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NOTES ON THE BIOLOGY AND BEHAVIOUR OF THE JEWEL WASP, AMPULEX COMPRESSA (FABRICIUS, 1781) (HYMENOPTERA; AMPULICIDAE), IN THE LABORATORY, INCLUDING FIRST RECORD OF GREGARIOUS REPRODUCTION1
Eduardo Gonalves Paterson Fox,2 Suzete Bressan-Nascimento,3 and Roberto Eizemberg4 ABSTRACT: A colony of the solitary parasitoid ampulicid wasp Ampulex compressa was established under laboratorial conditions. A total of 23 wasps were reared, which attacked about 80 cockroach hosts. Wasps longevity and development mean times recorded were 55.85 26.09 and 43.17 3.58 days, respectively. Of the attacked cockroaches, 60% yielded ordinary solitary brood (sexual ratio approximately 1:1), 23.75 % failed to hatch, and 16.25 % presented one egg over each middle coxa. The two eggs laid on one prey always produced two dwarf male wasps. Laying two eggs on one prey has never been reported before. Not all cockroaches were attacked by the wasps, and some avoided being stung by aggressively reacting against the wasps approaches. We consider these finds to demonstrate the plasticity of the host-handling behaviour of A. compressa, illustrating how synovigenic parasitoids can adapt rapidly to surrounding conditions. KEY WORDS: Periplaneta americana, jewel wasp, Ampulex compressa, Hymenoptera, Ampulicidae, laboratory, parasitoid, brood size, reproductive behaviour, gregarious reproduction, two eggs on one prey, solitary reproduction.

Ampulicidae is a family of cockroach-hunting parasitic wasps of about 200 species (Pulawski, 2003). Ampulex compressa (Fabricius) (Hymenoptera, Ampulicidae), is a metallic blue-green wasp with red femora measuring 2-3cm, also known as jewel wasp or emerald wasp, that actively hunts domestic cockroaches like Periplaneta americana (Linnaeus) (Dictyoptera, Blattidae). Its potential application to biological control of cockroach infestations was proposed by Veltman and Wilhelm (1991) and Lebeck (1991). The egg-laying and nesting behaviour of A. compressa was first described by Williams (1942), further illustrated by Piek et al. (1984) and, more recently, analysed in detail by Keasar et al. (2006). In brief, the adult wasps cause a kind of transient paralysis in cockroaches by stinging, drink out some of their haemolymph after cutting off their antennae, and then drag them to a hole to be used as a nest. Once inside this nest, the wasps typically lay one egg over one of the cockroachs middle coxa, block the nest entrance with surrounding debris, and leave. The cockroach remains unable to leave the nest, although it is able to
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Received on November 13, 2008. Accepted on December 16, 2008. Centro de Estudos de Insetos Sociais / Sao Paulo State University 24A Avenue 1515 - Bela Vista 13506-900 - Rio Claro, Sao Paulo, Brazil. Phone number: 55 19 92880949. Email: ofoxofox@ gmail.com Instituto de Biofisica / Universidade Federal do Rio de Janeiro. Brigadeiro Trompowisk Avenue, Centro de Ciencias da Saude, office 13 - Ilha do Fundao 21941-590 - Rio de Janeiro, Brazil. Phone number 55 21 25626589. Email: sbressan@biof.ufrj.br Instituto de Bioquimica Medica / Universidade Federal do Rio de Janeiro. Brigadeiro Trompowisk Avenue, Centro de Ciencias da Saude, office 31 - Ilha do Fundao 21941-590 - Rio de Janeiro, Brazil. Phone number 55 21 25626786. Email: insecta_tv@yahoo.com.br Mailed on May 13, 2010

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move. No ampulicid wasps were ever observed to lay more than one egg over their host, but they are a little studied insect family. We herein relate basic biological parameters (mean longevity, parasitism rates, and development times under laboratorial conditions), for the first time report laying two eggs on one host by A. compressa, and also describe an interesting defensive behaviour on part of the cockroaches. METHODS An original female wasp freely entered our laboratory attracted by a cockroach colony. We promptly captured it with an insect net and allocated it inside a 90 cm3 box of wooden frame faced with plastic screens, held at 26 2.2C and 69 3% of relative humidity, photoperiod exposition set to 14:10 (L:D). It later accepted reared cockroaches as hosts. It was fed on 20% sucrose solution ad libitum and tap water, and we supplied it with cylindrical glass vials (3 cm diameter x 9.5-cm length) internally lined with paper to be used as artificial nests, and also small crumpled paper fragments as debris for filling up the nest tubes. Therefore, a small wasp population was haphazardly initiated. As the population increased, the wasps were kept inside similar rearing chambers, always 2 or 3 wasps per cage, including at least one male. A stock colony of P. americana was established in the laboratory, as described in Fox and Bressan-Nascimento (2006). From this colony, we were able to obtain adult specimens for presenting to the parasitoid wasps as hosts. Every time a cockroach was stung and placed inside a glass tube by the wasp, we retrieved this tube from the rearing chamber, sealed it with a piece of tulle cloth and rubber bands, and stored it inside a plastic tray until the adults emergence. After adults emerged, they were sexed and distributed into other rearing chambers. The wasps and parasitized cockroaches were checked daily to measure development times and wasp longevity. We recorded the sex of the offspring, and measured body size of the attacked cockroaches and wasps after they were dead. Body measures of the wasps were taken in straight length (top of the head capsule down to the tip of the gaster), and maximum thoracic width. Cockroach carcasses were measured in straight length, to check for size preference of hosts, and compared with the mean size of cockroaches from the colony. As the glass tubes used were transparent, we could easily see from the outside how many eggs were placed on the cockroaches. We herein call solitary brood wasps emerging from individual hosts, and double brood those emerging from the same host at the number of two. Voucher specimens of host carcasses and wasps were deposited in the entomological collection of Museu de Zoologia da Universidade de Sao Paulo (MZUSP), Sao Paulo, Brazil. All obtained data were statistically evaluated using BioEstat software (v. 4.0), by performing t test (assuming homoscedasticity, or equal variance, for each case), using R = 0.05 as level of significance. All mean values are presented as mean standard deviation.

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RESULTS Biological parameters A total of 23 wasps were obtained in the laboratory, which parasitized 80 cockroaches (i.e. placed them in the glass nest-tubes and oviposited over their coxae). General mean longevity of the wasps was 55.85 26.09 days (median: 53 days) under the given conditions, ranging between 25 and 90 days (N=15), and their body sizes and development times are given in Table 1. Development times and longevity of female and male wasps, and of solitary and double brood were not statistically different (p = 0.0105, t= -2.48). From the parasitized cockroaches, 23.75 % failed to yield wasps (carcasses were dried up with no cocoons inside), 16.25 % presented two eggs, one laid on each middle coxa, and 60 % yielded solitary brood 52.17 % of which were female wasps and 47.83 % were males. We observed that not all cockroaches that were attacked were immediately parasitized only about one-third of them. The wasps usually fed from their haemolymph and left them alone for a period of time that could take days. Some of the presented cockroaches were never attacked by the wasps, being left alone indefinitely in the cage. Some cockroaches avoided being attacked by reacting aggressively to approaching wasps: they conspicuously elevated their bodies, while turning around to hide their heads and tried to kick with the hind legs (a typical defensive measure adopted by P. americana in our rearing colonies) (Fig. 1), and also tried to bite the wasps if they got too close (not shown). Gregarious reproduction Among the cases in which two eggs were laid on a single cockroach host, the death of one of the eggs was observed on two occasions: it turned brown and collapsed. On the other occasions, both larvae hatched and also penetrated the cockroach at about the same times on the same days. The double brood was always composed of male wasps, which were notably smaller than solitary wasps (Fig. 2, Table 1). They always emerged on the same day and from separate openings on the cockroaches carcasses (Fig. 3).

Fig. 1. Aggressive reactions adopted by some Periplaneta americana when approached by an Ampulex compressa female. A Body elevation followed by turning of the body. B Kicking with the hind leg; arrow blurred hind leg in mid-air during the kicking attempt.

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Fig. 2. Example specimens of the three morphological varieties of Ampulex compressa, mounted on entomological pins. From left to right: male, female and double-brood male.

Fig. 3. Cockroach carcass after the emergence of two Ampulex compressa males. Exit orifices are indicated with arrows.

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Table 1. Body measures of Ampulex compressa wasps, taken from specimens mounted on insect pins and separated by sex. Specimens measured Solitary females (N = 12) Solitary males (N = 11) Double-brood males (N = 10) Body length (cm) 3.20 0.26a 2.50 0.15b 1.70 0.11c Thorax width (cm) 0.65 0.05a 0.45 0.02b 0.38 0.01c

Note: Means followed by the same letter in same column did not differ by Students t test at 5% (p < 0.0001).

Table 2. Development times of various life stages of Ampulex compressa, as reared under the set laboratory conditions. Life stage Egg development (N=10) Larval development* (N=10) Complete development (N=18) Development time (days) 20 61 41 4

* All larval instars develop externally to the host (Williams, 1942; Fox et al., 2006).

Host body measures The length of host remnant carcasses were measured and separated according to the sex and emergence type (if single or double) of the resulting brood; mean sizes of each case were statistically compared (Table 3). Parasitized cockroaches that originated solitary female wasps were of about the same size as those that originated double brood, and significantly larger than cockroach carcasses that originated male brood or failed to emerge (Table 3). Table 3. Sizes of the carcasses of cockroaches attacked by Ampulex compressa females according with the number of deposited eggs and sex of emerged brood. Carcass precedence 1- One egg no emergence (N=18) 2- One egg female wasp (N=11) 3- One egg male wasp (N=11) 4- Two eggs male wasps (N=12) 5- Colony sample (N=60)* Carcass length (cm) 2.72 0.13a 3.40 0.12b 2.98 0.30c 3.32 0.35b 3.76 1.74e

* 30 male and 30 female cockroaches collected from the colony for size comparison. Note: Means followed by the same letters in same column did not differ by Students t test at 5%; 1 / 2: t= -13.70, p < 0.0001; 1 / 3: t = -2.74, p= 0.09; 1 / 4: t = -5.67, p < 0.0001; 2 / 3: t = 4.35, p = 0.0004; 2 / 4: t = 0.69, p = 0.223; 3 / 4: t = -2.48, p = 0.0108.

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DISCUSSION Our wasps lived less than the wasps reared by Williams (1942), who employed generally similar rearing conditions. The greater longevity was probably a result of lower temperatures. The same author briefly mentioned that some kind of diapause was frequent, thus resulting in greater developing periods. As temperature was favourable, our specimens developed directly and more rapidly. Females of this parasitoid always cut the cockroaches antennae at an approximately fixed length (Keasar et al., 2006) and drink the exuding haemolymph. They are synovigenic, i.e. born with some matured eggs, and host-feeding behaviour is frequent in synovigenic parasitoids (Jervis and Kidd, 1986) that use host protein to continue egg production. Keasar et al. (2006) proposed that the consumption of haemolymph in this species might serve to probe host suitability to oviposition, thus sometimes resulting in refusal. However, we noticed that the rejected cockroaches were usually used, albeit days later, for oviposition. This could be because the female wasp had no eggs to oviposit at the first time or result from a lack of another suitable host. This means that the wasps attack more hosts than they would need for oviposition, what elevates their biological control potential: rejected hosts are handicapped of their antennae and suffer from a long-term hypokinesia caused by the stings (Haspel, 2003; Libersat, 2003). This also means that they need new host continuously in artificial rearing. The defensive behaviour of the cockroaches has never been reported, but Williams (1942) mentioned having observed wasps dying from injuries caused by the cockroaches and Piek et al. (1984) saw that some cockroaches offered considerable resistance to the attacking wasps, which were often unable to grab them on the right spot. We observed similar aggressive behaviour (body elevation followed by side or hind kicks and biting) among the cockroaches inside their rearing chambers. Here we report laying two eggs on a single prey by A. compressa for the first time, which is rather surprising, as the reproductive behaviour of this ampulicid wasp was studied in detail before (Williams, 1942; Piek et al., 1984; Keasar et al., 2006), leading us to wonder if some aspects in our rearing conditions could have affected its behaviour. Among the factors that could have led to the laying of two eggs on one prey would be: a large egg load in the female wasp, low availability of suitable hosts, and even incapacity of discerning between hosts that were previously attacked and those that were not, resulting in some kind of altered superparasitism (Sirot et al., 1997). However, we made sure that cockroaches were always available in the cage and in general our rearing conditions were similar to those used by Williams (1942). In addition, females of A. compressa must be able to detect previously paralysed prey as the eggs are laid over a specific body part. This leaves us with large egg loads or even regional variation as responsible factors for the fact, but we have too little evidence to draw solid conclusions. We feel that finding a way of inducing laying two eggs on one

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prey in these wasps might make this species an interesting model for the study of the adaptive fitness of gregarious reproduction. Female wasps of this species are noticeably bigger than males. Due to this, immature stages of female wasps certainly demand more food to complete development, as many researchers (Spradberry and Sands, 1981; Honek, 1993; Visser, 1994; Ellers et al., 1998) associated larger adult body sizes with increased resource carry-over from the larval stage. In fact, we observed that hosts for female brood were larger cockroaches than for male brood, and that two eggs were only deposited on large hosts. This would suggest that host selection must be based, among other variables, on size, and that this selection would be linked to expected brood sex. This size-based selection of the hosts indicates that the wasp is physiologically aware of the sex of its egg to be laid, even the more considering its intention in selecting large hosts for laying two eggs on the same prey. As host size means amount of available food for the larvae, it is possible that limiting size in laboratory colonies might influence the sex allocation and resulting sex ratio we think this merits direct experimentation. Finally, we hope our observations provide new insights into the host-handling behavior of A. compressa, whose complexity was emphasized by Keasar (2006).

ACKNOWLEDGEMENTS
We would like to thank Daniel Russ Solis for his constructive remarks on the manuscript and also Sandor Cristiano Buys for identifying the parasite wasp species and providing useful tips on rearing the insects. Two anonymous reviewers provided useful recommendations. We are also grateful for the financial support provided by CNPq, FAPERJ and INCT Entomologia Molecular.

LITERATURE CITED
Ellers, J., J. J. M. van Alphen, and J. G. Sevenster. 1998. A field study of size-fitness relationships in the parasitoid Asobara tabida. Journal of Animal Ecology 67: 318-324. Fox, E. G. P. and S. Bressan-Nascimento. 2006. Biological characteristics of Evania appendigaster (L.) (Hymenoptera: Evaniidae) in different densities of Periplaneta americana (L.) oothecae (Blattodea: Blattidae). Biological Control 36: 183-188. Fox, E. G. P., S. C. Buys, J. R. S. Mallet, and S. Bressan-Nascimento. 2006. On the morphology of the juvenile stages of Ampulex compressa (Fabricius, 1781) (Hymenoptera, Ampulicidae). Zootaxa 1279: 43-51. Haspel, G., L. A. Rosenberg, and F. Libersat. 2003. Direct injection of venom by a predatory wasp into cockroach brain. Journal of Neurobiology 56: 287-292. Honek, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66: 483-492. Jervis, M. and N. Kidd. 1986. Host feeding strategies in hymenopteran parasitoids. Biological Reviews 61: 395-434. Jervis, M. and N. Kidd. 1997. Insect Natural Enemies: Practical approaches to their study and evaluation. Chapman and Hall. London, England, U.K. 491 pp. Keasar, T., N. Sheffer, G. Glusman, and F. Libersat. 2006. Host-handling behaviour: an innate

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component of foraging behaviour in the parasitoid wasp Ampulex compressa. Ethology 112: 699706. Libersat, F. 2003. Wasp uses venom cocktail to manipulate the behaviour of its cockroach prey. Journal of Comparative Physiology A 189: 497-508. Lebeck, L. M. 1991. A review of the hymenopterous natural enemies of cockroaches with emphasis on biological control. Entomophaga 36: 335-352. Piek, T., J. H. Visser, and R. L. Veenendall. 1984. Change in behaviour of the cockroach, Periplaneta americana, after being stung by the sphecid wasp Ampulex compressa. Entomologia Experimentalis et Applicata 35: 195-203. Pulawski, W. J. 2003. Catalog of Sphecidae sensu lato (= Apoidea excluding Apidae). Available at: http://research.calacademy.org/research/entomology/Entomology_Resources/Hymenoptera/sphecidae/Genera_and_species_PDF/introduction.htm. Consulted on December 2008. Spradberry, J. P. and D. P. A. Sands. 1981. Larval fat body and its relationship to protein storage and ovarian development in adults of the screw-worm fly Chrysomya bezziana. Entomologia Experimentalis et Applicata 30: 116-122. Sirot, E., H. Ploye, and C. Bernstein. 1997. State dependent superparasitism in a solitary parasitoid: egg load and survival. Behavioural Ecology 8: 226-232. Veltman, J. and W. Wilhelm. 1991. Husbandry and display of the jewel wasp Ampulex compressa and its potential value in destroying cockroaches. International Zoo Yearbook 30: 118-126. Visser, M. E. 1994. The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). Journal of Animal Ecology 63: 963-978. Williams, F. X. 1942. Ampulex compressa (Fabr.), a cockroach-hunting wasp introduced from New Caledonia into Hawaii. Proceedings of the Hawaiian Entomological Society 11: 221-233.