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Mermithid Parasitism of Black Flies (Diptera: Simuliidae)

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Mermithid Parasitism of Black Flies (Diptera: Simuliidae) Mermithid Peresitism of Bleck Flies (Diptere: Simuliidee) ~ Daniel P. Molloy 2 Abstract: 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. 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 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. 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 insect 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 nematode 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
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