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1 Aricle bibliographique NON-INSECT NEOAPLECTANA (STEINERNEMATIDAE) HOSTS FOR THE ENTOMOGENOUS RHABDITOID NEMATODES AND HEZ-ERORHABDITIS(HETERORHAB George O. POINAR, Jr. Deparmen of Enomological Sciences, Universiy of California, Berkeley, CA 94720, USA. The rhabdioid genera Neoaplecana (Seinernemaidae) and Heerorhabdiis (Heerorhabdiidae) are considered as enomogenous nemaodes. This is because al1 naural hoss of hese nemaodes were insecs and because under laboraory condiions, hese nemaodes develop mos suiably in insecs. In conras o he ypical obligae parasies of inverebraes, members of he above wo families are unique in producing hirdsage juveniles which cany and release symbioic baceria (Xenorhabdus s~.) ino he body caviies of heir hoss, hus esablishing an environmen conducive for nemaode developmen and muliplicaion. The major characerisic which makes hese nemaodes " parasiic " is he abiliy of he hird-sage dauer (= infecives) o penerae ino he body caviy of living insecs and iniiae developmen. Since he hos normally dies wihin 24 hours afer he nemaode has enered, developmen in Heerorhabdiis and Neoaplecana is similar o ha of microborophic rhabdioids which feed on baceria in decaying habias. The major difference is ha hese wo genera have become dependen on he presence of Xenorhabdus for opimum developmen. The major funcions of he baceria are a source of nourishmen and he producion of anibioic compounds o mainain a sable habia. The effec of hese compounds on microorganisms in he environmen have been cied by Gregson and McInerney (1986). The basic prerequisies for successful developmen of hese nemaodes require compleion of he following seps : 1) peneraion ino he body caviy of he poenial hos, 2) release of he symbioic baceria, 3) developmen o he adul sage, and 4) muliplicaion and producion of infecive sage juveniles. Whereas hese condiions are normally me in holomeabolous insecs which represen he majoriy of naural hoss for hese nemaodes, hey are rarely me in oher animals. The presen paper discusses examples in non-insecs where peneraion, moraliy, developmen or occasionally infecive juvenile formaion occur. Table 1 Moraliy of Onconzelania hupensis snails by Neoaplecana and Heerorhabdiis nemaodes (modified from Li e al. (1986)). Nemaode species Number of Number of Number O. hupensis dead of snails esed O. hupensis wih developing nemaodes N. glaseri N. carpocapsae N. bibionis H. heliohidis 10 5 O (NC srain) H. heliohidis (T 327 srain) Conrol 10 O O Table 2 Increase in numbers of infecive sage N. glaseriafer infecing he snail, Onconlelania hupensiswih hree dosages (modified from Li e al. (1986)). Dosage Number of Averag nunber of livins I increase of (nerm(oo) O. hupensis and dead nernaodesfiorn nernaodes over exarnined ilfeced0. hupensis iniial dosage living dead 106, ) (1 774 ( ) 15 (340/un2) 84, ( ) 460( ) 69 (300/cm2) 62, ( ) 370( ) 65 (200/cm2) Revue Némaol. 12 (4) (1989) 423

2 G. O. Poinar, Jr. CLASS GASTROPODA Phylum Mollusca A sudy by Li e al. (1986) was he firs o show ha Neoaplecana and Heerorhabdiis nemaodes could infec a snail. They repored moraliy in he semi-aquaic Oncomelania hupensis (Hydrobiidae) from infecions wih H. heliohidis, N. bibionis, N. carpocapsae and N. glaseri. Al1 four species showed some developmen in he snail, alhough N. gluseri appeared o be he bes adaped o his hos (Tab. 1). In furher experimens, living snails were added o 4.5 cm plasic dishes conaining moisened soi1 ogeher wih various concenraions of N. glaseri. Afer being held a 17-23' for one week, he snails were crushed and he number of nemaodes couned. Nemaode peneraion, bacerial release, nemaode developmen and producion of infecive juveniles occurred wih N. glaseri (Li e al., 1986) (Tab. 2). CLASS CRUSTACEA I Phylum Arhropoda Under laboraory condiions, Poinar and Paff (1985) demonsraed ha boh N. carpocapse and H. heliohidis were able o infec and develop in he hemocoel of he erresrial isopods, Amadillidium vulgare and Porcellio scaber. Alhough he body Wall broke down shorly afer he hos's deahs and he body caviy was invaded by oher microorganisms, some reproducion occurred and a few hundred infecive sages of boh nemaode species were produced (Tabs 3 & 4). I was ineresing ha no infecion of eiher isopod species resuled when N. glaseri was used. In laboraory experimens, Kermarrec and Mauléon (1985) placed he fresh waer prawns, Ayia innocous and Macrobrachium acanhunu in a lier of waer conaining 2 x 105 infecive sages of N. carpocapsae. No effec of he nemaodes on he shrimp was noed. I,,d. Table 3 Effec of Neoaplecana species on non-insec inverebrae hoss (NS = no saed) MOLLUSCA (Gasropoda) ARTHROPODA (SYmPhYla) (Collembola) (Arachnida) (Crusacea) (Diplopoda) Oncornelania hlrpensis Onconelania hupensis Oncomelania hupensis inmac~rlara Scu&rella amlalrs Onychilrns phalangiodes Pholclrs Larodeclrs nacans Piraa sp. Phlangirm sp. Gaypus cal$rnicus Arnadillidi~~n vrrkare Armadillidiilrm vukare Porcellio scaber Porcellio scaber Oxidus gracilis Has Nemaode Peneraion Bacerial Developmen Mul$licaion Refeence release A! glaseri Li e alj Li e al, 1986 A! bibionis - Li e alj 1986 N carpocapsae N carpocapsae N carpocapsae A! glaseri A! glaseri - - f, f Swenson, 1966 Rahayu, 1983 Poinar e al, 1985 Poinar & Thomas, 1985 B CLASS SYMPHYLA Swenson (1966) showed ha he DD-136 srain of N. carpocapsae was able o infec, develop and reproduce in he garden symphylan, Scuigerella immaculaa. Infecive-sage nemaodes emerged from parasiized hoss five o seven days afer infecion (Tab. 3). Since garden symphylans are someimes considered as plan pess, i may be feasible o use nemaodes for heir conrol. CLASS COLLEMBOLA Springails were originally considered o be insecs, however hey are now placed in a separae class. Using he DD-136 srain of N. carpocapsae, Rahayu (1983) was able o obain some infecion of Onychiurus amaus under laboraory condiions (Tab. 3). Rahayu (1983) also repored ha he applicaion of his nemaode o sugar bee fields a seedling and wo-leaf sages consider- 424 Revue Némaol. 12 (4) (1989)

3 Non-insec hoss for enomogenous nemaodes ably reduced he numbers of Collembola. Similar effecs of he DD-136 srain of N. carpocapsae on field populaions of Onychiurus collembola had been repored by Edwards and Oswald (1981). CLASS ARACHNIDA In laboraory experimens, Poinar and Thomas (1985) showed ha boh N. carpocapsae and H. heliohidis could ener and kill he aerial spiders, Pholcus phalangiodes and Larodecus macans, a ground spider, Piraa Table 4 Effec of Heerorhabdiis species on non-insec inverebrae hoss sp. and a harvesman, Phalangium sp., respecively. Alhough he nemaodes developed o he adul sage in al1 four hoss, hey reproduced and formed infecive juveniles only in Phalangium sp. An average of infecives (N = 6) of N. carpocapsae and 26 O00 infecives of H. heliohidis were produced from each parasiized Phalangium sp. (Tabs 3 & 4). The absence of reproducing forms in he oher arachnids was aribued o he appearance of foreign baceria which made he cadavers unhospiable for he developing nemaodes. Hos Nemaode Peuraion Developnea Bacerial Muliplicaion R&rence release MOLLUSCA (Gasropoda) ' Onco1nela1ia hnpensis h! heiiohidis - Li e a%, 1986 ARTHROPODA (Arachnida) (Crusacea) (Diplopoda) Pholcrrs phalangiodes Larodecus macans Piraa sp. Alangirrn sp. Gayprrs califomicus Amradiliidiun~ vrrlgare Porcellio scaber Oxidus gracilis h! heliohidis h! heliohidis h! hekohidis h! heliohidis h! Mohidis h! heliorhidis h! heiiohidis h! heliohidis Poinar e a%, 1985 Poinar & Thomas, 1985 B The pseudoscorpion, Ga ypus californicus, also proved suscepible o infecion by N. carpocapsae and H. heliohidis (Poinar, Thomas & Lee, 1985). The nemaodes released heir symbioic baceria, developed o he adul sage and muliplied in he hos cadaver (Tabs 3 & 4). However, as a resul of foreign baceria in he environmen, only a few infecives were formed. CLASS DIPLOPODA Under laboraory condiions, Poinar and Thomas (1985 b) showed ha boh N. carpocapsae and H. heliohidis were able o infec and kill he garden millipede, Oxidus gracilis. Alhough he peneraing infecives did liberae heir Xenorhabdus baceria, a quick encapsulaion reacion and enmeshemen of he nemaodes in he hos's racheoles and connecive issue resriced furher developrnen. Phylum Verebraa CLASS PICES Kermarrec and Mauleon (1985) challenged 30 speci- Revue Nénaol. 12 (4) (1989) mens of he fish, Lebiser reiculaus wih infecive-sage N. carpocapsae in a lier of waer. No nemaode developmen or any effec on he fish was noed (Tab. 5). CLASS BPTILIS Kermarrec and Mauléon (1985) challenged en individuals of he lizard Anolis mannoraus wih 5 O00 infecive sages of N. carpocapsae every hird day for 30 days. No moraliy of he lizards were observed (Tab. 5). In a single case, some necrosis of he inesinal epihelium adjacen o a mass of dead infecive-sage nemaodes was noed. Poinar and Miller (unpubl. rep., 1988) challenged snapping urle hachlings ber os) wih infecives of N. carpocapsae and H. heliohidis, respecively (N = 20 for each nemaode species). NO moraliy or signs of disease were noed in he urles afer wo weeks. CLASS AMPHIBIA Under laboraory condiions, Kermarrec and Mau- Iéon (1985) demonsraed ha N. carpocapsae could quickly kill adpoles of Bufo man'nus (Tab. 5). Chal- 425

4 G. O. Poinar, Jr. - Table 5 Resuls of exposing rhabdioid enomogenous nemaodes o verebraes Class Hos Nenaode Mehod Dose Efic R$rence Applicaion # il?fecivcs Pices Repilia Amphibia Aves Mammalia Lebises reicnlaus r1arnmau. Anolis BI@ marinus Hvla regilla Hda regilla Xenopus laevis Xenopus laevis gallus Gallrrs (chicken) pennsylvanicus Microns Raus raus R a m raus Raus Raus raus raus H heliohidis R heliohidis A! glaseri H heliohidis N bibionis h! glaseri H heliohidis h! bibionis h! bibionis in waer in waer in waer in waer in waer in waer inerperioneally inerperioneally subcuaneously subcuaneously subcuaneously subcuaneously inerperioneal inerperioneal 2 x 10 none 50,000 none loolml mordiy of young adpoles 100,200 moraliy of and 400/ml young adpoles 100,200 moraliy of and 4001ml young adpoles ZOO, 400 moraliy of and 800lml young adpoles ZOO, 400 moraliy of and 800/ml young adpoles 60,000 none 200,000 none 200,000 none 56,000 some nemaode viabiliy afer 5 days 50,000 some nemaode viabiliy afer 2 days 50,000 none 1,000 no developmen 1,000 no developmen 62,500 no developmen (over 25 days) 1000; 10,000 no developmen 1000; 10,000 no developmen 1000; 10,000 no developmen 1000; 10,000 no developmen 2 x 104 ulcers in skin 10 x 104 no nema develop. 2 x 104 ulcers in skin 10 x 104 no nema develop. 2 x 10 no developmen IO x x IO4 no developmen 10 x 104 Kermarrec & Maulion, 1985 Schrniege, 1963 Nurilie Producs, Inc. (in Poinar, 1979) Jackson & Bradbury, 1970 Gaugler & Boush, 1979 Gaugler & Boush, 1979 Poinar e al, 1982 Poinar e al, 1982 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 Kobayashi e al, 1987 lenging 60 adpoles wih a dose of 100 nemaodesld (1 O00 ml conainer) resuled in 100 O/O moraliy afer five days. The auhors noed ha dead clusered bundles of infecive sages were recovered from he bucal caviy and inesine of he adpoles, however no explanaion of he cause of deah was given. Afer hundreds of dissecions, hey recovered an adul female nemaode from he body caviy of one adpole. Poinar and Thomas (1988) performed similar ess wih N. carpocapsae and H. heliohidis agains he adpoles of he wesern ree frog, Hyla regilla and he clawed frog, Xenopus laevis. Boh nemaode species could kill young adpoles of bohos species, respecively (Tab. 5). The infecives were ingesed by he adpoles, peneraed hrough he gu wall, enered he body caviy and in a few cases wih N. carpocapsae released heir symbioic baceria. In wo insances, he infecives of N. carpocapsae developed ino maure females in he body caviy of heir adpole hoss. Boh Kermarrec and Mauléon (1985) and Poinar and Thomas (1988) noed ha he suscepibiliy of adpoles decreased markedly wih age, which was probably correlaed wih a hickening of he epihelial gu wall, hus making i more difficul for he nemaodes o ener. The laer auhors also noed a rapid defense reacion involving encapsulaion of he nemaodes by blood cells in H. regilla. 426 Revue Némaol. 12. (4) (1989)

5 Non-insec hoss for enomogenous nemaodes CLASS AVES Tess wih rhabdioid enomogenous nemaodes agains birds were conduced only by Kermarrec and Mauléon (1985). No effec was noed when 60 O00 infecives of N carpocapsae were given o 30 domesic chickens (Gallus gallus). CLASS MAMMALIA The fïrs mammalian es wih enomogenous rhabdiid nemaodes was repored by Schmiege (1963) Who fed four field (Microus pennsylvanicus) each a dose of 200 O00 infecive sage N. carpocapsae over a five-day period. Dead nemaodes were recovered from he feces and no damage o he was repored (Tab. 5). Jackson and Bradbury (1970) injeced from 5 O00 'o 6 O00 infecives of N. glaseri ino he perioneal caviy of female ras. Boh living and dead nemaodes were recovered from he perioneal caviy of reaed ras five days laer (Tab. 5). The majoriy of he recovered nemaodes were sill infecives. None had developed o he adul sage and rarely had a recovered nemaode developed beyond he hird sage. When he living nemaodes recovered from he injeced ras were placed in culure, some developed o aduls bu here was no reproducion. A he ime of removal from he ra perioneal caviy, many nemaodes were covered wih layers of ra perioneal exudae cells. Those removed afer hree days showed no cuicular aleraions, bu nemaodes recovered four and five days following injecion showed wo cuicular changes, a swollen surface shee and a disruped sriaion paern. The auhors concluded ha he laer condiion was no a resul of high emperaure bu was caused by hos cells, possibly as a resul of enzymaic acion. Mammalian ess wih enomogenous rhabdioid nemaodes also were conduced by Nurilie Producs, Inc. in 1970 (in Poinar, 1979). Al1 sages of N. carpocapsae were fed o laboraory ras. Al1 nemaodes recovered from he feces were dead and here was no inflammaion of he alimenary rac or nemaode developpmen inside he ra (Tab. 5). Since hese early aemps, and ras have been challenged wih various species of Neoaplecana and Heerorhabdiis heliohidis (Tab. 5). Gaugler and Boush (1979) inroduced 50 O00 N. carpocapsae and inraperioneally, respecively, ino five-week-old albino ras. Al1 reaed ras showed normal weigh gains over he 36-day es period and gross issue examinaion of he reaed ras sacrificed on day 36 revealed neiher nemaodes nor changes aribuable o nemaodes. Dead nemaodes were recovered from he feces of ras reaed. Some nemaodes did remain alive afer wo days when inroduced inraperioneally. However no developmen was noed and many were encapsulaed by perioneal macrophages or occasionally enmeshed in gelainous shees of hos maerial. However, he nema- Revue Némaoi. 12 (4) (1989) odes were unable o cause injury, become esablished or survive for over wo days in he ra body. Poinar e al. (1982) inoculaed 1 O00 infecive sages of H. heliohidis and N. carpocapsae, respecively, subcuaneously ino adul Swiss albino. No disease sympoms or nemaode developmen were noed in he adul during he 14-day posinoculaion period. Kobayashi, Okano and Kirihara (1987) placed doses of 1 O00 and 10 O00 infecive sages of N. glaseri, H. heliohidis, N. bibionis and N. carpocapsae, respecively, ino five-week-old male wih a somach probe. The same doses of N. bibionis and N. carpocapsae were injeced subcuaneously or inerperioneally ino similar. Mice wih oral doses were disseced afer seven days. No nemaodes were recovered and no disease sympoms were noed in hese. Alhough no hoss died, he subcuaneous injecion of nemaodes ino he hypodermal issue of resuled in ulcers in he injured porion of he skin. These ulcers became dislodged on he fourh day afer injecion and conained dead nemaodes. Dead nemaodes were also recovered from he inoculaed area on he 14h day afer injecion. The auhors concluded ha he ulcers were no specifically formed by he peneraing nemaodes, bu from an allergic reacion resuling from he injecion of foreign maerial ino he hypodermis. An allergic reacion was also considered responsible for mouse deahs afer he inerperioneal injecion of 100 O00 infecive sage N. carpocapsae. Discussion Represenaives of he classes Gasropoda, Symphyla, Collembola, Arachnida, Crusacea and Diplopoda are able o be infeced by neoaplecanid and heerorhabdiid nemaodes. However infecive juvenile producion is no compleed in every case. Thus, aside from he four basic prerequisies for successful developmen menioned earlier (peneraion, bacerial release, developmen and infecive juvenile producion), here are addiional condiions. Many inverebraes are no aacked because hey are oo small, hey are no aracive o he infecives, here are no naural openings (or hin enough cuicles in he case of Heerorhabdiis spp.) or he habia prohibis nemaode aciviy (oo dry or oo we). An aspec of arhropod srucure imporan in nemaode infecion is egumen inegriy. Wih isopod crusaceans and spiders, he body Wall breaks down rapidly afer deah, resuling in he exposure of he nemaodes o he exernal environmen. Ideal developmen for he nemaodes requires a closed environmen conaining Xenorhabdus baceria and hemolymph and he absence of hos defense reacions. A breakdown of he inersegmenal membranes resuls in he loss of his closed environmen and inerference by conaminans. I would appear ha in he case of inverebraes, one reason why hese 427

6 G. O. Poinar, Jr. nemaodes are such successful parasies of insecs is he inegral srucure of he inersegmenal hos membranes afer deah. REFERENCES EDWARDS, C. A. & OSWALD, J. (1981). Conrol of soil-inhabiing arhropods wih Neoaplecana carpocapsae. Proc Bri. Crop Proec. Con$ : GAUGLER, R. & MALLORY BOUSH, G. (1979). Nonsuscepibiliy of ras o he enomogenous nemaode, Neoaplecana carpocapsae. Environ. Enomol., 8 : GREGSON, R. P. & MCINERNEY, B. V. (1986). Xenocoumacins. Innl Paen-Public. Numb. WO 86/01509 : 22 p. JACKSON,G. J. & BRADBURY, P. C. (1970). Cuicularfine srucure and moling of Neoaplecana glaseri (Nemaoda), afer prolonged conac wih ra perioneal exudae. J. Parasiol., 56 : KERMARREC, A. & MAUL~ON, H. (1985). Nocuié poenielle du némaodenomoparasie Neoaplecana carpocapsae Weiser pour le crapaud Bzfo marinus aux Anilles. Med. Fac. Landbouww. Rijizsuniv. Gen., 50 : KOBAYASHI, M., OKANO, H. & KIRIHARA, S. (1987). Effec of enomogenous nemaodes (Seinernema and Heerorhabdiis) on he mouse. In : Ishibashi, N. (Ed.). Recen advances in Biological Conrol of insec pess by enomogenous nemaodes in Japan. Tokyo, Minisry of Educaion, Culure and Science, 179 p. LI, P. S., DENG, C. S., ZHANG, S. G. & YANG, H. W. (1986). Preliminary ess on Seinernema glaseri infecing he mail, Oncomelania hupensis, an inermediae hos of Schisosoma japonica. Chinese J. Biol. Conrol, 2 : POINAR, Jr., G. O. (1979). Nemaodes for Biological Conrol of Insecs. Boca Raon, Florida, CRC Press, 227 p. POINAR, Jr., G. O. & PAFF, M. (1985). Laboraory infecion of erresrial isopods (Crusacea: Isopoda) wih neoaplecanid and heerorhabdiid nemaodes (Rhabdiida : Nemaoda). J. Inver. Pahol., 45 : POINAR, Jr., G. O. & THOMAS, G. M. (1985 a). Laboraory infecion of spiders and harvesmen (Arachnida : Araneae and Opiliones) wih Neoaplecana and Heerorhabdiis nemaodes (Rhabdioidea). J. Arachnol., 13 : POINAR,Jr., G. O. & THOMAS, G. M. (1985 b). Effec of neoaplecanid and heerorhabdiid nemaodes (Nemaoda: Rhabdioidea) on he millipede Oxidus gracilis. J. Inver. Pahol., 45 : POINAR, Jr., G.O. & THOMAS, G. M. (1988). Infecion of frog adpoles (Amphibia) by insec parasiic nemaodes (Rhabdiida). Experienia, 44 : POINAR,Jr., G. O., THOMAS, G. M. & LEE, V. F. (1985). Laboraory infecion of Gaypus calgornicus (Pseudoscorpionida, Garypidae) wih neoaplecanid and heerorhabdiid nemaodes (Rhabdioidea). J. Arachnol., 13 : POINAR, Jr., G. O., THOMAS, G. M., PRESSER, S. B. & HARDY, J. L. (1982). Inoculaion of enomogenous nemaodes, Neoaplecana and Heerorhabdiis and heir associaed baceria, Xenorhabdus spp., ino chicksand. Environ. Enomol., Il : RAHAYU, A. (1983). Neoaplecana carpocapsae Weiser (Nem. Seinernemaidael : behavioral sudies and field applicaion. Ph. D. Diss., Swiss Federal Insiue of Technology, Ziirich, 88 p. SCHMIEGE, D. C. (1963). The feasibiliy of using a neoaplecanidnemaodeforconrol ofsome foresinsecpess. J. Econ. Enomol., 56 : SWENSON, K. G. (1966). Infecion of he garden Symphylan, Scuigerella immaculaa, wih he DD-136 nemaode. J. Inver. Pahol., 8 : Accepé pour publicaion le 3 janvier Revue Némaol. 12 (4) (1989)