Journal of Insect Behavior, Vol. 12, No. 5, 1999 Analyses of Two Parasitoids with Convergent Foraging Strategies Consuelo M. De Moraes1,3 and W. J. Lewis2 Accepted March 16, 1999; revised April 6, 1999 We compared the foraging strategies of two key braconid endoparasitoids of the tobacco budworm (Heliothis virescens Fab.), Cardiochiles nigriceps Vier. and Microplitis croceipes Cresson, that differ in host and habitat range but otherwise share comparable, overlapping niches. The most important host-location cues by far for both species were materials associated with damaged plants. Both species demonstrated a significant preference for volatiles released from plants damaged by H. virescens larvae over those released from undamaged tobacco and cotton plants. In choice experiments with damaged tobacco versus cotton, M. croceipes showed a significant preference for cotton plants. In contrast, C. nigriceps preferred damaged tobacco plants. Plant compounds provoked a strong response even when released from systemically induced plants (from which damaged leaves, host, and host by-products were removed). C. nigriceps appears to have a much keener ability to locate hosts over long distances than M. croceipes. This observation may be related to the highly specialized nature of this parasitoid. The possible adaptive significance of the foraging behaviors of these two parasitoids is discussed. KEY WORDS: foraging strategies; host location; larval parasitoids; Microplitis croceipes; Cardiochiles nigriceps; Heliothis virescens. INTRODUCTION Parasitoid proficiency in locating and attacking hosts is a major factor influenc- ing how a particular parasitoid population performs (Godfray, 1994). In recent 1 Department of Entomology, University of Georgia, Coastal Plain Experiment Station, Tifton, Geor- gia 31793. 2USDA-ARS, IBPMRL, Tifton, Georgia. 3 To whom correspondence should be addressed at CMAVE-USDA/ARS, P.O. Box 14565, Gainesville, Florida 32604. Fax: (352) 374-5707. e-mail: [email protected] 571 0892-7553/99/0900-0571$16.00/0 © 1999 Plenum Publishing Corporation 572 De Moraes and Lewis years, enormous advances have been made toward understanding the environ- mental cues used by parasitoids to locate hosts (Vinson, 1976, 1981; Waage, 1978; Nordlund et al., 1988; Lewis et al., 1990; Vet and Dicke, 1992; Tum- linson et al., 1993). The variety and subtlety of such cues attest to the inten- sity of selective pressures favoring efficient host-location strategies. Although parasitoids employ several sensory modalities, often in combination, to locate hosts (Wackers and Lewis, 1994), chemoreception appears to be by far the most important for the exploitation of environmental cues (Turlings et al., 1993). Godfray (1994) recognized three broad categories of environmental cues used by parasitoids to locate hosts: (1) stimuli arising from the host itself, (2) stimuli arising from the host's microhabitat or food plant, and (3) stimuli indi- rectly associated with the presence of the host. Herbivores rarely provide direct cues that reveal their presence over long distances, although some parasitoids exploit host sex or aggregation pheromones (e.g., Sternlicht, 1973) or sounds produced by the host (e.g., Cade, 1975). Thus, for long-range detection of hosts, parasitoids most often depend on indirect cues associated with the presence or activity of the host (Vet and Dicke, 1992; Vet et al., 1995). Herbivore-infested plants are important sources of volatile compounds used as indirect host-location cues by insect parasitoids (Turlings 1991; Geervliet et al., 1996; De Moraes et al., 1998). These plant volatiles are released not only from the site of herbivore damage, but also systemically from undamaged tissues (Turlings and Tumlinson, 1992; Rose et al., 1997). Many studies have demonstrated the importance of host plants for parasitoid foraging. Picard and Raubad (1914) showed that unrelated hosts feeding on the same plant frequently share the same parasitoids. Further- more, the intensity of parasitism suffered by polyphagous herbivores is often correlated with the food plants they attack (Vinson, 1981, 1985; Nordlund et al., 1988). In addition, the importance of plant odors as parasitoid host-location cues has been documented in laboratory behavioral studies using olfactometers and wind tunnel experiments (Elzen et al., 1983, 1984, 1986, 1987; Vet, 1983; Drost et al., 1986). Differences in parasitoid foraging strategies, including the efficient exploitation of environmental cues, are important components of variation in parasitoid performance. In the past, comparative examination of phylogeneti- cally related species that differ in some ecological characteristics has been employed successfully to interpret functional differences in parasitoid forag- ing behavior (Poolman Simons et al., 1992; Vet and Dicke, 1992; Vet et al., 1993; Wiskerke and Vet, 1994). In this paper, we compare the foraging strate- gies of Cardiochiles nigriceps and Microplitis croceipes, two key braconid endoparasitoids of the tobacco budworm (Heliothis virescens), that differ in host and habitat range but have otherwise comparable, overlapping niches. Both of these wasps attack the larval stages of their hosts. H. virescens is a solitary, polyphagous feeder that attacks many crops and weeds. M. croceipes is host-spe- Two Parasitoids with Convergent Foraging Strategies 573 cific within the Heliothis/Helicoverpa complex (Stadelbacher et al., 1984; King et al., 1985), while C. nigriceps is a highly specialized parasitoid that utilizes Heliothis virescens almost exclusively (Chamberlin and Tenhet, 1926; Vinson, 1980). Competition studies (De Moraes et al., 1999) involving these parasitoids have shown that the less specialized of the two, M. croceipes, has a shorter devel- opmental time and dominates intrinsic competition except when its oviposition follows that of the more specialized C. nigriceps by more than 16 h. However, females of C. nigriceps possess superior host-searching efficiency that may more than compensate for disadvantages in intrinsic competition (De Moraes et al., 1999). C. nigriceps is more proficient at detecting host infestations via airborne odors and at locating and attacking early-instar larvae. The study reported here was designed to explore how differences in for- aging strategies, host-location cues, and/or intrinsic sensory preferences and abilities may account for these differences in host-location efficiency. Improved understanding of the nature and adaptive significance of the behaviors underly- ing parasitoid foraging strategies, and the relative importance of different envi- ronmental cues, provides insights into the ecology of host location and other tritrophic interactions. Such knowledge also enhances our ability to predict and manage parasitoid performance and thus facilitates our ability to employ these parasitoids as agents of classic and conservation biological control. MATERIALS AND METHODS Hosts Larvae of H. virescens were obtained from USDA-ARS Gainesville, Florida. Larvae of H. zea were obtained from the Insect Biology and Popula- tion Management Research Laboratory (IBPMRL), USDA-ARS, Tifton, Geor- gia. Larvae were fed a laboratory-prepared pinto bean diet (Perkins et al., 1973) and held in a climatic-controlled room at 25°C, 14:10 LD, and 70% RH until used for experiments. Parasitoids M. croceipes and C. nigriceps were reared on H. virescens larvae accord- ing to the procedure of Lewis and Burton (1970). Both species were held at 25°C, 14:10 LD, and 70% RH. All experiments were conducted with mated M. croceipes and C. nigriceps females, 2 and 5 days old, respectively. Plants Tobacco plants (Nicotiana tabacum, K 326 variety) and cotton plants (Gossypium hirsutum, strain DPL 90) were grown in a greenhouse at 25-30°C, 574 De Moraes and Lewis 15:9 LD, and 60 ± 20% RH from seeds planted in a 1:1 mixture of peatmoss (Promix Bx) and potting soil fertilized with Osmocote. Seven- to nine-week-old plants were used in the experiments. Experimental Procedures Two experimental arenas were used: the field and a wind tunnel. Field experi- ments (cotton and tobacco) were used to determine C. nigriceps (field population) foraging preferences, as this approach provides the most realistic conditions for conducting parasitoid choice experiments. Unfortunately, the same approach could not be used for such tests with M. croceipes because this once-common parasitoid has been found only rarely in Georgia fields for the last few years. Experiments involving this parasitoid were instead carried out in a wind tunnel. Field Experiments with C. nigriceps Two plants of each treatment were placed in a cotton (Bellflower farm, Tifton GA) or tobacco field (Coastal Plain Experiment Station, Tifton, GA) with an active population of C. nigriceps. The plants were arranged 80 cm apart in a two-by-two design with the two treatments placed in alternate positions. Female parasitoids landing on plants in a period of 1 h were visually observed and counted. Each bioassay was conducted on 4 days to account for day-to-day variation. For assays involving systemically induced plants (Rose et al., 1995) damaged leaves were removed and the cut areas covered with aluminum foil. Wind Tunnel Experiments Experiments were conducted in a 50 x 50 x 120-cm wind tunnel (Drost et al., 1986) at a wind speed of 45 ± 2 cm/s (M. croceipes) or 60 ± 2 cm/s (C. nigriceps) at 25 ± 2°C and 40 ± 10% RH. Two plant terminals were placed at the upwind end. At the beginning of each test, a female,