JOURNAL OF NEMATOLOGY VOLUME 28 MARCH 1996 NUMBER 1

Journal of Nematology 28(1): 1-7. 1996. © The Society of Nematologists 1996. Ectoparasitic Acugutturid Nematodes of Adult 1 A. M. SIMMONS 2 AND C. E. ROGERS 3 Abstract: Noctuidonema gu~aneme is an interesting ectoparasite of adult Lepidoptera that feeds on hosts from at least five families with its long stylet. Noctuidonema guyanense spends its entire life on the adult and is sustained as it is passed from moth to moth during host mating. Overlapping host generations are essential for parasite survival. This nematode occurs throughout tropical and sub- tropical America and is transported by at least one of its hosts, Spodopterafrugiperda, during migra- tion to northern sites in the United States each spring. Noctuidonema guyanense debilitates its hosts. Research conducted to help determine the biological control importance of this nematode is re- viewed. Two additional species, N. dapt~a and N. dibolia, are now known for Noctuidonema. Keywords: Aphelenchoididae, biological control, distribution, ecology, ectoparasite, entomopatho- genic nematode, fall armyworm, host range, Noctuidonema guyanense, Spodopterafrugiperda.

There are only a few known ectopara- with the conus much longer than the shaft sitic nematodes of adult . Ektaphelen- (3). chus spp. are facultative ectoparasitic aph- In 1988, researchers in French Guiana elenchoids (12) in the subfamily Entaph- described the first known case of an ecto- elenchinae (11). They are found on larvae, parasitic nematode from adult Lepi- pupae, and adults of wood-boring scolytid doptera (14). They described this nema- beetles. Although facultative parasitic tode as Noctuidonema guyanense Remillet & nematodes may feed on insects, they can Silvain, an aphelenchoid, and classified it also complete their life cycle separate from in the subfamily Acugutturinae (14). Hunt the (13). Hunt (3) described an ob- (4) revised the Aphelenchida by placing ligate ectoparasitic nematode, Acugutturus Acugutturus and Noctuidonema in separate parasiticus Hunt, from the American cock- subfamilies in the Acugutturidae. roach, Periplaneta americana (L.), in St. Lu- Interest in N. guyanense as a biological cia, West Indies. He proposed placing A. control agent against the fall armyworm, parasiticus in a new subfamily, Acugutturi- frugiperda (J. E. Smith), has re- nae, in the family Aphelenchoididae. All suited in numerous studies. Research has stages of the nematode were found on the been done to document its host range on insect's body surface. The nematode feeds nontarget species of insects and its patho- on the adult as well as on the nymphal genicity on targeted insect taxa, and to ob- stages of its host (3). Acugutturus parasiticus tain information on its biology, ecology, has an unusually long stylet (50-60 p,m), and infectivity. This article reviews the re- search published on this remarkable nematode. Received for publication 15 February 1995. Most of the research to date has been 1 Symposium paper presented at the 33rd Annual Meeting of the Society o f Nematologists, 14-18 August 1994, San An- conducted using one of the nematode's tonio, TX. natural hosts, the fall armyworm, because USDA ARS, U.S. Vegetable Laboratory, 2875 Savannah Highway, Charleston, SC 29414. it is the most common economically impor- ~USDA ARS, Insect Biology and Population Management tant host for N. guyanense (14,18,19). The Research Laboratory, P.O. Box 748, Tifton, GA 31793. The authors thank N. D. Epsky, O. G. Marti, J. A. Thies, fall armyworm is among the most destruc- and C. E. Thomas for manuscript review. tive pests of agriculture in the southeast- The JOURNAL OF NEMATOLOGY for December (27:423-528) 1 was issued 30 January 1996.

...... I I I • I • ' ...... 2 Journal of Nematology, Volume 28, No. i, March 1996 ern United States (32), Caribbean Basin, readily than juveniles (25). In addition, the Central America, and South America more frequently the host mates, the more (10,21). likely it will acquire or disseminate N. guyanense. Spodoptera frugiperda females DESCRIPTION AND BIOLOGY may mate up to 11 times and males up to 15 times during their lifetimes (23). Al- The adult of N. guyanense is yellowish though they mate over most of their life when feeding on its host in nature. In the span, the highest incidence of mating oc- laboratory it is pale, but the color may vary curs during the first 2-3 days after reach- depending on its host and the diet of its ing the adult stage (23,27). host. The effect of the host's diet on the Optimal development and population color of the nematode was illustrated by growth ofN. guyanense occurs at about 32C feeding infested fall armyworm (25), which is the optimal temperature for blue-dyed sucrose solution. Nematodes re- mating in the fall armyworm (23). En- covered from these moths had a bluish doparasitic nematodes are very susceptible hue. Morphologically, adults of N. guya- to low relative humidity (33). For example, nense are distinct because of their swollen Steinernema carpocapsae Weiser survives body, a long stylet (in excess of 100 txm), well near 100% RH, but mortality is almost and shape and size of spicules; the spicules 100% at 85% relative humidity while on are large, each with a long basal projection the surface of leaves (5). Conversely, N. (14). Noctuidonema guyanense has no inter- guyanense is able to survive in a low ambient mediate resting or infective stages and relative humidity (e.g., 20% RH), although spends its entire life on the adult moth. an environment with 80% RH is more con- Attempts to rear this nematode in vitro ducive to population increases (25,26,29). have been unsuccessful, suggesting that it Moreover, a higher relative humidity is is a true obligate ectoparasite. Noctui- more favorable for nematode transfer to a donema guyanense most commonly occurs new host than is a lower relative humidity on the posterior abdominal segments of (25). Unlike most other entomopathogenic the adult host (16). However, a host also nematodes, which are usually in a pro- may harbor nematodes on its thorax when tected environment such as soil or water, it is heavily infested. N. guyanense is exposed to and can with- Noctuidonema guyanense transfers during stand the fluctuations of ambient condi- host mating (14,25). The greater the num- tions experienced by its adult hosts. ber of nematodes on the host, the more likely nematodes will be transferred to a HOST RANGE new host. Moreover, the longer the dura- tion of host mating, the more likely nema- Five families of Lepidoptera are hosts of todes will be transferred to a new host. The Noctuidonema: , , nematode apparently transfers actively , Pyralidae, and Sphingidae and passively to a new host during host (14,18,19,24). Most host species are in the mating. Moths of the fall armyworm mate family Noctuidae. Remillet and Silvain (14) for an average of 130 minutes, but have initially reported this nematode attacks six been observed in copula for as long as 6.25 species in the family Noctuidae (Spodoptera hours (23). Even when moths are in copula androgea (Cramer), S. frugiperda, S. latifacia for only 15 minutes, a previously unin- Walker, S. marima (Schaus), infecta rested moth can acquire N. guyanense (15). (Ochsenheimer), and Leucania spp.) in There is a positive correlation between the French Guiana. Subsequently, this nema- number of nematodes on a new host and tode was found on 35 additional species of the duration of host mating (25). Adult as noctuids including: two species of Agrotis well as juvenile nematodes can transfer to (cutworms), six species of , two spe- a new host, but adults transfer more cies of Ptichodis, four species of Spodoptera, Ectoparasites of Adult Lepidoptera: Simmons, Rogers 3

Lesmone formularis (Htibner), PseudaIetia Americas; it occurs at least from southern unipuntata (Haworth) (armyworm), Zale fic- Brazil into the United States and through- tilis (Guen6e), and out the Caribbean and Bermuda. Nema- (Cramer) in French. Guiana (18), Mexico todes were recovered similar to Noctui- (24), and the United States (19) (Table 1). donema from alcohol-preserved specimens In French Guiana, no ectoparasitic nema- of unidentified moths that had been col- tode was found infesting 121 species of lected in 1969 from Bel6m, Brazil (24). Noctuidae and 55 species of other lepi- It is not known how long N. guyanense dopterans (18). In addition, non- has occurred in the United States. How- lepidopteran of French Gui- ever, based on an examination of stored ana were examined including 12 orders lepidopteran samples housed at the De- and 70 families of Insecta, two orders and partment of Plant Industry, Gainesville, 6 families of Arachnida, and 1 family of Florida, N. guyanense has occurred in Diplopoda, but none were infested. In the southern Florida at least as early as 23 May southeastern United States, 65 species of 1972 (24). As in the tropical locations, N. Noctuidae and 70 other species of Lepi- guyanense probably has existed on the fall doptera from 20 other families were neg- armyworm for a long time in the United ative for Noctuidonema (19). Larvae and States, but was not detected. nymphs of several species were examined The fall armyworm is a migratory insect. in French Guiana and the United States, During the spring, it migrates to northern but no ectoparasitic nematodes were re- states from overwintering sites in southern covered; they were found only on adult Texas and southern Florida. A study was Lepidoptera (18,19). conducted to determine if N. guyanense were transported with this migratory pest. DISTRIBUTION AND DISPERSAL This ectoparasite was recovered from 17 widely separated locations throughout the The fall armyworm has been studied ex- eastern half of the United States, extend- tensively since it was recognized as a pest in ing from Florida to New Hampshire, and the mid-1700 (6). Apparently, no one westward to Indiana, Kansas, and west found ectoparasitic nematodes on this pest Texas. Noctuidonema guyanense was recov- before the 1980s. In 1987-89, an extensive ered at all locations from which the host study was conducted to determine the dis- was collected (26). tribution of N. guyanense. Fall armyworm moths were used to detect the presence of SEASONAL ABUNDANCE this parasite. Pheromone traps with artifi- cial fall armyworm lures were set up at sites The abundance of N. guyanense varies in South America, Central America, the among locations and across seasons. In Caribbean basin, Bermuda, and southern tropical and subtropical sites where the fall North America. All of these locations have armyworm has overlapping generations active overlapping populations of the fall year round, parasitism by N. guyanense armyworm year round (2,6,30,31). Noctui- ranged from nearly 0% to about 90%, with donema guyanense was recovered from fall an average of 30 to 40 nematodes per armyworm moths at all sites surveyed. Be- moth (24,29). Likewise, at sites where its cause N. guyanense is transferred to a new host does not survive year round, the inci- host during host mating (25), it is essential dence of parasitism varies during the year. that its host have overlapping generations The initial migrant moths are usually not for its sustenance; such is the case for the parasitized or have only a few nematodes. fall armyworm in the surveyed tropical In the United States, after the fall army- and subtropical locations. worm migrates to northern sites in spring Noctuidonema guyanense has a wide distri- or summer, the percentage of parasitism bution in the tropical and subtropical and .the number of nematodes harbored 4 Journal of Nematology, Volume 28, No. 1, March 1996

TABLE 1. Lists of hosts of" Noctuidonema guyanense.

Host group a Reference Lasiocampidae Euglyphis sp. Rogers et al, (19) Noctuidae Acronictinae Iscadiafurcifera (Walker) Rogers et al. (18) Amphipyrinae Elaphira sp. Rogers et al. (19) Oxythres splendens Druce Rogers et al. (18) Spodoptera eridania (Cramer) Rogers et al. (19) Spodoptera androgea (Cramer) Remillet and Silvain (14) Spodoptera dolichos (Fabricius) Rogers et al. (18) Spodoptera frugiperda (J. E. Smith) Remillet and Silvain (14) Spodoptera latifascia Walker Remillet and Silvain (14) Spodoptera marima (Schaus) Remillet and Silvain (14) Spodoptera ornithogaUi (Guen6e) Rogers et al. (19) Spodoptera sp. Rogers et al. (18) Anomis oedema Guen6e Rogers et al. (18) Ephyrodes cacata Guen6e Rogers et al. (19) Lesmoneforraularis (H~ihner) Rogers et al. (18) Melipotis fasciolaris (Hfibner) Rogers et al. (18) Metria sp. Rogers et al. (18) Mocis d~fluens Guen~e Rogers et al. (18) Mocis diplocyma Hampson Rogers et al. (18) Mocis disseverans (Walker) Rogers et al. (19) Mocis latipes (Guen6e) b Rogers et al. (18) Mocis marcida (Guen~e) Rogers et al. (19) Mocis texana (Morrison) Rogers et al. (19) Nymbis arcuata Walker Rogers et al. (18) Ptichodis agrapha Hampson Rogers et al. (18) Ptichodis vinculum (Guende) Rogers et al. (19) Zalefictilis (Guen~e) Rogers et al. (18) Erebiinae Itomia opisthographa Guen6e Rogers et al. (18) Selenisa sp. Rogers et al. (18) Leucania spp. Remillet and Silvain (14) Tandilia rodea Schaus Rogers et al. (18) Pseudaletia unipuncta (Haworth) Rogers et al. (17) Xanthopastis timais (Cramer) Rogers et al. (18) (Ochsenheimer) Remillet and Silvain (19) Agrotis ipsilon (Hufnagel) Simmons and Rogers (24) Agrotis subterranea (Fabricius) Rogers et al. (19) Agrapha oxygramma (Geyer) Rogers et al. (19) Argyrogramma verruca (Fabricius) Rogers et al. (18) Notodontidae Nystalea eutalanta (Dyar) Rogers et al. (18) Pyralidae Lamprosema moccalis Schaus Rogers et al. (18) Sphingidae Erinnys obscura (Fabricius) Rogers et al. (18)

a Family, subfamily, and species of Insecta. b Marti and Rogers (7) described a new species of nematode, N. dibolia, on this host. Ectoparasites of Adult Lepidoptera: Simmons, Rogers 5 by moths peaked in mid- to late August its hosts. In the laboratory, N. guyanense and declined to few or no nematodes by decreased fertility but had no apparent ef- mid- to late October (26). The initial low fect on fecundity of the fall armyworm level of infestation in the spring suggests (28). Fertility of the fall armyworm was af- that the more heavily infested moths may fected more at 20C than at 30C, suggesting be less able to migrate. The decline and that the effect of the nematode on the fall subsequent low infestation level in the late armyworm was increased by the stress of fall may be primarily correlated with de- low temperature. Survival of male and fe- creasing temperature. male fall armyworm moths is decreased Temperature and humidity are impor- when infested with N. guyanense (28). The tant regulators ofN. guyanense populations nematode reduced survival of the female and its levels of parasitism (25,29). In ad- fall armyworm less (15%) than it reduced dition, nematode populations are highly survival of male moths (30%) (28). It is not correlated with the percentage of host known why female moths were less af- population infested (22,24,26,29). Nema- fected than male moths, although the fe- tode population and infestation levels were male moths are larger and may harbor higher on moths in the southeastern about twice as many nematodes as the male United States than on moths from more moths. western and northern states (26). Corre- spondingly, temperature averages are CONCLUDING REMARKS higher and vapor pressure deficiencies (an index of humidity) averages are lower in Although much information has been southeastern states than in mid-western obtained about this nematode, many ques- and northeastern states (26). Moreover, at tions still remain unanswered. For exam- tropical and subtropical sites, N. guyanense ple, how many species of ectoparasitic Noc- was more numerous and occurred more tuidonema exist? In 1992, Anderson and frequently on hosts at lower latitudes than Laumond described another species of at higher latitudes (24,29). However, be- Noctuidonema (N. daptria Anderson & Lau- cause there are fluctuations in nematode mond) recovered from moths of Lesmone populations at sites where the climate is porcia (Stoll), a noctuid, in Guadeloupe, fairly stable year round, factors other than West Indies (1). In 1995, Marti and Rogers temperature and vapor pressure defi- described N. dibolia from M. latipes in ciency (e.g., migration and age of host) also Tifton, Georgia (7). may affect the population of N. guyanense. Transportation of N. guyanense during migration of its fall armyworm host to new PATHOLOGY habitats enables the nematode to maintain continued pressure on its host population. Microscopic examination of infested This enhances the biological control po- hosts revealed several chronic pathologies tential of N. guyanense relative to other bi- associated with feeding by N. guyanense (8, ological control organisms that affect im- 17,20). Infested moths have small (5-50 mature stages, but which are left behind as p.m), irregular, dark spots of oxidized he- adults migrate to new locations. Increases molymph on their cuticle and interseg- in the likelihood of nematodes transfer- mental membranes (8,20). Also, cuticutar ring to a new host because of lengthy and depression, cuticular erosion, and intracel- frequent mating by an infested moth as lular bacteria occur in association with the well as decreases in host survival and fer- nematodes (8,9,20). In heavily infested tility from infestation by N. guyanense all moths, the intersegmental space of the add to the biological control potential of host may become enlarged at the expense the nematode. The effect the nematode of the hemocoel (8,17). It appears that has on the migratory ability of its hosts is Noctuidonema feeds on the hemolymph of not understood. Circumstantial evidence 6 Journal of Nematology, Volume 28, No. 1, March 1996 suggests that the nematodes are debilitat- 10. Mitchell, E. R., and V. H. Waddill. 1984. Pref- ing to flight ability of their hosts at some ace-fall armyworm symposium. Florida Entomolo- gist 67:323. threshold population. For example, the I1. Nickle, W.R., and D.J. Hooper. 1991. The first migrant moths in early spring harbor aphelenchina: Bud, leaf, and insect nematodes. Pp. few or no nematodes. Also, moths cap- 465-507 in W. R. Nick]e, ed. Manual of agricultural nematology. New York: Marcel Dekker. tured in pheromone traps tend to harbor 12. Poinar, G. O., Jr. 1972. Nematodes as faculta- low populations of nematodes relative to tire parasites of insects. Annual Review of Entomol- the capacity of the fall armyworm to har- ogy 17:103-122. bor nematodes in the laboratory under 13. Poinar, G. O., Jr. 1975. Entomogenous nema- todes: A manual and host list of insect-nematode as- warm humid conditions. Noctuidonema sociations. E. L. Brill, Leiden, Netherlands. guyanense is best adapted to a tropical en- 14. Remillet, M., and J. F. Silvain. 1988. Noctui- vironment; high temperature and relative donema guyanense n. g., n. sp. (Nematoda: Aphelen- humidity are favorable for its survival. choididae) ectoparasite de noctuelles du genre Spodoptera (Lepidoptera: Noctuidae). Revue de Moreover, its performance under warm N6matologie 11:21-24. conditions and its tolerance of low relative 15. Rogers, C. E., and O. G. Marti, Jr. 1992. Noc- humidity are aspects of its bionomics tuidonema guyanense (Nematoda: Aphelenchoididae): which favor its use as a biological control Population profiles on male and female fall army- worm moths. Journal of Entomological Science 27: agent against the fall armyworm. 354-360. 16. Rogers, C. E., and O. G. Marti, Jr. 1992. Infes- LITERATURE CITED tation and dispersal of Noctuidonema guyanense Remil- let and Silvain (Nematoda: Aphelenchoididae) on 1. Anderson, R. V., and C. Laumond. 1992. Noc- Spodopterafrugiperda (]. E. Smith) (Lepidoptera: Noc- tuidonema daptria, n. sp. (Nematoda: Aphelenchoi- tuidae). Environmental Entomology 21:417-421. didae), an ectoparasite of the moth Lesmone porcia 17. Rogers, C. E., O.G. Marti, and A. M. Sim- (Stoll). Journal of Nematology 24:16-22. mons. 1993. Noctuidonema guyanense (Nematoda: 2. Andrews, K. L. 1988. Latin America research on Aphelenchoididae): Host range and pathogenicity of Spodopterafrugiperda (Lepidoptera: Noctuidae). Flor- the fall armyworm, Spodoptera frugiperda (Lepi- ida Entomologist 71:630-653. doptera: Noctuidae). Pp. 27-32 in R. Bedding, R. 3. Hunt, D.J. 1980. Acugutturus parasiticus n.g., Akhurst, and H. K. Kaya, eds. Nematodes and the n.sp., a remarkable aphelenchoid nematode from biological control of insect pests. East Melbourne: Pe~planeta americana (L.), with proposal of Acugut- CSIRO Publications. turinae n. subf. Systematic Parasitology 1:167-170. 18. Rogers, C. E., O. G. Marti, A. M. Simmons, 4. Hunt, D.J. 1993. Aphelenchida, Longidoridae, and J. F. Silvain. 1990. Host range of Noctuidonema and Trichodoridae: Their systematics and bionomics. guyanense (Nematoda: Aphelenchoididae): An ecto- CAB International, UK: Cambridge University Press. parasite of moths in French Guiana. Environmental 5. Kamionek, M., I. Maslana, and H. Sandner. Entomology 19:795-798. 1974. The survival of invasive larvae of Neoaplectana 19. Rogers, C. E., A. M. Simmons, and O. G. carpocapsae Weiser in a waterless environment under Marti. 1990. Parasitism of Lepidoptera adults by Noc- various conditions of temperature and humidity. tuidonema guyanense Remillet and Silvain (Nematoda: Zeszyty Problemowe Postepow Nauk Rolniczych. 154: Aphelenchoididae) in southeastern United States. 409-412. Journal of Agricultural Entomology 7:241-245. 6. Luginbill, P. 1928. The fall armyworm. USDA 20. Rogers, C. E., A. M. Simmons, and O. G. Technical Bulletin 34:1-92. Marti. 1991. Noctuidonema guyanense: An ectoparasitic 7. Marti, O.G., and C. E. Rogers. 1995. Noctui- nematode of fall armyworm adults in the tropical donema dibolia, n. sp. (Aphelenchida: Acugutturidae), Americas. Florida Entomologist 74:246-257. an ectoparasite of the moth Mocis latipes (Lepi- 21. Santiago-Blay, J.A. 1983. Plumeria rubra: A doptera: Noctuidae). Journal of Nematology. 27: new plant record of the fall armyworm (Lepidoptera: 387-394. Noctuidae) in Puerto Rico. Florida Entomologist 66: 8. Marti, O. G., C. E. Rogers, J. F. Silvain, and 359. A. M. Simmons. 1990. Pathological effects of an ec- 22, Silvain, J. F., and M. Remillet. 1993. Ecology toparasitic nematode Noctuidonema guyanense (Nema- and biology of Noctuidonema guyanense (Nematoda: toda: Aphelenchoididae) on adults of the fall army- Aphelenchoididae), an ectoparasite of Spodoptera fru- worm (J. E. Smith). Annals of the Entomological So- giperda (Lep., Noctuidae), in French Guiana. Ento- ciety of America 83:956-960. mophaga 38(4):465-474. 9. Marti, O. G., C. E. Rogers, and E.L. Styer. 23. Simmons, A. M., and O. G. Marti, Jr. 1992. 1995. Report of an intracellular bacterial symbiont in Mating by the fall armyworm (Lepidoptera: Noctu- Noctuidonema guyanense, an ectoparasitic nematode of idae): Frequency, duration, and effect of tempera- Spodopterafrugiperda. Journal of Invertebrate Pathol- ture. Environmental Entomology 21:371-375. ogy 66:94-96. 24. Simmons, A. M., and C. E. Rogers. 1990. Dis- Ectoparasites of Adult Lepidoptera: Simmons, Rogers 7 tribution and prevalence of an ectoparasitic nema- Spodoptera frugiperda (Lepidoptera: Noctuidae). Bio- tode, Noctuidonema guyanense, on moths of the fall ar- logical Control 4:285-289. myworm (Lepidoptera: Noctuidae) in the tropical 29. Simmons, A. M., C.E. Rogers, K.U. Buck- Americas. Journal of Entomological Science 25:510- mire, B. Gray, K.D. Monkman, A. Pantoja, J. R. 518. Raulston, and V. H. Waddill. 1991. Seasonal chronol- 25. Simmons, A. M., and C. E. Rogers. 1990. Tem- ogy of Noctuidonema, an ectoparasitic nematode of perature and humidity effects on Noctuidonema adult moths, in tropical and subtropical America. (Nematoda: Aphelenchoididae), an ectoparasite of Florida Entomologist 74:311-319. adult Spodoptera frugiperda (Lepidoptera: Noctuidae) 30. Snow, J. W., W. W. Cantelo, R. L. Burton, and and transfer success during host mating. Annals of S.D. Hensley. 1968. Populations of fall armyworm, the Entomological Society of America 83:1084-1087. corn earworm, and sugarcane borer on St. Croix, 26. Simmons, A. M., and C. E. Rogers. 1991. Dis- U.S. Virgin Islands. Journal of Economic Entomol- persal and seasonal occurrence of Noctuidonema ogy 61:1757-1760. guyanense, an ectoparasitic nematode of adult fall ar- 31. Snow, J. W., and W. W. Copeland. 1969. Fall myworm (Lepidoptera: Noctuidae), in the United armyworm: Use of virgin female traps to detect males States. Journal of Entomological Science 26:136-148. and to determine seasonal distribution. USDA-ARS 27. Simmons, A. M., and C. E. Rogers. 1994. Fall Production Research Report. 110, 9. armyworm (Lepidoptera: Noctuidae) mating effects of age, and scotophase on pre-mating time, mating 32. Sparks, A.N. 1986. Fall armyworm (Lepi- incidence, and fertility. Journal of Entomological Sci- doptera: Noctuidae): Potential for area-wide manage- ence 29:201-208. ment. Florida Entomologist 69:603-614. 28. Simmons, A. M., and C. E. Rogers. 1994. Ef- 33. Wouts, W.M. 1984. Nematode parasites of fect of an ectoparasitic nematode, Noctuidonema Lepidoptera. Pp. 655-696 in W. R. Nickle, ed. Plant guyanense, on adult longevity and egg fertility in and insect nematodes. New York: Marcel Dekker.