mermithid flies (Simuliidae: Diptera). Ann. Entomol. Soc. Am. preparasites has thus far been conducted 53:386-403. (32). High rates of mortality (> 70%) were 5. Bailey, C. H., and R. Gordon. 1977. Observa- tions on the occurrence and collection of mermithid achieved in early instar S. verecundum, but nematodes from blackflies (Diptera: Simuliidae). only after application of large quantities of Can. J. Zool. 55:148-154. inoculum. It should be noted, however, 6. Bailey, C. H., R. Gordon, and C, Mills. 1977. that the mermithids used as the inoculum Laboratory culture of the free-living stages of Neo- mesomermis flumenalis, a mermithid nematode were naturally parasitic in Prosimulium parasite of Newfoundland blackflies (Diptera: larvae, and greater infectivity would prob- Simuliidae). Can. J. Zool. 55:391-397. ably have been obtained against larvae of 7. Batson, B. S. 1979. Body wall of juvenile and this genus. adult Gastromermis boophthorae (Nematoda: More laboratory and field trials are ob- Mermithidae): ultrastructure and nutritional role. Int. J. Parasitol. 9:495-503. viously required, but the problem of in- 8. Brenner, R. J., and E. W. Cupp, 1980. 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