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Entomopathogenic Nematodes for the Biological Control of Insects 1

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Entomopathogenic Nematodes for the Biological Control of Insects 1 Supplement to the JOURNAL OF NEMATOLOGY VOLUME 27 DECEMBER 1995 NUMBER 4S Supplement to the Journal of Nematology 27(4S):529-534. 1995. © The Society of Nematologists 1995. VIEWPOINT Entomopathogenic Nematodes for the Biological Control of Insects 1 G. C. SMART, JR. 2 Nematode parasites of insects have been rode in the various plots ranged from 0.3% known since the 17th century (33), but it to 81%. They determined nematode per- was only in the 1930s, that serious consid- sistence in four of the plots by placing eration was given to using a nematode to healthy beetle larvae in the plots and later Control an insect. In 1929, Glaser and Fox examining them for infection. The nema- (19) found a nematode infecting grubs of tode persisted in the plots for the 8.5 years the Japanese beetle, PopilIiajaponica, at the of their trials (18,20). Tavistock Golf Course near Haddonfield, Glaser's outstanding research should New Jersey. Steiner (44) described the have issued in an era of biological control nematode that same year as Neoaplectana using entornopathogenic nematodes. In- (= Steinernema) glaseri. We now know that stead, the widespread use of the highly ef- these nematodes carry a symbiotic bacte- fective and relatively inexpensive persis- rium which provides essential food for the tent pesticides during the 1940-1960 pe- nematodes whether they are infecting a riod caused Glaser's work to be forgotten host or in culture. Glaser was not aware of temporarily. In the 1960s and 70s, when the symbiotic bacterium (5); nonetheless, some persistent pesticides became unavail- the methods that he devised to culture the able due to action by the U.S. Environmen- nematode in vitro were suitable for the tal Protection Agency, there was renewed bacterium to multiple (16,17). interest in entomopathogenic nematodes Glaser and colleagues produced suffi- as biological control organisms, and inves- cient numbers of the nematode for field tigations on them have been carried out trials and in the 1930s applied it to 73 dif- since. ferent field plots in New Jersey to control Classification and biology: The genus Stein- the Japanese beetle (17,20). Parasitized ernema is in the family Steinernematidae grubs were recovered from 72 of the 73 (Rhabditida: Nematoda). The family con- plots two weeks after application. Parasit- tains one other genus, Neosteinernema, with ism of the grub population by the nema- a single species, N. longicurvicauda, a para- site of termites (31). In 1976, Poinar (38) described a new genus and species of en- tomopathogenic nematode, Received for publication 1 August 1995. Heterorhabditis a Florida Agricultural Experiment Station Journal Series bacteriophora, which he placed in a new No. R-04644. Professor, Entomology and Nematology Department, In- family, Heterorhabditidae (Rhabditida: stitute of Food and Agricultural Sciences, University of Flor- Nematoda). The two genera Steinernema ida, Gainesville, FL 32611-0620. and contain the most impor- The author thanks R. McSorley and K. B. Nguyen for cri- Heterorhabditis tiquing the manuscript. tant species of entomopathogenic nema- 529 ......... [.......... 530 Journal of Nematology, Volume 27, Supplement to December 1995 todes. Currently, there are 16 species in hosts, the second generation is omitted Steinernema and six species in Heterorhabditis. and the eggs that are laid by first-gener- All members of the Order Rhabditida ation aduk females develop into infective are bacteriophagous, and many of them juveniles. The cycle from entry of infective have phoretic associations with insects. juveniles into a host from emergence of Over time, apparently some of the nema- infective juveniles from a host is tempera- todes evolved into insect pathogens. In the ture-dependent and varies somewhat for Steinernematidae and Heterorhabditidae, different species and strains. However, it an area of the anterior part of the intestine takes about 7-10 days at 25C in Galleria of the infective juvenile is modified as a melloneUa (30,47,48). Differences for the bacterial chamber. In this chamber the in- Heterorhabditidae are that all juveniles of fective juvenile carries cells of a symbiotic the first generation become hermaphro- bacterium. The bacterium carried by dites. In the second generation, males, fe- Steinernematidae is usually a species of the males, and hermaphrodites develop. genus Xenorhabdus, and that carried by Dispersal of juveniles: The juveniles of Heterorhabditidae is a species of Photo- steinernematids and heterorhabditids dis- rhabdu~. perse vertically and horizontally, both ac- Pathogenicity and life cycle: The infective tively and passively (8,24,29,35,45). Pas- juvenile enters the insect host through the sively, they may be dispersed by rain, wind, mouth, anus, spiracles, or by direct pene- soil, humans, or insects. Active dispersal tration through the cuticle. If the mode of may be measured in centimeters, while entry is by mouth or anus, the nematode passive dispersal by insects may be mea- penetrates the gut wall to reach the hemo- sured in kilometers (43). coel, and if by spiracles, it penetrates the Survival of juveniles: The infective juve- tracheal wall. When the infective juvenile niles do not feed but can live for weeks on reaches the hemocoel of a host, it releases stored reserves as active juveniles, and for the bacteria, which multiply rapidly in the months by entering a near-anhydrobiotic hemolymph. Usually the insect dies within state. This is almost certainly the most im- 24-72 hours. Even though the bacterium portant survival strategy for the nematode. is primarily responsible for the mortality The length of time that juveniles survive in of most insect hosts, the nematode also the soil in the absence of a host depends produces a toxin that is lethal to the insect upon such factors as temperature, humid- (4). The infective juvenile becomes a feed- ity, natural enemies, and soil type. Gener- ing third-stage juvenile, feeds on the bac- ally, survival is measured in weeks to teria and their metabolic byproducts, and months, and is better in a sandy soil or molts to the fourth stage and then to males sandy-loam soil at low moisture and with and females of the first generation. After temperatures from about 15-25 C than in mating, the females lay eggs that hatch as clay soils and lower or higher tempera- first-stage juveniles that molt successively tures (1,24,26-28). The Heterorhabditi- to second-, third-, and fourth-stage juve- dae do not survive as well as do Steiner- niles and then to males and females of the nematidae (27). second generation. The adults mate and Natural enemies: Natural enemies play an the eggs produced by these second-gener- important role in the population ecology ation females hatch as first-stage juveniles of all organisms. Populations of ento- that molt to the second stage. The late sec- mopathogenic nematodes in the soil are ond_stage juveniles cease feeding, incorpo- reduced by bacteria, fungi, mites, preda- rate a pellet of bacteria in the bacterial tory nematodes, tardigrades, and other chamber, and molt to the third stage (in- soil organisms. Survival is better in steril- fective juvenile), retaining the cuticle of ized soil than in nonsterilized soil (24,29). the second stage as a sheath, and leave the Mites appear to be especially voracious cadaver in search of new hosts. In some nematode-feeders (8,28,46). Entomopathogenic Nematodes: Smart 531 Insects controlled: Insects controlled with terium, and nematodes are added 24 entomopathogenic nematodes have been hours later. Infective juveniles are har- reviewed by Georgis and Manweiler (15), vested after about 15 days. This method is Kaya (23), Klein (25), by several authors in labor-intensive and is particularly well- Nickle (32), and by Wouts (49). Some of suited for situations where labor is plenti- the insects controlled are armyworms, car- ful, and for the so-called cottage industry. penter worms, cat fleas, crown borers, cut- Production in liquid medium can be worms, filth flies, flea beetles, German done in small containers or in fermenta- cockroaches, leaf miners, mole crickets, tion tanks. Greater numbers of juveniles phorid flies, plume moths, root weevils, can be produced per unit area in fermen- sciarid flies, stem borers, webworms, and tation tanks, which makes this method es- white grubs. pecially suited for large-scale commercial Advantages of entomopathogenic nematodes: production (10,11). Entomopathogenic nematodes have cer- Comparative costs: In 1991, it was esti- tain advantages over chemicals as control mated that it costs 10-60% more to control agents. Nematodes are non-polluting and insects with nematode-based products thus environmentally safe and acceptable, than with chemical insecticides (14). That although some countries do not allow the is changing, however, as technological im- release of non-indigenous species. Infec- provements in production, formulation, tive juveniles can be applied with conven- packaging, and shelf life of nematode tional equipment (13), and they are com- products occur. Since nematode products patible with most pesticides (6,9,40,41). are safe to apply and do not contaminate They find their hosts either actively or pas- the environment, some clients will opt for sively, and in cryptic habitats and some- a biological control method even at a times in soil, they have proven superior' to higher cost. Also, at least in some situa- chemicals in controlling the target insect tions, the nematodes become established, (12). They are not well-suited for foliar ap- recycle, and their offspring continue to plication, however, since they are sensitive control the target insect (35-37). Thus, the to desiccation and ultraviolet radiation. higher short-term cost may be lower in the The nematodes usually reproduce in the long run when continued control by the insect host and thus provide new infective recycling nematode is obtained. In Florida, juveniles to search for additional host in- a recreational turf area supervisor, who sects.
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