Precocious larvae in the polyembryonie Copidosoma sosares (: )

Ian C.W. Hardy

HARDY, I.C.W., 1996. PRECOCIOUS LARVAE IN THE POLYEMBRYONIC PARASITOID COPIDOSOMA SO¬ SARES (HYMENOPTERA: ENCYRTIDAE). - ENT. BER., AMST. 56 (5): 88-92.

Abstract: In polyembryonie Hymenoptera, many larvae develop clonally from a single egg. Some species exhibit with- in-clone dimorphism: most larvae eventually develop into adult , but a minority of precociously developing larvae differ in form and die before pupation. Precocious larvae in some (and possibly all) species defend their genetical¬ ly identical siblings from competition by other parasitoids. In this paper I document, for the first time, the occurrence and prevalence of precocious larvae in Copidosoma sosares (Hymenoptera: Encyrtidae) and discuss their possible function.

Institute of Evolutionary and Ecological Sciences, University of Leiden, P.O. Box 9516, 2300 RA Leiden, The Netherlands.

Introduction competing endoparasitic species (Cruz, 1981, 1986a; Grbic & Strand, 1991) offering a com¬ Polyembryony, defined as the production of pelling explanation for the observed success multiple embryos from a single egg, has evol¬ of polyembryonie species faced with inter¬ ved in four families of parasitoid Hymeno¬ specific competition (Browning & Oatman, ptera: Braconidae, Platygasteridae, Dryinidae 1984; Cruz, 1986a; Strand et al., 1990). Fur¬ and the Encyrtidae (Ivanova-Kasas, 1972). thermore, precocious larvae developing from Polyembryony is the most extreme in the cop- female C. floridanum eggs attack their male idosomatine encyrtids where up to 3000 larvae siblings when male and female eggs are laid in can be produced from just one egg (Ode & the same host (Grbic et al., 1992). Intersexual Strand, 1995). In some encyrtid species, gene¬ attack is probably explained by the differing tically identical larvae are dimorphic. The ma¬ sex ratio optima of males and females due to jority, termed ‘reproductive’ larvae, eventual¬ the details of adult mating behaviour; the sex ly pupate and develop into adult parasitoids. A ratio conflict is apparently settled in favour of minority of larvae develop precociously into females (Grbic et al., 1992; see also Godfray, ‘asexuals’ which die before pupation. 1992; Hardy, 1994). Such precocious larvae were first described There is a large interspecific, intersexual in Copidosoma truncatellum (Dalman) (prob¬ and intrasexual variation in the production of ably a misidentification of Copidosoma florid- precocious larvae, the causes and consequenc¬ anum (Ashmead) (Noyes, 1988)) by Silvestri es of which are not fully understood. For in¬ (1906) who suggested that their function is to stance, C. floridanum and C. tanytmemus, re¬ macerate host tissues to assist their siblings in spectively produce up to about 50 and 20 feeding. This explanation for their reprodu¬ precocious larvae in each host (Cruz, 1986b; ctive altruism has, however, been supplanted Grbic et al., 1992), while some polyembryon¬ by subsequent observations of larval behavi¬ ie species may lack precocious larvae altoget¬ our which suggest that precocious larvae pro¬ her (references in Cruz, 1986a). In C. koehleri tect their genetically identical siblings from Blanchard (probably a misidentification of both inter- and intraspecific resource competi¬ Copidosoma desantisi Annecke and Mynhardt tion. Precocious larvae of both Copidosomo- (Annecke & Mynhardt, 1974)) precocious lar¬ psis tanytmemus Caltagirone and C. florida- vae are found in female but not male broods num have been observed attacking larvae of (Doutt, 1947). In C. floridanum, broods of Ent. Ber., Amst. 56 (1996) 89 both sexes produce precocious larvae, but they 1988; Hendrix & Trapp, 1989; Berenbaum, are usually more numerous in female broods, 1991). On hatching, D. pastinacella larvae and are also produced earlier during brood de¬ move to the floral structures, feeding inside velopment in females (Grbic & Strand, 1991; the umbel petiole sheaths and also on more Grbic et ah, 1992). The age of the host-egg in mature flowers and fruits. Larvae typically which the female C. floridanum oviposits has bore into the plant stem before pupation, also been shown to influence the production of emerging several weeks later to overwinter as precocious larvae by the subsequently devel¬ adults (Gorder & Mertins, 1984; I. Hardy, per¬ oping brood (Ode & Strand 1995). sonal observations). In The Netherlands, I In this paper, which forms part of an inves¬ have found D. pastinacella (and C. sosares) tigation into the reproductive biology of the most commonly on Heracleum sphondylium polyembryonie encyrtid Copidosoma s osar es L. but also on H. mantegazzianum Sommier (Walker), I report that precocious larvae are and Levier and Pastinaca sativa L. However, produced and investigate the between-brood I have not found D. pastinacella on Angelica variation in their numbers. sylvestris L. or (in concord with the literature) on other Umbelliferae such as Anthriscus syl¬ vestris (L.) Hoffm. or Aegopodium podagra- Biology of C. sosares and its host ria L., despite year round entomological field Like all known polyembryonie encyrtids, C. work involving these plant species. sosares is an egg-larval parasitoid of . Its life history appears to be qui¬ Methods te similar to that of other polyembryonie en¬ cyrtids (e.g. Cruz, 1986b; and see Godfray Depressaria pastinacella larvae were collec¬ (1994, pp 10-12) for the most recent summa¬ ted from H. sphondylium growing in a patch of ry). Copidosoma sosares females parasitize partially wooded wasteland next to a railway the eggs of Depressaria pastinacella Dupon- line, a canal and near urban dwellings in chel (Lepidoptera: Oecophoridae) in the Leiden, The Netherlands at the end of July spring. The parasitized host eggs hatch into 1995. Heracleum sphondylium plants which larvae which feed and develop until the end of hosted D. pastinacella larvae were obvious their larval stage, whereupon the host body due to the webbed-up and damaged appearan¬ contents become completely consumed by the ce of their umbels and by the holes in their parasitoid brood and the host forms a stiff stems made by larvae entering the hollow ‘mummy’, inside which the parasitoids pupa¬ stem prior to pupation. Some larvae were col¬ te. Adult parasitoids emerge several weeks la¬ lected from the umbels on which they were ter (late August to early September, personal feeding, but most were collected from inside observations). Like its host (Gorder & Mer- the stems by slicing these open longitudinally. tins, 1984), C. sosares appears to be univolti- A total of 171 motile larvae was collected. ne and to overwinter in the adult stage. Brood Twenty mummified D. pastinacella larvae sizes at emergence range from less than 10 to found inside the stems were also collected, but more than 300 individuals, and may contain pupae were not (because they were not parasi¬ only males, only females or both sexes (I. tized by egg-larval parasitoids). Hardy, unpublished data). Mixed sex broods Motile and mummified D. pastinacella lar¬ almost certainly arise from the oviposition of vae were brought back to the laboratory and more than one parasitoid egg into the host. individually dissected under a binocular mi¬ Depressaria pastinacella females oviposit croscope using fine needles. Following decap¬ onto the leaves and flower stalks of various itation the body contents of motile larvae were members of three genera of Umbelliferae: squeezed out into a drop of water. The remains Heracleum, Angelica and Pastinaca (e.g. of the larvae were then ripped open to expose Gorder & Mertins, 1984; Nitao & Berenbaum, remaining tissue. The contents of the larvae 90 Ent. Ber., Amst. 56 (1996)

to their large numbers (fig. 1). Larvae develop to virtually fill the host, by which time host fatty tissue is absent, presumably consumed by the parasitoid brood. When hosts were dis¬ sected, parasitoid larvae could clearly be ob¬ served ingesting particles floating in the water around them. However, larvae were not ob¬ viously associated with any particular host tis¬ sue or part of the host’s anatomy. Hosts which were mummified but not stiff were found to contain parasitoid larvae. Stiff mummified hosts contained parasitoid pupae which are, Figure 1. Well developed reproductive larvae. initially, white. There was an approximately twofold variation in size among the collected were examined for the presence of parasitoid motile hosts. Although parasitoids were found larvae or developing parasitoid tissue. When in both small and large hosts, large D. pasti¬ parasitoid broods or tissue were found, they nacella larvae very frequently contained C. conformed closely to published descriptions sosares. Mummified hosts were large and blo¬ of immature polyembryonie encyrtids. In pre¬ ated in comparison to active larvae. These ob¬ vious collections from the same field site (I. servations suggest that parasitized D. pasti¬ Hardy, unpublished data) almost all parasi¬ nacella may undergo a supemumary larval tized D. pastinacella larvae contained C. instar, as reported for hosts of another Copido¬ sosares (identified by J.S. Noyes, British soma species (Jones et al., 1982). Museum, Natural History, London [where Precocious larvae were found in 27 of the voucher material is lodged]), and no other 30 motile hosts and also in 3 of the 20 mum¬ Copidosoma species were found. Thus all par¬ mies (in these 3 cases the mummified larvae asitoid broods were assumed to be C. sosares. were not stiff and contained reproductive lar¬ In each host, C. sosares broods were scored as vae rather than pupae). Precocious larvae oc¬ present or absent and the number of preco¬ curred singly, with one exception in which six cious larvae in each host counted. Mummified precocious larvae were found in a motile host. hosts were also dissected and any precocious Precocious larvae were approximately 1.7-3.4 larvae found were counted. mm long and were clearly different from re¬ productive larvae (figs 2-3). All precocious larvae had yellow coloured intestines and a Results clear integument. Mandibles could not be Thirty of the 171 motile larvae contained ‘re¬ clearly observed. productive’ parasitoid larvae or developing Precocious larvae were motile but, at least tissue. Developing tissue could be distinguis¬ when the hosts were dissected, did not appear hed from that of the host (such as white fatty to differ greatly in motility from large re¬ tissue) by its slightly brown colour and lobed productive larvae. Precocious larvae were nor¬ appearance. Parasitoid tissue was found in a mally found ‘free’ in the host haemocoel, range of developmental stages. As develop¬ among the reproductive brood and not asso¬ ment advances, the volume of tissue increases ciated with any particular host tissue or part of and the lobes become more defined until they the host’s anatomy. There were no obvious form distinct embryos which then become se¬ differences in morphology or mobility be¬ parate larvae. Reproductive larvae are initially tween precocious larvae found in hosts con¬ transparent, but larger, more developed, larvae taining reproductive brood tissue, small lar¬ take on a light yellow colour. On dissection of vae, large larvae or in mummies. Clearly, the host, larvae are very obvious, not least due precocious larvae do indeed have very ad- Ent. Ber., Amst. 56(1996) 91

Figure 2. Precocious larva. Figure 3. Precocious larva between two reproductive lar¬ vae from the same brood. vanced development as they are already fully to pupate and not in stiff mummies containing formed when the reproductive brood consists C. sosares pupae. of yet undifferentiated tissue. The production of precocious larvae in C. sosares is low in comparison with some other polyembryonie species (e.g. Cruz, 1986b; Discussion Grbic & Strand, 1991). Most broods contain To my knowledge, this is the first record of just one precocious larva, although there is a precocious larvae in C. sosares. There can be small degree of variation (even if recorded ab¬ little doubt that the observed serpentine larvae sences are artifacts) since six precocious lar¬ are indeed precocious ‘asexual’ larvae: the re¬ vae were found in one of the hosts. The impor¬ semblance to published drawings and photo¬ tance of this finding is unclear, but it is graphs of precocious larvae of other polyem¬ possible that multiple precocious larvae arise bryonie encyrtids is striking (e.g. Silvestri, due to superparasitism (multiple females para¬ 1906; Cruz, 1981, 1986b; Grbic et ah, 1992). sitizing one host). However, five of the six In addition, they were never found in hosts precocious larvae found in this host were in which did not contain reproductive larvae or close association with each other and dis¬ developing tissue, making extremely unlikely played none of the aggressive behaviour the possibility that they belong to another spe¬ which might be expected if they were not ge¬ cies. netically identical. Furthermore, the reprodu¬ Precocious larvae are present in most C. so¬ ctive larvae in this particular brood were well sares broods. Although it is unlikely that I did developed, implying that the precocious lar¬ not find intact precocious larvae in a motile vae had coexisted in the host for several host once dissected, it remains possible that weeks. Although in this study I was unable to precocious larvae may have been inadvertent¬ determine the sexual composition of immature ly destroyed during the dissection process. It is broods, it seems unlikely that there is much in¬ thus not possible to determine whether the re¬ ter-sexual variation in precocious larval pro¬ corded absence of precocious larvae from duction in C. sosares, in contrast to some oth¬ three motile but parasitized hosts is a biologi¬ er Copidosoma species (Doutt, 1947; Grbic & cal phenomenon or an experimental artifact. Strand, 1991). Studies on other polyembryonie encyrtids in¬ The role of precocious larvae in C. sosares dicate that precocious larvae die once the re¬ is unknown, although there are several plau¬ productive larvae pupate (e.g. Cruz, 1986b; sible possibilities. Copidosoma sosares Strand, 1989). It is thus not surprising that pre¬ broods are occasionally hyperparasitized by cocious larvae were found only in newly Tyndarichus scaurus (Walker) (Hymenoptera: mummified hosts in which the brood was yet Encyrtidae) and either multi- or hyperparasi- 92 Ent. Ber., Amst. 56 (1996) tized by Dibrachys sp. (Hymenoptera: Ptero Encyrtidae). -Ann. ent. Soc. Am. 79: 121-127. Doutt, R.L., 1947. Polyembryony in Copidosoma koeh¬ malidae) (the latter trophic relationship is not leri Blanchard. - Am. Nat. 81: 435-453. clear, I. Hardy, unpublished data). Further, Godfray, H.C.J., 1992. Strife among siblings. - Nature three unidentified species of Ichneumonidae, 360: 213-214. and possibly one Braconid species, are also Godfray, H.C.J., 1994. Parasitoids: behavioral and evolutionary ecology: 1-473. Princeton University parasitoids of D. pastinacella (I. Hardy, un¬ Press, Princeton. published data, E. Dijkstra, personal commu¬ Gorder, N.K.N. & J.W. Mertins, 1984. Life history of nication). These observations suggest that pre¬ the parsnip webworm, Depressaria pastinacella (Le¬ cocious larvae may defend the reproductive pidoptera: Oecophoridae), in central Iowa. - Ann. ent. brood against interspecific competition. The Soc. Am. 77: 568-573. Grbic, M„ P.J. Ode & M.R. Strand, 1992. Sibling rival¬ prevalence of superparasitism in C. sosares is ry and brood sex ratios in polyembryonie wasps. - unknown, but precocious larvae could also Nature 360: 254-256. function to defend against conspecific com¬ Grbic, M. & M.R. Strand, 1991. Intersexual variation in petitors. A role in influencing the sex ratio of the development of precocious larvae from the parasi- toid . In: Proceedings of the mixed sex broods (Grbic et al., 1992) is also 3rd International Symposium, on Trichogramma and possible as about 12% of C. sosares broods other egg parasitoids, San Antonio (Tx, USA) (E. contain both sexes (I. Hardy, unpublished Wajnberg & S.B. Vinson, eds): 23-21. INRA, Paris. data). Although it currently seems unlikely Hardy, I.C.W., 1994. Sex ratio and mating structure in that precocious larva production differs the parasitoid Hymenoptera. - Oikos 69: 3-20 Hendrix, S.D. & E.J. Trapp, 1989. Floral herbivory in between the sexes, among mixed sex broods Pastinaca sativa: do compensatory responses offset re¬ females tend to predominate on adult emer¬ duction in fitness? - Evolution 43: 891-895. gence (I. Hardy, unpublished data). Future in¬ Ivanova-Kasas, O.M., 1972. Polyembryony in . In: vestigations will examine these possibilities Developmental Systems (SJ. Counce & C.H. Wadington eds): 243-271. Academic Press, New York. further. Jones, D., G. Jones, R.A. van Steenwijk & B.D. Hammock, 1982. Effect of the parasite Copidosoma Acknowledgements truncatellum on the development of its host Tricho- plusia ni. - Ann. ent. Soc. Am. 75: 7-11. I thank Mollie Hardy, John Noyes, K-D Dijkstra, Eddie Nitao, J.K. & M.B. Berenbaum, 1988. Laboratory rear¬ Dijkstra and Paul Ode for discussion and Kees Hofker for ing of the Parsnip webworm, Depressaria pastinacella taking the photographs. I am especially grateful to John (Lepidoptera: Oecophoridae). - Ann. ent. Soc. Am. 81: Noyes for identifying C. sosares. This work was funded 485-487. by a N.E.R.C. (U.K.) post-doctoral fellowship. Noyes, J.S., 1988. Copidosoma truncatellum (Dalman) and C. floridanum (Ashmead) (Hymenoptera, En¬ cyrtidae), two frequently misidentified polyembryonie References parasitoids of (Lepidoptera). - Syst. En¬ tomol. 13: 197-204. Annecke, D.P. & M.J. Mynhardt, 1974. On the identity Ode, P.J. & M.R. Strand, 1995. Progeny and sex alloca¬ of Copidosoma koehleri Blanchard, 1940 (Hymeno¬ tion decisions of the polyembryonie wasp Copi¬ ptera: Encyrtidae). -J. ent. Soc. Sth. Afr. 37: 31-33. dosoma floridanum. - J. Anim. Ecol. 64: 213-224. Berenbaum, M.R., 1991. Patterns of furaocoumarin pro¬ Silvestri, F., 1906. Contribuzioni alia conoscenza biolo- duction and herbivory in a population of wild gica degli Imenotteri parassiti. Biologia del Litomastix parsnip (Pastinaca sativa L.). - Oecologia 49: 236- truncatellus (Dalm.) (2° nota preliminare). - Ann. 244. Regia Sc. Agric. Portici 6: 3-51. Browning, H.W. & E.R. Oatman, 1984. Intra- and inter¬ Strand, M.R., 1989. Development of the polyembryonie specific relationships among some parasites of Tricho- parasitoid Copidosoma floridanum in Trichoplusia ni. plusia ni (Lepidoptera: Noctuidae). - Env. Entomol. - Entomologia exp. appl. 50: 37-46. 13:551-556. Strand, M.R., J.A. Johnson & J.D. Culin, 1990. Intrinsic Cruz, Y.P., 1981. A sterile defender morph in a polyem¬ interspecific competition between the polyembryonie bryonie hymenopterous parasite. - Nature 294: 446-447. parasitoid Copidosoma floridanum and solitary endo- Cruz, Y.P., 1986a. The defender role of the precocious lar¬ parasitoid Microplitis demolitor in Pseudoplusia inclu- vae of Copidosomopsis tanytmemus Caltagirone (En¬ dens. - Entomologia exp. appl. 55: 275-284. cyrtidae, Hymenoptera). -J. exp. Zool. 237: 309-318. Cruz, Y.P., 1986b. Development of the polyembryonie parasite Copidosomopsis tanytmemus (Hymenoptera: Accepted 20.xi.1995.