Analyses of Two Parasitoids with Convergent Foraging Strategies

Journal of Insect Behavior, Vol. 12, No. 5, 1999

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]

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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 environmental 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 intensity 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 phylogenetically related species that differ in some ecological characteristics has been employed successfully to interpret functional differences in parasitoid foraging 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 strategies 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 foraging 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 environmental 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 experiments (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, was released from a shell vial at the downwind end. The vial was positioned with its opening toward the center of the two volatile plumes generated by the plant terminals. The plant on which the female first landed was recorded. Females were given a maximum of three chances to land on a plant. Landings anywhere else in the wind tunnel constituted an incomplete flight. For each combination tested, 10 females were bioassayed per day on 4 days. Plants were switched after five complete flights.

Plant Preparation Third-instar caterpillars were caged on the lower leaves (two caterpillars/ leaf) of 8-week-old, potted, greenhouse-grown tobacco (Nicotiana tabacum, strain K326) or cotton (Gossypium hirsutum, strain DPL 90) plants for 48 h prior to placement in the field or wind tunnel. For assays measuring effects of systemi- Two Parasitoids with Convergent Foraging Strategies 575 cally induced plants the damaged leaves, caterpillars, and host by-products were removed prior to the experiments and the cut areas covered with aluminum foil.

Bioassays Host Plant (Plant Species Preference) H. virescens occurs commonly in both cotton and tobacco fields (Manley et al., 1991). To determine whether host-plant identity influences foraging behavior in the two parasitoid species, the following choice experiments were conducted. C. nigriceps (Cotton and Tobacco Field Tests). (1) Damaged versus undamaged cotton; (2) damaged versus undamaged tobacco; (3) damaged cotton versus damaged tobacco. M. croceipes (Wind Tunnel Tests). (1) Damaged versus undamaged cotton; (2) damaged versus undamaged tobacco; (3) damaged cotton versus damaged tobacco. Parasitoids were given prior oviposition experience with larvae that had been fed on diet, cotton, or tobacco.

Host Plant (Indirect Cues) Similar choice experiments were conducted to determine the importance of herbivore-induced plant compounds (i.e., volatiles emitted only as a delayed response to herbivore feeding damage). Systemically induced plants, from which all damaged leaves and caterpillars were removed, were employed. C. nigriceps (Cotton Field). (1) H. virescens-induced cotton versus undamaged cotton; (2) H. zea-mduced cotton versus undamaged cotton; (3) H. virescens-induced cotton versus H. zea-induced cotton. M. croceipes (Wind Tunnel). (1) H. virescens-induced cotton versus undamaged cotton; (2) H. zea-induced cotton versus undamaged cotton; (3) H. virescens-induced cotton versus H. zea-induced cotton.

Data Analysis Results of all dual-choice tests were analyzed using paired t tests [GLM procedure (SAS Institute, 1988)].

RESULTS Host Plant (Plant Species Preference) C. nigriceps Females demonstrated a significant preference for damaged over undamaged cotton and tobacco plants in the field. Presented with a choice between damaged tobacco and cotton plants, C. nigriceps preferred damaged tobacco 576 De Moraes and Lewis

Fig. 1. Field-observed flight response of C. nigriceps females to tobacco or cotton plants infested by H. virescens. Bars indicate the percentage of visits to tobacco (N = 340) or cotton plants (N = 198). Asterisks indicate a significant difference within the choice test (paired / test, **P < 0.05). The experiment was conducted in both cotton and tobacco fields with active populations of C. nigriceps. placed in both cotton (272 of 340 visits over four trials) (M = -51.5, t = -4.1, P < 0.02) and tobacco (158 of 198 visits over four trials) (M = -25.5, t = -3.6, P<0.03) fields (Fig. 1).

M. croceipes Like C. nigriceps, M. croceipes demonstrated a significant preference for damaged over undamaged cotton and tobacco plants. However, presented with a choice between damaged tobacco and damaged cotton plants, they preferred cotton. Seventy-two percent (43 of 60 choices) of wasps given oviposition experience with larvae fed on diet preferred cotton (M = 6.3, t = 7.2, P < 0.01). This preference persisted (40 of 60 choices) when female parasitoids were given experience with host larvae fed on cotton (M = 3.3, t = 5, P < 0.03). In contrast, when female wasps were given oviposition experience with larvae fed on tobacco, their preference for damaged cotton plants increased (44 of 60 choices) (M = 9.3, t = 7.8, P < 0.01) (Fig. 2). Two Parasitoids with Convergent Foraging Strategies 577

Fig. 2. Flight response of M. croceipes females in wind tunnel choice experiments. Bars indicate the percentage of complete flights to tobacco or cotton plants infested by H. virescens (N = 60 each treatment). Asterisks indicate a significant difference within the choice test (paired t test, **P < 0.05). Before the release in the wind tunnel females were given oviposition experience with larvae that had different feeding treatments.

Host Plant (Indirect Cues) C. nigriceps In choice bioassays conducted in a cotton field, females demonstrated a significant preference for H. virescens-induced cotton plants over undamaged plants but showed no clear preference for H. zea-induced plants (C. nigriceps females vis- ited the combination of H. zea and undamaged plants only eight times). When the wasps were presented with a choice between cotton plants systemically induced by either H. virescens or H. zea, C. nigriceps exhibited a preference for plants induced by H. virescens (49 of 70 visits over three trials) (Fig. 3).

M. croceipes In wind tunnel choice experiments, M. croceipes demonstrated a strong preference for cotton plants systemically induced by either herbivore over undamaged plants [H. zea M = 7.75, P < 0.05 (44 of 60 choices); H. virescens M - 8.75, P < 0.05 (48 of 60 choices)]. When M. croceipes females were presented 578 De Moraes and Lewis

Fig. 3. Field-flight response of C. nigriceps females to systemically induced and undamaged cotton plants. Bars indicate the percentage of visits to tobacco or cotton plants. The experiment was conducted in both cotton and tobacco fields with active populations of C. nigriceps. Asterisks indicate a significant difference within the choice test (paired t test, **P < 0.05). Undamaged plants—plants never exposed to caterpillar damage. Systemically induced plants—plants damaged on three lower leaves (by either H. virescens or H. zea larvae) 48 h prior to the test. The undamaged top part of the plant was used in the test. Asterisks indicate a significant difference within the choice test (N - 70; paired t test, **P < 0.05). with a choice between plants systemically induced by either H. virescens or H. zea, a higher number of flights was observed to H. virescens-induced plants over H. zea-induced plants, although no significant difference was found (36 of 60 flights choices over three trials) (M = 3.5, t = -4.04, P < 0.1) (Fig. 4).

DISCUSSION In choice experiments, both parasitoids demonstrated a significant plant- species preference. C. nigriceps preferred damaged tobacco over damaged cotton plants, while M. croceipes exhibited a significant preference for damaged cotton. Furthermore, M. croceipes' preference for damaged cotton intensified when females were given oviposition experience with H. virescens larvae fed on tobacco, indicating an aversion to tobacco. In contrast, C. nigriceps preference for damaged tobacco over damaged cotton plants persisted in both tobacco and cotton fields. Although damaged tobacco was preferred, it is important to note that C. nigriceps was also highly attracted to damaged cotton plants (in this case no aversion was observed). Two Parasitoids with Convergent Foraging Strategies 579

Fig. 4. Flight response of M. croceipes females to systemically induced and undamaged cotton leaves in wind tunnel choice experiments. Bars indicate the percentage of complete flights for each odor source (N = 60 each treatment). Asterisks indicate a significant difference within the choice test (paired t test, **P < 0.05). Undamaged plants—plants never exposed to caterpillar damage. Sys- temically induced plants—plants damaged on three lower leaves (by either H. virescens or H. zea larvae) 48 h prior to the test. The undamaged top part of the plant was used in the test.

Tobacco is a favored host plant for H. virescens and is rich in toxic allelochemicals. These compounds provide H. virescens a degree of protection from natural enemies through direct toxic effects as well as indirect effects involving alteration of the nutritional quality of the caterpillar (Vinson and Barbosa, 1987). These factors may influence the interactions among M. croceipes, H. virescens, and tobacco. Cardiochiles nigriceps' inherent preference for tobacco was maintained even when C. nigriceps females had previous positive experience with cotton (i.e., when tobacco plants were placed in the cotton field). The ability to locate and successfully develop on H. virescens larvae in tobacco fields may give C. nigriceps a competitive advantage by lessening competition with other herbivore natural enemies. Manley et al. (1991), in a survey conducted in South Carolina between 1986 and 1989 reported that C. nigriceps represented 96% of parasitized H. virescens larvae on tobacco (no M. croceipes were col- lected). On cotton 66% of the larvae were parasitized by C. nigriceps and 6% by M. croceipes. The predominant foraging cues used by both M. croceipes and C. nigriceps were herbivore-induced signals emitted by damaged plants. In choice experiments the odor of damaged plants of the less preferred species (cotton for 580 De Moraes and Lewis

C. nigriceps and tobacco for M. croceipes) was more attractive than that of undamaged plants of the preferred species. These results imply that such cues play a significant role in the foraging sequence of these parasitoids, allowing them quickly to exclude unprofitable habitat areas even in the midst of a preferred plant species. Herbivore-induced cues are reliably linked to the presence of hosts, especially in the case of herbivore-specific signals, which have been shown to exist in the case of H. virescens feeding on cotton and tobacco (De Moraes et al., 1998). Of these two parasitoid species, C. nigriceps appears to have a keener ability to detect individual hosts, an observation which may be related to the highly specialized nature of this parasitoid. C. nigriceps exhibits a superior host-location proficiency involving both long-range (volatile) and short-range (contact) cues and an ability to exploit early-instar hosts that are unavailable to M. croceipes (De Moraes et al., 1999). Field studies by Tillman (1996) showed that C. nigriceps parasitized more hosts at both low and high host densities than did M. croceipes', on this basis, she concluded that C. nigriceps should outper- form M. croceipes in a cotton field. Furthermore, C. nigriceps is able to distinguish between host and nonhost infestations on phylogenetically distant plant species (tobacco and cotton) by exploiting herbivore-specific volatile emissions (De Moraes et al., 1998). Although a specialist, M. croceipes apparently has only a poor ability to distinguish host infestations from nonhost before alighting on a plant, and decisive host recognition may require nonvolatile chemicals in the frass (Drost et al., 1988; McCall et al., 1993; Cortesero et al., 1997). At short range, the arrestant response of C. nigriceps is triggered by mandibular and labial gland secretions of H. virescens (Vinson and Lewis, 1965; Vinson, 1968; Vinson et al., 1975). In the case of M. croceipes, frass is a major source of attraction (Lewis and Tumlinson, 1988; Lewis et al., 1991). This attraction is mediated both by nonvolatile contact chemical and by volatile chemical cues (Lewis et al., 1991). The antennation stimulant, 13-methylhentriacontane, a chemical in the host frass, is an important source of attraction for M. croceipes and has been shown to facilitate associative learning (Lewis and Jones, 1971; Lewis and Tumlinson, 1988). This difference may account for the ability of C. nigriceps to attack young larvae, since silk is produced by very young instars, whereas frass accumulation to detectable levels may take some time.

CONCLUSION M. croceipes and C. nigriceps are solitary larval endoparasitoids that employ similar strategies to locate their hosts. Both have restricted host ranges; C. nigriceps generally utilizes only H. virescens, while M. croceipes parasitizes both H. virescens and H. zea. For each plant-herbivore complex, volatile signals used by foraging parasitoids can originate from the plant, the host, or an Two Parasitoids with Convergent Foraging Strategies 581 interaction between the two (Turlings et al., 1990; Loughrin et al., 1994). In our study system, the strongest response of both parasitoids was to induce compounds produced by the plant, even when systemically induced plants were used (from which all damaged tissue, host, and host by-products were removed). The dominance of herbivore-induced signals implies that these indirect, plant-based cues represent an important means of quickly differentiating between profitable and unprofitable sites. Larvae of H. virescens feed on a wide variety of plants and plant parts of various ages, often in diverse vegetational settings, along with many other actively feeding herbivorous insects. Consequently, their trail odors vary considerably and occur in the context of a vast array of unrelated chemical compounds. Linkage of chemical cues associated with the site to a dependable host recognition cue, independent of host contact, provides the parasitoid with a valuable alternative means for ongoing reinforcement or adjustment of its foraging behavior. In the case of C. nigriceps, specialization limits the range of host resources, but the efficient use of herbivore-induced plant signals along with exploitation of multiple habitats enables this species to compete effectively.

ACKNOWLEDGMENTS We thank M. C. Mescher, J. W. Ruberson, R. W. Matthews, and P. Barbosa for comments on the manuscript. We are grateful to Thoris Green for rearing the parasitoids. Financial support was provided in part by a CAPES grant from the Brazilian Minister of Education to C. M. De Moraes.

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