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Ectoparasitic Acugutturid Nematodes of Adult Lepidoptera 1 A

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Ectoparasitic Acugutturid Nematodes of Adult Lepidoptera 1 A 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 Lepidoptera 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 moth 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 insects. 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 insect (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- Spodoptera 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 moths (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: Lasiocampidae, Noctuidae, nematode apparently transfers actively Notodontidae, 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), Anicla 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 Mocis, 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 Xanthopastis timais 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 arthropods 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).
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