BioControl 48: 659–669, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

Host suitability of the New World stalkborer considerata for three Old World Cotesia parasitoids

Robert N. WIEDENMANN1,∗,J.W.SMITH,JR.2 and Luis A. RODRIGUEZ-DEL-BOSQUE3 1Center for Economic Entomology, Illinois Natural History Survey, Champaign, IL 61820, USA; 2Department of Entomology, Texas A&M University, College Station, TX 77843, USA; 3Campo Experimental Río Bravo, INIFAP, Rio Bravo, Tamaulipas, Mexico 88900 ∗Author for correspondence; e-mail: [email protected]

Received 23 October 2001; accepted in revised form 15 April 2003

Abstract. Biological control of stalkboring often has been successful when the braconid parasitoids in the genera Cotesia and Apanteles were the natural enemies of choice. Constraints in using these gregarious, koinobiont, endoparasitoids have included host suita- bility, especially as influenced by the host’s immune response. The suitability of a novel host, the New World stalkborer Diatraea considerata (Lepidoptera: Pyralidae), for parasitization by three Old World braconids, Cotesia chilonis, C. flavipes and C. sesamiae (Hymenoptera: Braconidae), was compared to the suitability of another New World novel host, Diatraea saccharalis. D. considerata was less suitable for all three parasitoids than was D. saccharalis. The frequent occurrence of parasitized D. considerata larvae that did not yield parasitoids, or pupate within an appropriate time interval, suggested encapsulation of the parasitoid progeny, which was visible through the host cuticle. Given the suitability results, these three parasitoids would not be appropriate candidates for use against D. considerata. The results also have important implications for the narrow host range expressed by these parasitoids.

Key words: Braconidae, Cotesia chilonis, Cotesia flavipes, Cotesia sesamiae, Diatraea, host range, host suitability, Hymenoptera, Lepidoptera, novel association, parasitoid, Pyralidae

Introduction

Successful biological control of pest using parasitic wasps requires that a host be ecologically and physiologically compatible with a parasitoid. Ecological compatibility ensures that the parasitoid successfully locates the host’s habitat and subsequently encounters a host in the microhabitat. Physiological compatibility ensures that the host attacked will be nutritionally suitable for parasitoid progeny growth and reproduction. With endoparasitic braconids, physiological compatibility further relies on the parasitoid over- coming host defenses, especially the host immune response. Reuniting pests with their indigenous natural enemies, commonly referred to as classical 660 ROBERT N. WIEDENMANN ET AL. biological control or an old association (Hokkanen and Pimentel, 1984), has relied on implied host-parasitoid compatibility formed during historical host- parasitoid interactions. However, novel-host-parasitoid pairings that occur through ecological equivalency or taxonomic relatedness of hosts, require that both ecological and physiological compatibility be tested explicitly (Wiedenmann and Smith, 1997, 1999). Stalkboring Lepidoptera have been the targets of numerous biological control attempts, using both old and novel associations (Bennett, 1965; Smith et al., 1993; Rodriguez-del-Bosque and Smith, 1997; Overholt, 1998). In one novel-association success, the New World pyralid, Diatraea saccharalis F. (sugarcane borer) has been controlled in several locations with the Old World microgastrine braconid, Cotesia flavipes Cameron, which originated from Asia (Alam et al., 1971; Simmonds, 1972; Meagher et al., 1998). This same parasitoid species has been imported into Africa for use against its old-association host, the pyralid Chilo partellus (Swinhoe); the parasitoid has established and subsequently expanded its range from the original colonization sites in eastern Africa (Overholt, 1998). Although C. flavipes successfully parasitizes D. saccharalis (Fuchs et al., 1979; Wiedenmann and Smith, 1995) and Diatraea lineolata (Walker) (Rodriguez-del-Bosque et al., 1990), attempts to use it against other New World pyralid stalkborers, such as Eoreuma loftini (Dyar), Diatraea grandiosella,andD. lineolata have been unsuccessful because of ecological and/or physiological incompatibility (Overholt and Smith, 1990; Rodriguez-del-Bosque et al., 1990; Meagher et al., 1998). Recent studies have attempted to elucidate patterns of physiological suitability among several novel stalkborer-parasitoid pairings of Old World parasitoids and New World stalkborers and the reciprocal pairings. Ecologi- cally equivalent, novel stalkborer-parasitoid pairings include stalkborers in the Old World genera Chilo Zincken and the New World Diatraea Guilding, and parasitoids in the Paleotropical braconid genus Cotesia Cameron and the related Neotropical Apanteles Foerster. Alleyne and Wiedenmann (2001a) showed differences in success among parasitoid species when three Paleo- tropical Cotesia (C. flavipes, C. sesamiae [Cameron], and C. chilonis Matsumura), which are part of the C. flavipes complex, parasitized the Neotropical stalkborer D. grandiosella, whereas all three parasitoids were similarly compatible with Neotropical D. saccharalis. In a parallel study, Ngi-Song et al. (1999) found physiological suitability inconsistent among the three Cotesia species as well as the two parasitoids, Apanteles deplanatus Muesebeck and A. minator Muesebeck, when parasitizing D. grandiosella, D. saccharalis, Chilo partellus and Chilo orichalcociliellus Strand. HOST SUITABILITY OF THE NEW WORLD STALKBORER 661

Diatraea considerata (Heinrich) is a stalkboring pyralid pest that attacks sugarcane (Saccharum officinarum L.) in west central Mexico. Within its indigenous distribution, i.e., the states of Colima, Jalisco and Nayarit (Box, 1951; Rodriguez-del-Bosque and Smith, 1989), D. considerata is commonly attacked by its putative ancestral parasitoid A. deplanatus (Austin and Dangerfield, 1989; Smith and Rodriguez-del-Bosque, 1994). Similarly, A. deplanatus also has been collected from its only other known host, Diatraea magnifactella Dyar, within this host’s indigenous distribution, but not from other Diatraea that are sympatric with D. considerata and D. magnifac- tella (Smith and Rodriguez-del-Bosque, 1994). Both D. considerata and D. magnifactella remain pests of sugarcane production in west central Mexico and are especially troublesome in areas where the indigenous parasitoid, A. deplanatus, does not occur (Smith and Rodriguez-del-Bosque, 1994). The Old World Cotesia spp. that attack lepidopteran stalkborers are considered to be ecologically equivalent to the New World Apanteles spp. that also attack lepidopteran stalkborers (Wiedenmann and Smith, 1997, 1999). Species attacking stalkborers from both parasitoid genera have equivalent life histories and foraging strategies (Smith and Wiedenmann, 1997). Both Apanteles and Cotesia are gregarious, endoparasitic, koinobiont, micro- gastrine braconids whose progeny are challenged by host defenses after oviposition (Wiedenmann and Smith, 1995). The foraging strategy of both parasitoid genera includes utilizing a series of synomone and kairomone cues emitted from infested host plants (Ngi-Song et al., 1996) and host frass (van Leerdam et al., 1985) to locate the host microhabitat. Foraging female parasitoids searching infested plants are initially attracted to the frass deposited at the entrance to the tunnel excavated by the stalkborer larvae, then enter the tunnel and attack the host (van Leerdam et al., 1985). Thus, the Old World Cotesia spp. that attack sympatric gramineous stalk- borers are ecologically very similar to the New World Apanteles spp. that attack Neotropical stalkborers, and are considered excellent candidates for importation as biological control agents against D. considerata. Testing a contrived host-parasitoid union, coupled with our continued quest to discover host suitability patterns for novel host-parasitoid pairings, generated the following research. We report findings on the suitability of D. considerata as a novel host for C. chilonis, C. flavipes,andC. sesamiae, and compare the host suitability to another novel, suitable host, D. saccharalis.

Materials and methods

The experimental parasitoids, Cotesia chilonis, C, flavipes and C. sesamiae were all reared similarly using D. saccharalis as the factitious host 662 ROBERT N. WIEDENMANN ET AL.

(Wiedenmann et al., 1992), with the colony of each parasitoid species main- tained in isolation to prevent contamination. The C. flavipes colony originated as founders reared in D. saccharalis larvae collected from sugarcane in the lower Rio Grande Valley of Texas (van Leerdam et al., 1985), the C. chilonis colony originated as founders reared in Chilo suppressalis collected from rice in Japan, and the C. sesamiae colony originated as founders reared in C. orichalcociliellus collected from maize in Kenya. Pupae of D. considerata were collected from sugarcane fields near Los Mochis, Sinaloa, Mexico, and the emergent were allowed to oviposit on waxed-paper in a local laboratory. Fresh egg masses were subsequently shipped overnight to Entomology Quarantine at Texas A&M University, College Station, Texas. Emergent neonate larvae were placed onto artificial diet (Martinez et al., 1988) for rearing to the experimental host size. Larvae of D. saccharalis came from a laboratory culture maintained at Texas A&M University, using the same artificial diet. When larvae of both stalkborers reached the fourth instar, they were exposed to each parasitoid species, by hand-stinging the larvae to visually confirm host attack and presumed oviposition by the parasitoid (Wiedenmann and Smith, 1995). Hand-stinging has been used effectively in our laboratories in previous studies (e.g., Alleyne and Wiedenmann, 2001a, b) with these three Cotesia species. Three replications of cohorts represented by ten larvae of each host species per parasitoid species were exposed; the replications were blocked at three times over a six-week period. After being parasitized, larvae were returned individually to containers containing artificial diet and their fates were observed periodically. Fates of host larvae exposed to parasitoids were categorized as either (1) successful pupation, (2) emergence of parasitoids, (3) host death, or (4) terminal larvae. Host larvae exposed to parasitoids that did not pupate for 30 days after exposure were considered terminal, as the probability was low that the larvae would eventually pupate successfully. Many larvae categorized as terminal showed signs of encapsulated larvae, as evidenced by darkened, melanized parasitoid larvae visible through the host cuticle, as has been seen in studies with other stalkborer hosts (Wiedenmann and Smith, 1995; Alleyne and Wiedenmann, 2001b). The time from oviposition to emergence of parasitoid progeny, number of parasitoid cocoons formed, and the numbers of emerged adult parasitoids were recorded. Comparisons were made among parasitoid species for each host, and between hosts for each parasitoid species. Data were subjected to analysis of variance (Proc GLM, SAS Institute, 1985) followed by Tukey’s mean separation tests when the ANOVA was significant (P < 0.05). T-tests were made to compare the results between host species for each parasitoid. HOST SUITABILITY OF THE NEW WORLD STALKBORER 663

Results

Host suitability

Diatraea saccharalis was suitable for all three parasitoids (Table 1). The average number of hosts from the three replications of 10 hosts that produced parasitoid progeny (successful parasitization) was 6.33 for C. sesamiae,7.0 for C. chilonis; and 8.0 for C. flavipes. These means for successful parasitiza- tion did not differ among the three parasitoids (F =1.09;df=2,4;P = 0.42). In contrast, the suitability of D. considerata differed markedly (F = 8.14; df = 2, 4; P = 0.04) among the three parasitoids (Table 1). Diatraea considerata was most suitable for C. chilonis development, with an average of 5.33 suitable hosts per 10 hosts exposed; followed by C. sesamiae which averaged 2.33 and C. flavipes, which averaged only 0.33 suitable hosts per 10 hosts exposed. Comparisons between host species exposed to each parasitoid species showed differences among parasitoids. Mean suitability of D. saccharalis and D. considerata did not differ for C. chilonis (t = 1.58; df =4.0;P = 0.19). In contrast, mean suitability of D. considerata was signifi- cantly lower than that of D. saccharalis for C. sesamiae (t = 4.24; df = 4.0; P = 0.01) and C. flavipes (t =6.38;df=4.0;P = 0.003). Hosts that did not yield parasitoid progeny either pupated, died, or remained in a larval stage (terminal larvae) until sacrificed (>30 days after parasitoid oviposition; normal pupation occurred 9–12 days after exposure to parasitoid oviposition). Occurrence of host pupation indicated unsuccessful parasitization. Numbers of hosts that pupated, died or remained as terminal larvae did not differ among parasitoid species for either host species (Table 1). No D. saccharalis yielded terminal larvae. In contrast, the occurrence of terminal D. considerata larvae was great for all three parasitoid species, ranging from 4.00 to 5.33 per 10 hosts (Table 1).

Developmental times

Development of parasitoid cocoons from parasitized D. saccharalis larvae required approximately 12–13 days (Table 2), with C. chilonis taking signifi- cantly less time for development than either C. flavipes or C. sesamiae, which did not differ from each other (F = 16.90; df = 2, 59; P = 0.0001). The range in developmental times from parasitoid egg deposition to cocoon formation was much broader from D. considerata larvae. Cotesia chilonis required 12.7 days, which was significantly shorter than the 15.0 days for development of C. flavipes and 17.0 days for C. sesamiae (F = 122.3; df = 2, 19; P = 0.0001; Table 2). Development time for all three parasitoid species 664 ROBERT N. WIEDENMANN ET AL.

Table 1. Fate of Diatraea saccharalis and D. considerata larvae parasitized by Cotesia chilonis, C. flavipes and C. sesamiae. Reported are means per three replicates of ten larvae (+/− S.E.) that produced parasitoid progeny, pupated, died or remained as terminal larvae

Host Parasitoid Host fate Died Terminal progeny pupation larvae

D. saccharalis C. chilonis 7.00 (0.58)aA 2.00 (0.58)aA 1.00 (0.58)aA 0.00 (0.00)A C. flavipes 8.00 (1.15)aA 1.67 (0.88)aA 0.33 (0.33)aA 0.00 (0.00)A C. sesamiae 6.33 (0.33)aA 2.67 (0.33)aA 0.67 (0.67)aA 0.00 (0.00)A F =1.09 F =0.44 F =2.00 df = 2, 4 df = 2, 4 df = 2, 4 P =0.42 P =0.67 P =0.25

D. considerata C. chilonis 5.33 (1.45)aA 0.00 (0.00)aA 0.67 (0.67)aA 4.00 (1.00)aB C. flavipes 0.33 (0.33)bB 2.67 (1.20)aA 2.00 (0.58)aA 5.00 (0.58)aB C. sesamiae 2.33 (1.45)abB 0.00 (0.00)aB 2.33 (0.33)aA 5.33 (1.45)aB F =8.14 F =4.92 F =2.00 F =0.81 df = 2, 4 df = 2, 4 df = 2, 4 df = 2, 4 P =0.04 P =0.08 P =0.22 P =0.51 Column means for each parasitoid species compared per host species that are followed by a different lower-case letter differ at P = 0.05. Means for each parasitoid species compared between the two host species that are followed by different upper-case letters differ at P = 0.05. was shorter (all P < 0.006; Table 2) when D. saccharalis was the host than when D. considerata was the host.

Brood sizes

Brood sizes varied significantly (F = 14.41; df = 2, 52; P = 0.0001) among parasitoid species when D. saccharalis was the host (Table 3). Cotesia sesamiae produced an average of 57.4 cocoons, followed by C. flavipes (41.5 cocoons) and C. chilonis (28.3 cocoons). Cotesia flavipes and C. sesamiae had similarly larger percentages of adults emerging successfully from cocoons (87.2% and 83.7%, respectively), versus 56.4% of C. chilonis adults that emerged successfully from D. saccharalis. Brood sizes also varied significantly (F = 7.46; df = 2, 19; P = 0.004) among the three parasitoid species when D. considerata was the host (Table 3). Cotesia sesamiae brood size averaged of 53.4 cocoons; C. chilonis 17.8 cocoons and only one host HOST SUITABILITY OF THE NEW WORLD STALKBORER 665

Table 2. Developmental time (days) for immature Cotesia chilonis, C. flavipes and C. sesamiae parasitoid progeny (time to emergence of cocoons) from Diatraea saccharalis and D. considerata

Host species Parasitoid species C. chilonis C. flavipes C. sesamiae

D. saccharalis 11.95 (0.16)aA 12.83 (0.07)bA 12.95 (0.24)bA D. considerata 12.69 (0.19)aB 15.00 (0.00)bB 17.00 (0.00)cB t =2.90 t =6.16 t = 17.20 df = 35 df = 23 df = 18 P = 0.006 P = 0.001 P = 0.0001 Means within a row followed by different lower-case letters are different at P = 0.05. Means within a column followed by different upper-case letters are different at P = 0.05. produced 25 C. flavipes cocoons. A total of 75.5% of Cotesia sesamiae cocoons produced adults, versus 51.2% of C. chilonis, and the one host that yielded C. flavipes progeny had 44.0% of its cocoons that successfully produced adults. Brood sizes of C. chilonis were significantly greater (t = 2.40; df = 35; P = 0.02) in D. saccharalis hosts than in D. considerata hosts (Table 3). Brood sizes for C. flavipes and C. sesamiae did not differ between host species (Table 3).

Discussion

The stalkborer D. considerata was generally a much less suitable host than its congener D. saccharalis for the three novel-association parasitoid pair- ings tested. A greater proportion of D. saccharalis larvae produced parasitoid progeny of C. flavipes and C. sesamiae and the progeny of all three parasitoid species had shorter developmental times. However, exceptions to this general pattern of suitability occurred. Although the life history parameters for C. chilonis generally appeared to be consistently superior to its congeners across both hosts, the smaller brood size of C. chilonis appears to be characteristic of the species (Kajita and Drake, 1969; Wiedenmann and Smith, 1995). Of interest was the large number of terminal D. considerata larvae – hosts that did not produce parasitoid progeny, but also did not pupate – for all three parasitoid species. At the same time, no terminal D. saccharalis larvae were observed. The outcome of terminal larvae has been seen in other host-parasitoid studies among these stalkborers and the microgastrine parasitoids (Overholt and Smith, 1990; Wiedenmann and 666 ROBERT N. WIEDENMANN ET AL. progeny from C. sesamiae =0.79 =0.27 t P and C. flavipes , Cotesia chilonis = 0.05. Means within a column followed by different upper-case P =0.41 =0.86 t P =0.02 =2.40 t C. chilonis n C. flavipes n C. sesamiae n df = 35P df = 16 df = 7 D. considerata = 0.05. P and Brood size (numbers of cocoons) and percent adult emergence for CocoonsAdult emergenceCocoonsAdult 56.4% emergence 28.33 (3.06)aA 51.2% 17.75 21 (3.03)aB 41.53 16 (4.45)bA 87.2% 25.00 17 (0.00)bA 44.0% 57.37 (0.24)cA 1 19 53.42 (14.01)cA 83.7% 7 75.5% -test for cocoons Host speciesD. saccharalis D. considerata t Parasitoid species Table 3. Means within a row followed by differentletters lower-case are letters are different different at at Diatraea saccharalis HOST SUITABILITY OF THE NEW WORLD STALKBORER 667

Smith, 1995). Alleyne and Wiedenmann (2001a, b) found that D. grandi- osella parasitized by C. sesamiae and C. flavipes produced terminal larvae, all of which contained encapsulated parasitoid progeny, whereas terminal larvae (and the associated encapsulated parasitoids) did not occur with D. sacccharalis. These terminal D. considerata showed darkened, melanized parasitoid progeny, visible through the host cuticle; however these encapsu- lated parasitoid progeny were only observed through the host cuticle, and not via dissection of hosts. This study provided additional detail to help clarify the original miscon- ception among biological control practitioners working with stalkborers in sugarcane that the Old World Cotesia flavipes-complex parasitoids could universally and successfully parasitize novel-New World stalkborer hosts. Just as Alleyne and Wiedenmann (2001a, b) showed that D. grandiosella was less suitable for C. sesamiae and C. flavipes, the present study yielded the same results for D. considerata. Cotesia flavipes has been released against D. grandiosella in the High Plains of Texas, with little success (Overholt and Smith, 1990), likely due to the partial physiological incompatibility. Releases of these three Cotesia species against D. considerata in Mexico would likely produce the same failure. Use of novel associations for biological control has been widely criticized as using natural enemies with broad host ranges. The logic is that, if they can be used against a novel host, they must inherently have a broad host range. However, the present study, and other similar studies, does not support the novel-host, broad-host range concept. The congeneric Diatraea hosts were not equally compatible for the novel parasitoids. The differences in suitability seen between D. saccharalis and D. considerata were striking; similar levels of compatibility among parasitoids exposed to D. saccharalis were mirrored by the dissimilar levels of compatibility among parasitoids exposed to D. considerata. These results have important implications for the need to assess potential non-target impacts of novel parasitoids used for biological control. Testing closely related host species may indicate a parasitoid’s potential host range, but the variability among the two congeneric Diatraea hosts exposed to three congeneric Cotesia parasitoids indicated that results from this type of testing cannot be extrapolated and will require further explicit host-parasitoid testing.

Acknowledgements

We thank Patricia Gillogly, of Texas A&M University, for working with D. considerata in quarantine and for rearing the hosts and parasitoids used for these experiments. Marianne Alleyne, Charlie Helm and Jim Nardi provided 668 ROBERT N. WIEDENMANN ET AL. comments on an early draft. The work presented here was supported in part by Hatch project 65-0331 to RNW, and Texas Agricultural Experiment Station funds to JWS.

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