Influence of Oviposition Experience on Multiparasitism by Pimpla disparis Vierick and Itoplectis conquisitor Say (Hymenoptera: Ichneumonidae)

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1 BEHAVIOR Influence of Oviposition Experience on Multiparasitism by Pimpla disparis Vierick and Itoplectis conquisitor Say (Hymenoptera: Ichneumonidae) SUSAN E. MOSER, 1,2 MARIANNE ALLEYNE, 1 ROBERT N. WIEDENMANN, 3,4 AND LAWRENCE M. HANKS 1 Environ. Entomol. 37(5): 1307Ð1312 (2008) ABSTRACT We evaluated the potential for competition between the exotic ichneumonid parasitoid Pimpla disparis Vierick and the native ichneumonid Itoplectis conquisitor Say, in the form of multiparasitism and destructive host feeding, by examining how previous oviposition experience inßuenced host selection. Both species commonly attack the host species, bagworm, Thyridopteryx ephemeraeformis (Haworth) (Lepidoptera: Psychidae), in central Illinois. We used in our study adult female parasitoids that were naõ ve, had previously oviposited into hosts that contained heterospeciþcs, or had oviposited into hosts that initially were unparasitized. Naõ ve parasitoids of both species were disinclined to oviposit into hosts that already were parasitized by heterospeciþc larvae, suggesting that female parasitoids could detect the larvae. However, parasitoids with prior oviposition experience were less selective and oviposited into hosts that already were parasitized and unparasitized hosts. Female P. disparis and I. conquisitor probed parasitized hosts more frequently than unparasitized hosts. Adult female parasitoids of both species rarely directly fed on hosts, but those that did preferred to feed on hosts that already were parasitized. For both parasitoid species, the Þrst larva to colonize a multiparasitized host was the most likely to survive to adulthood. KEY WORDS bagworm, parasitoid, competition, host discrimination, host feeding Parasitoid species that overlap in host range can be brought into direct competition when females of different species oviposit into the same host individuals, termed multiparasitism (Godfray 1994). Multiparasitism can be adaptive when hosts are in short supply (van Alphen and Visser 1990), and acceptance of previously parasitized hosts may vary with the prior oviposition experience of the female (Klomp et al. 1980, van Alphen and Visser 1990, Godfray 1994). When multiparasitism occurs, however, the Þrst parasitoid larva to colonize the host may be most likely to complete development because it attacks younger larva, is better able to compete for resources, or induces physiological defenses of the host that kill younger larva (Strand 1986, Godfray 1994, De Moraes et al. 1999, Pexton and Mayhew 2004). Adult female parasitoids of some species can discriminate between unparasitized hosts and those parasitized by conspeciþcs, but few studies have considered such interactions between 1 Department of Entomology, University of Illinois at Urbana- Champaign, 320 Morrill Hall, 505 South Goodwin Ave., Urbana, IL Corresponding author: Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY ( susanmoser@uky.edu). 3 Center for Ecological Entomology, Illinois Natural History Survey, 1816 S. Oak St., Champaign, IL Current address: Department of Entomology, University of Arkansas, 319 Agriculture Building, Fayetteville, AR parasitoid species (van Alphen and Visser 1990, Godfray 1994). Adult females may assess the suitability of hosts by probing them with the ovipositor (Godfray 1994). Parasitoid species also may compete when adult parasitoids feed destructively on parasitized hosts, killing both the host and the parasitoid larva (Ueno 1997, 1999c). This behavior is most common if the female requires nutrients for ovigenesis or if nutrients enhance her longevity (Jervis and Kidd 1986, Heimpel and Collier 1996, Ueno 1999b, c). Adult female parasitoids often feed destructively on low-quality hosts, including those that have been parasitized. They may kill many immature parasitoids during their lifetime in this manner (Ueno 1997). In this paper, we evaluate the potential for competition for hosts between the polyphagous solitary pupal endoparasitoids Pimpla ( Coccygomimus) disparis Vierick and Itoplectis conquisitor Say (Hymenoptera: Ichneumonidae). P. disparis was introduced into the United States as a biological control agent of gypsy moth during the mid-1970s and early 1980s (Weseloh and Anderson 1982, Schaefer et al. 1989), but I. conquisitor is endemic to North America (Krombein et al. 1979). Both parasitoid species are highly polyphagous, attacking caterpillars of many lepidopterous families, especially species that feed in concealed situations, such as leaf rollers, stem borers, X/08/1307Ð1312$04.00/ Entomological Society of America

2 1308 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 5 and tent caterpillars (Krombein et al. 1979). They are among the most common pupal parasitoids of bagworm, Thyridopteryx ephemeraeformis (Haworth) (Lepidoptera: Psychidae), in the area of our study (eastcentral Illinois; Ellis et al. 2005). We conducted choice tests to test the hypotheses that naõ ve female I. conquisitor and P. disparis are more likely to accept hosts that already are parasitized than more experienced females and that adult females would be more likely to feed destructively on hosts that already are parasitized. Materials and Methods Insect Rearing. We established colonies of P. disparis and I. conquisitor by rearing adult wasps from T. ephemeraeformis pupae collected from arborvitae (Thuja spp.) shrubs in central Illinois during fall 2003 and The two parasitoid species were maintained in separate colonies, with adults held in two Plexiglas sleeve cages (30 by 30 by 30 cm) under ambient laboratory conditions (ßuorescent lighting, 16:8 L:D, air temperature 25 C). Adult were provided 10% sucrose solution on cotton rolls, and cages were misted with distilled water daily. The hosts for our experiments were pupae of Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), a natural host of both parasitoid species (Krombein et al. 1979, Schaupp and Kulman 1992). O. nubilalis larvae and diet were obtained from the USDAÐARS Corn Insects and Crop Genetics Research Unit, Ames, IA. Larvae pupated within folds of corrugated cardboard (10 by 7.5 by 5-cm strips), and adult parasitoids of both species readily parasitized the pupae in the rearing cages. We removed the cardboard strips after 3Ð4 d and put them in Plexiglas sleeve cages. Cages were checked daily for adult parasitoids. Newly emerged adult females were moved to separate Plexiglas sleeve cages with several males and provided cotton soaked with 10% sucrose water, and cages were misted with distilled water daily. Dissections showed that adult females of both species carried at least six mature eggs 7Ð8 d after eclosing (S.E.M., unpublished data). Preliminary studies showed that female parasitoids of both species would accept O. nubilalis pupae as hosts if the pupae were enclosed in a roll of paper ( 4 layers thick; Kimwipes, model EX-L; Kimberly-Clark, Neenah, MI). In our experiments, we presented paper-wrapped pupae (within 24 h of pupation) to parasitoids in new plastic petri dishes (100 by 15 mm; Fisher, Pittsburgh, PA). Characterization of Oviposition and Host-Feeding Behavior. We characterized oviposition and hostfeeding behaviors of both parasitoid species by presenting individual females with unparasitized host pupae and observing them under a stereomicroscope for 5 min each. We conþrmed that parasitoids had oviposited by dissecting 20 hosts per parasitoid species to Þnd the parasitoid egg. In some cases, females inserted their ovipositor into hosts without ovipositing (termed probing ). Choice Tests. We conducted a choice test for each parasitoid species during spring 2005 to determine whether host selection was inßuenced by previous oviposition experience. Our treatments were as follows: naõ ve female (never had encountered a host), female that had oviposited into an unparasitized host, and female that had oviposited into a host that was parasitized by a heterospeciþc larva. Females in the latter two treatments had oviposited one to three times before the experiment. Parasitized hosts were obtained by visually conþrming that females had oviposited (see Results). Hosts were immediately removed after oviposition to prevent host feeding and were placed separately into plastic cups (89 ml). We also placed unparasitized host pupae of similar age in plastic cups on the same dates. The choice test was conducted 2 d after initial parasitization. Parasitized pupae were rolled in fresh paper to eliminate chemical cues that may have been deposited during the initial parasitization, and unparasitized pupae also were rolled in paper. We attached two paper rolls containing host pupae (one parasitized by a heterospeciþc and one unparasitized) with adhesive tape, parallel to one another and 2.5 cm apart, to the bottom of a petri dish (100 by 15 mm; Fisher, Pittsburgh, PA). A female parasitoid (7Ð8 d old, mated) was released in the dish and observed for 30 min or until she had oviposited into both pupae. We recorded the number of ovipositor insertions into each host type, oviposition events (con- Þrmed visually, see Results), and host-feeding events. We removed host pupae from paper rolls, placed each into an individual plastic cup (89 ml), and monitored them daily for emergence of adult parasitoids or hosts. Moistened cotton was placed on the pupae to prevent desiccation. We recorded pupae as dead if neither parasitoid nor adult host eclosed after 28 d. Each choice test was replicated 50 times per parasitoid species. Statistical Analysis. We tested differences between treatment means in numbers of probes per host with a three-way mixed-model analysis of variance (ANOVA) with the Þxed effects of experience (three levels), host type (control or parasitized host), and the random effect of the host type Þrst encountered. A Tukey honestly signiþcant difference (HSD) was performed on signiþcant effects and interaction terms. Data were transformed to natural logs before the analysis. Only females that probed both host types were included in the analysis. We used a 3 3 contingency table and generalized Cochran-Mantel-Haenszel (CMH) stratum-adjusted 2 statistic (Agresti 1996), stratiþed by the host Þrst encountered, to test differences between treatments in the number of oviposition events for each species. Females that did not oviposit into either host type were excluded from the analyses. We conducted likelihood-ratio 2 tests to test differences in host mortality, parasitoid survival, and host feeding between treatments. Statistical software was JMP (SAS Institute 2004). All statistical analyses were tested with a signiþcant level of 0.05.

3 October 2008 MOSER ET AL.: INFLUENCE OF EXPERIENCE ON HOST SELECTION BY PARASITOIDS 1309 Results Characterization of Oviposition and Host-Feeding Behavior. Adult females of both parasitoid species responded in a similar manner to hosts: they climbed onto the roll of paper containing a host pupa, tapped it with their antennae, and inserted the ovipositor through the paper perpendicularly into the host. Female parasitoids probed hosts one to three times before oviposition. Oviposition was characterized by a pumping motion of the third valve of the ovipositor, after which the parasitoid remained still for 8Ð10 s, and the egg was visible as it passed through a membrane in the hypopygium and into the ovipositor. The third valve resumed the pumping motion until the egg was inserted into the host. Oviposition was completed within 20 s. After oviposition, external marking behavior by the parasitoid was not observed for either species. We visually conþrmed oviposition with 100% accuracy for both species through pupal dissection (n 20 per parasitoid species). Parasitoid females fed destructively on hosts by inserting the ovipositor, moving it in a circular motion, withdrawing it, and feeding on exuding hemolymph and tissues at the wound. The process of host feeding varied from 20 min to 1 h, with most of this time ( 70%) spent creating the wound. After oviposition, some adult females fed brießy ( 1 min) on hemolymph that was exuded from the wound. Choice Tests. Adult female I. conquisitor probed parasitized hosts more frequently than unparasitized hosts (F 44.32; df 1,249; P ; Fig. 1a). Naõ ve females tended to probe hosts more frequently ( events) than females with prior oviposition experience with parasitized hosts ( ; F 3.01; df 2,249; P 0.051). The host type Þrst encountered by the adult I. conquisitor did not signiþcantly inßuence the number of probes (F 0.59; df 1,249; P 0.44), and there was no interaction between experience and host type (F 0.45; df 2,249; P 0.64). Female P. disparis probed parasitized hosts more frequently, but this difference was only signiþcant for females that had previous experience with unparasitized hosts (interaction: F 3.29; df 2,251; P ; Fig. 1b). The Þrst host encountered within the dish did not inßuence the subsequent number of probes by female P. disparis (F 3.36; df 1,251; P 0.07). Naõ ve female I. conquisitor and P. disparis frequently oviposited only into hosts that initially were unparasitized, avoiding the parasitized hosts (I. conquisitor CMH ; df 4,120; P ; P. disparis CMH ; df 4,134; P ; Table 1). Female parasitoids with previous experience with parasitized hosts, however, usually oviposited into both hosts (Table 1). The same was true for female P. disparis that had previous experience with unparasitized hosts, but female I. conquisitor in the same treatment usually parasitized either the unparasitized host or both hosts (Table 1). Hosts often died after parasitoids had oviposited, with the result that parasitoid larvae did not complete development (I. conquisitor: 44%, n 183; P. disparis: Fig. 1. Mean number of probes ( SE) into unparasitized and parasitized O. nubilalis hosts by naõ ve and experienced adult female I. conquisitor (a) and P. disparis (b). Experienced females had previously oviposited into an unparasitized or a parasitized host. Means with different letters are signiþcantly different (Tukey HSD test, P 0.05). 35%, n 223). Mortality rates were similar for singly parasitized and multiparasitized hosts (51 and 49%, respectively; 2 0.3; df 1,157; P 0.87). However, adult parasitoids were more likely to eclose from singly parasitized hosts than multiparasitized hosts (61 versus 39%, respectively; ; df 1,247; P ). Adult parasitoids that emerged from multiparasitized hosts were usually of the species that Þrst parasitized the host (78% of cases for P. disparis, ; df 1,39; P ; 67% of cases for I. conquisitor, 2 6.5; df 1,56; P 0.011). Only 8% of adult female I. conquisitor and 3% of adult P. disparis fed destructively on hosts (n 300 hosts for each species). Female parasitoids were more likely to feed on parasitized hosts than unparasitized hosts (96% of cases for I. conquisitor, ; df 1,299; P ; 100% of cases for P. disparis, ; df 1,299; P ). The likelihood that a

4 1310 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 5 Table 1. Percentage of adult female I. conquisitor and P. disparis, with different types of oviposition experience, to select one or more available hosts for oviposition Prior experience of parasitoid Percent of females choosing the host that already was parasitized (N) Percent of females choosing the host that was not parasitized (N) Percent of females choosing both hosts (N) Itoplectis conquisitor Naõ ve 24% (8) 55% (18) 21% (7) Parasitized host 26% (5) 11% (12) 63% (29) Unparasitized 2% (1) 51% (24) 47% (22) host Pimpla disparis Naõ ve 23% (10) 43% (19) 34% (15) Parasitized host 12.5% (6) 12.5% (6) 75% (36) Unparasitized host 12.5% (6) 25% (12) 62.5% (30) Females were presented with two O. nubilalis hosts simultaneously: one that was parasitized by a heterospeciþc larva and one that was unparasitized. female parasitoid of either species would feed destructively on hosts was not inßuenced by her previous oviposition experience (I. conquisitor: 2 4.6; df 2,299; P 0.10; P. disparis: 2 3.2; df 2,299; P 0.20). Discussion In our study, experienced females of both parasitoid species were usually less selective than naõ ve females, contrary to the Þndings of earlier researchers (van Lenteren and Bakker 1975, van Lenteren 1976, Klomp et al. 1980, Chow and Mackauer 1986, van Alphen et al. 1987). It seems possible that the 1-d period between the Þrst oviposition experience and the second opportunity to oviposit may have encouraged females to be less selective because it signaled that hosts were scarce (Bakker et al. 1985). The probability that females of both species would multiparasitize hosts also was inßuenced by the quality of hosts that they had encountered previously (i.e., whether they were parasitized versus unparasitized). Similarly, female Anaphes victus Huber (Hymenoptera, Mymaridae) were more likely to superparasitize hosts if they had previously been exposed to hosts that already were parasitized than when exposed to unparasitized hosts (van Baaren et al. 2005). In contrast, oviposition by Leptopilina heterotoma (Hymenoptera: Eucoilidae) is dependent on the number of prior oviposition events rather than the quality of hosts that were encountered previously (Henneman et al. 1994). Naõ ve I. conquisitor and P. disparis probed and fed more frequently on parasitized hosts rather than on unparasitized hosts. In addition, females of both species selected unparasitized hosts most frequently for oviposition. This Þnding suggests that adult female endoparasitoids can determine that hosts are parasitized by another parasitoid species. Ours is one of few studies that have reported interspeciþc host discrimination among species of endoparasitoids that are not closely related (see Wylie 1970, Baur and Yeargan 1995, Wang and Messing 2003, Tamò et al. 2006, Tian et al. 2008), although it may be more common among closely related species (Vet et al. 1984, McBrien and Mackauer 1990, van Baaren et al. 1994, Pijls et al. 1995, Agboka et al. 2002). To our knowledge, ours is the Þrst report of host discrimination between new and old world parasitoid species. Turlings et al. (1985) and Bakker et al. (1985) suggested that interspeciþc host discrimination is uncommon because it is not an evolutionary stable strategy for parasitoids that are not egg limited; however, their model included a limited number of outcomes (survival or death) and did not include additional consequences of multiparasitism, such as changes in larval development time (McBrien and Mackauer 1990, Utsunomiya and Iwabuchi 2002), changes in host physiology (Zaviezo and Mills 2001), or giving up time in unsuitable host patches (Turlings et al. 1985). Female parasitoids of both species undoubtedly improved their Þtness by avoiding multiparasitism because it usually resulted in death of their larvae. This was particularly true for I. conquisitor because the larvae were less likely to survive when hosts were multiparasitized. Some adult female P. disparis and I. conquisitor oviposited into hosts even though they apparently could detect that the host already was parasitized. Nevertheless, females may beneþt from multiparasitizing hosts when hosts are in short supply, because some of their offspring will complete development (Bakker et al. 1985). Female I. conquisitor assess host suitability based on the amino acid and inorganic ion composition of the hemolymph (Arthur et al. 1969, 1972, Hegdekar and Arthur 1973). Females of a congener of P. disparis, Pimpla nipponica Uchida, also use internal host cues to assess suitability and can distinguish between hosts that have been parasitized by conspeciþcs and unparasitized hosts (Ueno 1999c). Female parasitoids of different species may discriminate between parasitized and unparasitized hosts by detecting internal or external chemical markers deposited by the other species (van Alphen and Visser 1990) or because of physiological changes of the host (van Strien-Liempt and van Alphen 1981). Our results suggest that female I. conquisitor and P. disparis use internal cues to detect host suitability, and the increase number of probes into parasitized hosts was likely caused by the female assessing host suitability (Godfray 1994). Host discrimination may be innate or learned (van Alphen and

5 October 2008 MOSER ET AL.: INFLUENCE OF EXPERIENCE ON HOST SELECTION BY PARASITOIDS 1311 Visser 1990), and we found evidence for both modes in our study; naõ ve wasps distinguished between parasitized and unparasitized hosts and recognized hosts after fewer probes when experienced with that host type. An earlier study showed that adult female I. conquisitor feed destructively on hosts that are unsuitable for oviposition (Leius 1961), which is consistent with their preference for parasitized hosts in our study. Ours is the Þrst study to document this behavior in P. disparis, to our knowledge. Females of a congener of I. conquisitor, Itoplectis naranyae Ashmead, also prefer to feed on hosts that are parasitized by conspeciþcs (Ueno 1998). Host feeding may provide nutrients that enhance longevity and fecundity in these synovigenic parasitoids (Leius 1961, Jervis and Kidd 1986, Heimpel and Collier 1996). 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