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Prey Preference by the StinkbugPerillus bioculatus,a Predator of the Colorado Potato Beetle
BIOLOGICAL CONTROL ARTICLE NO.
7, 251–258 (1996)
0091
Prey Preference by the Stinkbug Perillus bioculatus, a Predator of the Colorado Potato Beetle JEAN-FRANC¸OIS SAINT-CYR
AND
CONRAD CLOUTIER1
Centre de Recherche en Horticulture, De´partement de Biologie, Universite´ Laval, Cite´ Universitaire, Que´bec, Canada G1K 7P4 Received January 26, 1996; accepted May 31, 1996
INTRODUCTION Perillus bioculatus (F.) is sometimes considered a generalist but has most often been recorded as predator of Colorado potato beetle (CPB),Leptinotarsa decemlineata. (Say). This study was designed to analyze prey selection in P. bioculatus with respect to factors that may lead to specialization. To establish if parental prey determines preference in naı¨ve progeny, prey selection experiments were conducted with the CPB and two unusual prey, the yellow mealworm Tenebrio molitor (L.) and the house cricket Acheta domesticus (L.). Naı¨ve nymphs reared from yellow mealworm-fed parents in the absence of contact with the CPB initiated feeding more frequently on CPB (81.4%) than on cricket prey (69.6%) (P 5 0.038), suggesting genetically inheritable preference for CPB. Progeny from CPBfed parents initiated feeding more frequently on CPB prey (93.3%) than on yellow mealworm prey (76.6%) (P 5 0.0001), but progeny from yellow mealwormfed parents initiated feeding on yellow mealworm prey as frequently (89.2%) as on CPB (95.0%) (P 5 0.613). Similarly, progeny from CPB-fed parents established proboscis contact more frequently on CPB (39.2%) than on house cricket prey (25.0%) (P 5 0.008), whereas those from cricket-fed parents probed house cricket prey as frequently (12.5%) as CPB prey (15.4%) (P 5 0.416). Results confirm specialization of P. bioculatus toward CPB or related prey and suggest genetically inheritable as well as maternally reinforcible affinity toward CPB prey. However, affinity of naı¨ve nymphs for the CPB can be lowered by rearing parents on alternative prey, increasing their chances of survival when alternative prey must be relied upon. r 1996 Academic Press, Inc.
KEY WORDS: Perillus bioculatus; Leptinotarsa decemlineata; Acheta domestica; Tenebrio molitor; prey selection; maternal induction.
1 To whom correspondence should be addressed. Fax: 418-6562043. E-mail [email protected].
Generalist arthropod predators feed on various prey species from different families or even orders, among which they show no clear preference. The opposite is true for specialists, which feed mainly on one type of prey or a few closely related species (Hsiao, 1985). Preference is evident when predators select certain prey species among others that are equally available. Behavior leading to feeding is guided by intrinsic and extrinsic stimuli, including chemical cues from the environment (Kennedy, 1978; Haynes and Birch, 1985; Hsiao, 1985; New, 1991). Especially flexible prey selection behavior in generalist predators may result from a lesser need than specialists for specific cues from the environment, before potential prey is recognized. According to current theory, feeding behavior in predatory insects is largely stereotyped and programmed in the developing central nervous system as predetermined (at least in part) by the genetic code of the species (Bell, 1985; Thompson, 1990). Such programs are the basis of expressed behavior which permit the insect to find and catch prey. However, flexibility also is observed in actual feeding. Flexibility results from interaction between experiences and basic behavioral programs. Through experiences the insect may ‘‘learn’’ to discriminate between more and less significant cues leading to successful feeding, thus allowing more adapted exploitation of available resources. Conditioning and habituation are examples of simple learning that play an important role in predator searching behavior (Bell, 1991). Behavioral programming without actual learning also is possible through induction by chemical or other environmental cues during early development. Thorpe (1939) suggested that chemical cues deposited by the mother in or on an egg could later guide the chemosensory responses of newly hatched progeny. Selectivity could thus arise as a result of chemical cues acquired by the mother and transferred to its progeny via egg provisioning, to affect developing neural processes involved in food recognition (Bell, 1990). This is similar to
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the idea that ingestion of a certain food during immature stages would create a certain preference for the same food as an adult (Dethier, 1982), except that induction would be effective in the next generation as a sort of ‘‘chemical legacy’’ (Corbet, 1985). Induction refers to conditioning by simple contact and does not involve reinforcing or deterring (Bell, 1991). This phenomenon has been studied in parasitoids (Wardle and Borden, 1985; Kester and Barbosa, 1991). It is related to imprinting, which is described in vertebrates as a form of rapid, irreversible ‘‘learning,’’ characteristic of the early juvenile stages (Lorenz, 1937). This study was designed to better understand the prey selection behavior of Perillus bioculatus (Fabricius), a potentially useful predator whose feeding preferences are still unclear. P. bioculatus in potato fields seems to feed mostly if not exclusively on the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Knight, 1923; Tamaki and Butt, 1978; Hough-Goldstein and Keil, 1991; Biever and Chauvin, 1992; Hough-Goldstein et al., 1993), and some researchers have considered it oligophagous (Berre and Portier, 1963). However, in experimental conditions, P. bioculatus has been reared on diverse prey (Table 1). This confusion on the degree of polyphagy of P. bioculatus should be clarified. We consider two nonexclusive hypotheses regarding the determination of prey preference in P. bioculatus. They refer to the possibilities of: (1) genetic predisposition, toward CPB or related prey, and (2) a determining role for early experience of the prolarva with chemical cues within the egg. The first hypothesis implies that P. bioculatus could have developed through selection of a ‘‘taste’’ for the Colorado potato beetle, an inherent preference for the CPB. The second hypothesis states that prey preference by P. bioculatus is determined at least partly by specific components of its mother’s food during ovogenesis. The results should help establish if apparent preference for CPB in P. bioculatus is a specialized character with a large genetic component or if there is evidence that prey selection is determined environmentally through maternal induction. MATERIALS AND METHODS
The Predator P. bioculatus came from a laboratory colony maintained on eggs and larvae of the CPB. The colony was founded in 1992 from egg masses obtained from Dr. Mark Sears, Guelph University, and was supplemented yearly in late summer with adults from field plots where mass releases had been made several weeks earlier (Cloutier and Bauduin, 1995). Second instars that were naı¨ve with no feeding experience or direct
TABLE 1 Prey Recorded under Natural and Artificial Rearing Conditions for the Asopine Pentatomid Perillus bioculatus Species Coleoptera Bruchidae Acanthoscelides obtectus (Say) Chrysomelidae Cassida nebulosa (L.) Chrysomela sanguinolenta (L.) Chrysomela scripta (F.) Crioceris asparagi (L.) Disonycha xanthomelas (Dalm.) Galeruca pomonae (Scop.) Gastroidea polygoni (L.) Gastroidea viridula (Deg.) Lema trilineata (Oliv.) Leptinotarsa decemlineata (Say) Leptinotarsa lineolata (Stal.) Lina scripta (F.) Phytodecta fornicata (Bru¨ggm.) Trirhabda canadensis (Kirby) Zigogramma suturalis (F.) Zigogramma heterothecae Linell Coccinellidae Epilachna corrupta Epilachna varivestis (Mulsant) Subcoccinella 24-punctata (L.) Curculionidae Phytonomus variabilis (Hbst.) Homoptera Centrotinae (Microcentrus) Hymenoptera Athalia rosae (L.) Lepidoptera Ascia rapae (L.) Loxostege sticticalis (L.) Polia oleracea (L.) Trichoplusia ni (HBN.) Mamestra trifolii (Rott.) a Cabbage worms Pierid caterpillars Tussock moth larvae
Reference
Jermy (1962) Jermy (1962) Jermy (1980) Burkot and Bemjamin (1979) Landis (1937) Landis (1937) Jermy (1962) Jermy (1962) Jermy (1980) Landis (1937) Knight (1923) Jacques (1988) Strickland (1953) Jermy (1962) McPherson (1982) Altieri and Whitcomb (1979a) Altieri and Whitcomb (1979b) Bruneteau (1937) Howard and Landis (1936) Jermy (1962) Jermy (1962) Bruneteau (1937) Jermy (1962) Esselbaugh (1948) McPherson (1982) Jermy (1962) Landis (1937) Marsh (1913) Bruneteau (1937) Moens (1965) Nash (1912)
a Cited as Mamestra (Ceramica) picta (Harris) by Esselbaugh (1948).
contact with any potential source of food were evaluated [first instar nymphs do not normally feed (Knight, 1923; Landis, 1937; Tamaki and Butt, 1978)]. They were deprived of food for 45–50 h following molting to the second stage. Fasting time was adjusted so that nymphs would be hungry enough to readily examine and initiate feeding on usual prey, while not attacking all accessible but potential prey. Nymphs were held in a climatic chamber with a 16:8 h L:D photoperiod and temperature cycling according to a sine wave pattern between 15 and 25°C.
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Prey To test the hypotheses two unusual alternate prey species for P. bioculatus, in addition to the CPB, were used. Alternate prey were selected to satisfy two conditions: (1) P. bioculatus should have no particular predisposition or ecological link with prey; and (2) that alternate prey should allow P. bioculatus full development and reproduction. Alternate prey used were the yellow mealworm, Tenebrio molitor (L.), and the house cricket, Acheta domesticus (L.), which were easily available. The alternate prey are not likely to be ecologically linked to P. bioculatus, a foliage inhabiting hunter, and are unlikely to have played any role in the evolution of its prey selection behavior. The performance of P. bioculatus on yellow mealworm and house cricket prey was suboptimal compared to that of the CPB, but good enough to allow full development and reproduction as required (Saint-Cyr, 1995). However, both alternate prey had to be cut into pieces to be usable as food by P. bioculatus. The yellow mealworm is too vigorous to be handled and its exoskeleton is difficult to pierce by P. bioculatus nymphs. The house cricket is too large and mobile to be subdued successfully by P. bioculatus. The CPB prey were fourth larval stages that were also cut to eliminate any bias. Yellow mealworms were reared on flour and house crickets were fed pelleted rabbit food, potato tuber slices, and grass. Preference Test Predator preference data were obtained from observations on prey examination behavior by individual P. bioculatus nymphs in a small arena 1.5 cm in diameter in the center of a plastic cup half filled with water. A test involved several repetitions of alternate presentation of two kinds of prey. A single prey was accessible during any presentation but because both were briefly available at short interval, it was assumed that discrimination and preference would become apparent after several consecutive presentations. A test lasted 20 min, during which each nymph had an opportunity to examine 10 prey. Prey was alternated between presentations for five presentations of each species. Behavior recorded included antennation, proboscis contact or probing, and feeding indicated by stylets penetration and proboscis retraction. If no prey examination had occurred after 2 min, a nymph was moved to a new arena for a subsequent presentation involving succeeding prey. Nymphs that started feeding were immediately removed to a new arena, to limit positive conditioning through food ingestion. The prey species presented first in the sequence was alternated between individuals. To reduce variability in size and shape and to eliminate defense reactions, only the excised abdomen of each prey was presented; thus, all prey were ca. 5 mm
in length. Prey standardization presumably ensured that a nymph could not discriminate between prey on the basis of shape, size, or resistance of the exoskeleton and was thus more likely to use chemical cues, which were of particular interest. Experimental Design and Data Analysis Three different experiments were conducted (Table 2). The first hypothesis, that P. bioculatus would favor the CPB because of evolved affinity toward this prey, was evaluated by rearing parents on the yellow mealworm and then testing the F1 progeny (n 5 45 F1 nymphs) for preference for the CPB over the house cricket (Table 2). By rearing parents on the yellow mealworm, any bias toward either of the tested prey that might be due to a maternal influence (as supposed to exist according to the second hypothesis) presumably would be avoided. Therefore, any residual preference for the CPB in this test would likely be due to genetically inheritable affinity toward CPB. The second hypothesis, that there is prehatching preference induction by chemicals from the mother’s food, was evaluated in two steps. First, we reared P. bioculatus from egg to adult on the yellow mealworm and then tested F1 progeny (n 5 52 F1 nymphs) for preference toward CPB when presented the yellow mealworm as alternative prey. Second, we reared P. bioculatus on CPB larvae and tested the F1 for any preference toward the CPB, again with the yellow mealworm as alternative prey (n 5 52 F1 nymphs). A similar experiment was repeated this time with F1 progeny from house cricket-reared parents and using the house cricket as alternative prey to the CPB (n 5 48 F1 nymphs) (Table 2). For these two tests, we predicted that if there is a determining maternal influence on prey selectivity, it would appear as preference for an alternative prey. However, there also is the possibility that such maternal influence would interact with genetic predisposal of P. bioculatus toward the CPB (first hypothesis). Accordingly, preference of F1 nymphs whose parents were reared on CPB should be TABLE 2 Experimental Design for Investigating Genetic Predisposition and Maternal Induction as Determinants of Preference for the CPB in the Pentatomid Predator P. bioculatus Experiment
Parental prey
Prey choice test
Genetic predisposition Maternal predisposition
Yellow mealworm
House cricket/CPB
Yellow mealworm
Yellow mealworm/CPB Yellow mealworm/CPB House cricket/CPB House cricket/CPB
CPB House cricket CPB
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stronger, due to summation of genetic and maternal predispositions or to positive synergism between them. Data compiled were incidences of probing and feeding by F1 progeny on each prey. Data were analyzed using a generalized linear model with a binomial response, namely, a probit model (McCullagh and Nelder, 1989). The model considered up to three factors (main effects) possibly affecting the feeding behavior of naı¨ve nymphs: (i) the parental prey (Pa), which varied only in the maternal induction tests (see Table 2); (ii) the individual nymph tested (In) which, in the maternal induction tests, is nested within Pa [expressed as In(Pa)] for F1 nymphs from different parental background had to be different individuals; and (iii) the prey species presented to F1 progeny (Pr). The full statistical model for the induction tests also included a term for the interaction between parental prey and the prey presented to the progeny (symbolized by an asterisk joining the two factors below). Note that this interaction is expected under the hypothesis that the progeny’s preference for a particular prey is affected by parental prey. The full model is summarized by the equation f21(Iresp) 5 Pa 1 In (Pa) 1 Pr 1 Pa p Pr, where f21 stands for the probit link function (inverse of the cumulative normal distribution function) and Iresp is the incidence (probability) of responding to prey. Incidences of probing and feeding were modeled separately. The incidence of antennation was not analyzed, for all nymphs antennated prey that were placed in front of them. The incidence of probing of a prey was calculated for all presentations of that prey, but feeding incidence was calculated for only those presentations resulting in a nymph first responding by probing. The model was fitted using the SAS statistical package, using PROC GENMOD (SAS Institute 1987). Wald x2 was used for evaluating statistical significance at the 5% error rate level.
this and house cricket prey (Fig. 1; x2 5 3.23, df 5 1, P 5 0.036 for probing; and x2 5 3.17, df 5 1, P 5 0.038 for feeding). Because our a priori hypothesis specifically stated that P. bioculatus is genetically predisposed to the CPB, the P values reported for this test are for a one-tail x2 distribution (a more general null hypothesis would have doubled the P values, raising them slightly above the 5% error threshold). The results suggest that, without showing very strong preference, nymphs were able to discriminate potential prey at both stages of predation. Based on similar observations of P. bioculatus, Heimpel and Hough-Goldstein (1994b) suggested that P. bioculatus nymphs may recognize prey primarily by touch. Nymphs may have to contact prey with their proboscis because specific receptors providing information for the decision to proceed to feeding are probably located on that organ. However, ability to discriminate from a short distance by vision or smell would explain the unequal frequencies of probing observed here. These results are compatible with the idea that there is a genetic basis for P. bioculatus preference toward CPB prey, because nymphs tested were totally naı¨ve with respect to CPB prey, as they had neither direct nor indirect (maternal) prior contact with CPB. Any maternal influence in this experiment would predispose the F1 progeny to feed on the yellow mealworm, which was not available as prey. Maternal Induction These experiments revealed differences in prey selectivity by P. bioculatus nymphs that can be partly
RESULTS AND DISCUSSION
Average probing incidences varied between 10 and 40% but incidences of feeding were higher, varying from 70 to 100% for prey that were probed. Statistical analysis indicated that individual variation among nymphs was sometimes highly significant, justifying including this effect in the model. Results are described separately below for genetic predisposition and maternal induction tests. Genetic Predisposition P. bioculatus nymphs born from parents fed yellow mealworm showed significantly higher incidences for probing and feeding on the CPB with choices between
FIG. 1. Incidences of probing and feeding by naı¨ve second instar Perillus bioculatus reared from parents fed yellow mealworm prey, for the Colorado potato beetle (CPB) over house cricket prey. Each nymph (n 5 45 F1 tested) was presented with 5 CPBs and 5 house crickets alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
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TABLE 3 Statistical Analysis of Incidences of Probing and Feeding by P. bioculatus Nymphs in Preference Tests with the Colorado Potato Beetle and Alternate Prey (see text for details) Alternate prey Yellow mealworm Probing
Feeding
House cricket Probing
Source
DF
x2
P value
Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr
1 102 1 1 1 38 1 1
0.0 88.16 0.26 5.11 0.0 262.40 9.04 5.11
0.999 0.834 0.612 0.050 1.0 0.0 0.003 0.024
Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr
1 94 1 1
0.0 82.25 2.27 7.64
0.999 0.801 0.132 0.006
explained by prey used by their parents but again, there was evidence of intrinsic affinity for the CPB prey. Statistical modeling results are reported in Table 3 for both probing and feeding in the case of yellow mealworm as alternate prey, but only for probing with house cricket as alternate prey. In this case, feeding incidence was nearly 100% (Fig. 2), with insufficient variation to allow statistical modeling. For all three responses that could be modeled, interaction was significant, indicating that nymphs exhibited a different pattern of prey preference depending on prey used by their parent (Table 3). Therefore, statistical analysis was completed by contrasting responses to prey separately for progeny of each parental background (Figs. 2 and 3). In the experiment with the yellow mealworm as
alternate prey, F1 progeny from parents fed CPB tended to probe CPB prey selectively when presented with the yellow mealworm and the CPB, the difference being very close to statistical significance (Fig. 2; x2 5 3.18, df 5 1, P 5 0.074). However, evidence for preferred feeding on CPB prey was quite clear, as nymphs probing both prey initiated feeding on the CPB significantly more frequently (Fig. 2, x2 5 15.23, df 5 1, P 5 0.0001). In contrast to F1 progeny from CPB-fed parents, those from parents fed on yellow mealworm showed no sign of preference between these two prey, either by probing (Fig. 2, x2 5 1.01, df 5 1, P 5 0.314) or feeding (Fig. 2, x2 5 0.26, df 5 1, P 5 0.613). Results of testing the house cricket as alternate prey to CPB were similar, except that only probing could be modeled as mentioned (Fig. 3). Nymphs from CPB-fed parents selectively probed the CPB prey (x2 5 11.31, df 5 1, P 5 0.008), while progeny from house cricketfed parents showed no preference (x2 5 0.663, df 5 1, P 5 0.416). Statistical contrasts are thus consistent between results of both tests in showing that while nymphs from parents fed CPB preferred this prey, those from parents reared on alternate prey showed no selectivity toward maternal prey, in agreement with finding a significant Pa p Pr interaction (Table 3). Just as important as the fact that there was no evidence of selectivity for alternate prey despite maternal background, there is the other fact that the CPB was not preferred either, suggesting that the expression of any genetic predisposition toward this prey is affected by rearing parents on alternate prey. CONCLUSIONS
The first experiment suggests that the P. bioculatus population that we used probably has genetic predispo-
FIG. 2. Incidences of probing and feeding by naı¨ve second instar P. bioculatus reared from parents fed CPB prey (A) or yellow mealworm prey (B). For A and B, N 5 52 F1 tested, each with 5 CPBs and 5 yellow mealworms alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
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FIG. 3. Incidences of probing and feeding by naı¨ve second instar P. bioculatus reared from parents fed CPB prey (A) or house cricket prey (B). For A and B, N 5 48 F1 tested, each with 5 CPBs and 5 house crickets alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
sition to feed on the CPB. This does not exclude the possibility of P. bioculatus also having genetic affinity toward other prey species that are closely related to the CPB, particularly other Chrysomelid species (Heimpel and Hough-Goldstein, 1994b). The results also are compatible with the idea that prey consumed by adult P. bioculatus females can induce or raise acceptance for that prey in their progeny, although the efficiency of this modification of food selectivity seems to be greater when the prey is the CPB. This form of induction in P. bioculatus would be adaptive in helping young nymphs to focus on the CPB when it is available, but to exhibit no strong preference for it when different prey is available. We saw an apparent intrinsic affinity of P. bioculatus nymphs toward the CPB, as evidenced by results of the first experiment, that was not overcome by maternal induction with alternate prey. The CPB remained just as acceptable as maternal prey in tests involving yellow mealworm or house cricket as maternal prey, indicating that the supposed effect of maternal feeding on alternate prey does not eliminate inherent affinity toward the CPB. Intrinsic predisposition toward CPB was enhanced by maternal feeding on the CPB, suggesting additive interaction between genetic and maternally derived preference when prey is CPB. The function of induction in arthropod predators can be compared with imprinting that occurs in vertebrates, which is thought to be useful in circumstances in which individuals need to develop quick recognition of a complex environmental configuration that is critical to their survival (Ellis, 1985). Maternal induction in P. bioculatus could play a similar a role in helping this versatile predator to recognize and accept an alternative prey that is temporarily available. Such prey would be nutritionally suitable, as indicated by the presence of specific traces in the mother’s diet.
A close parallel can be made between our results with P. bioculatus and those obtained with some phytophagous insects. For example, larvae of Spodoptera littoralis (Boisd.) from parents reared on potato show high acceptance of this foodplant (Anderson et al., 1995). This type of epigenetically inherited preference gives the progeny the possibility of recognizing and more readily accepting a new prey after a single generation on this alternative food. In natural conditions, predators such as P. bioculatus would occasionally be forced to temporarily survive on suboptimal prey. Acceptability of a new prey could be quickly established by prey-specific chemical traces passed on from the adult female to the nymphs of the next generation. Eventually, maternally inherited preference could also be enhanced by selection, resulting in genetic changes that could lead to bias of a predator for a particular prey species, as may have occurred as P. bioculatus followed the CPB expansion in North America over the last 150 years. In accordance with the studies of several observers, including the recent ones by Heimpel and HoughGoldstein (1994a,b), our results based on intergeneration switching of prey species indicate that P. bioculatus is probably closer to the specialist than the generalist end of the prey specificity spectrum. Nevertheless, it does exhibit clear adaptability through maternal influence and possibly also through typical learning during nymphal development, which was not studied here. More should be known of the extent and nature of prey relationships with this predator, as such knowledge may directly increase the possibility of developing its exploitation for the biological control of the Colorado potato beetle. Indeed, finding that a predator’s prey preference can be partly under maternal influence is very important in the context of biological control. We know that diet
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changes can alter development (Hattingh and Samways, 1992), and we saw here that predators from parents fed on alternate prey behaved differently from those reared from parents fed with a normal prey. This would affect the efficacy of mass-reared predators, and we must know the consequences of this kind of variation in predator quality (Leppla and Ashley, 1989). ACKNOWLEDGMENTS We thank France Bauduin, Christine Jean, and Claude Carpentier for technical assistance and Jean-Se´bastien Brien for help with statistical analysis, all from Laval University. This study was supported by an NSERC grant to C.C.
REFERENCES Altieri, M. A., and Whitcomb, W. H. 1979a. Predaceous arthropods associated with Mexican tea in north Florida. Florida Entomol. 62, 175–182. Altieri, M. A., and Whitcomb, W. H. 1979b. Predaceous and hebivorous arthropods associated with camphorweed (Heterotheca subaxillaris Lamb.) in north Florida. J. Georgia Entomol. Soc. 15, 290–299. Anderson, P., Hilker, M., and Lo¨fqvist, J. 1995. Larval diet influence on oviposition behavior in Spodoptera littoralis. Entomol. Exp. Appl. 74, 71–82. Bell, W. J. 1985. Sources of information controlling motor patterns in arthropod local search orientation. J. Insect Physiol. 31, 837–847. Bell, W. J. 1990. Searching behavior patterns in insects. Annu. Rev. Entomol. 35, 447–467. Bell, W. J. 1991. ‘‘Searching Behavior: The Behavioral Ecology of Finding Resources’’ (D. M. Broom and P. W. Colgan, Eds.). Chapman & Hall, New York. Berre, J. R., and Portier, G. 1963. Utilisation d’un he´te´ropte`re Pentatomidae Perillus bioculatus (Fabr.) dans la lutte contre le doryphore Leptinotarsa decemlineata (Say): premiers re´sultats obtenus en France. Entomophaga 8, 183–190. Biever, K. D., and Chauvin, R. L. 1992. Suppression of the Colorado potato beetle (Coleoptera: Chrysomelidae) with augmentative releases of predaceous stinkbugs (Hemiptera: Pentatomidae). J. Econ. Entomol. 85, 720–726. Bruneteau, J. 1937. Recherches sur les ennemis naturels du doryphore en Ame´rique. Ann. Epiphyt. Phytoge´n. 3 (n.s.), 113–135. Burkot, T. R., and Benjamin, D. M. 1979. The biology and ecology of the cottonwood leaf beetle, Chrysomela scripta (Coleoptera: Chrysomelidae), on tissue cultured hybrid Aigeiros ( Populus x euramericana) subclones in Wisconsin. Can. Entomol. 111, 551– 556. Cloutier, C. and Bauduin, F. 1995. Biological control of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) in Que´bec by augmentative releases of the two-spotted stinkbug Perillus bioculatus (Hemiptera: Pentatomidae). Can. Entomol. 127, 195–212. Corbet, S. A. 1985. Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Entomol. 10, 143–153. Dethier, V. G. 1982. Mechanism of host-plant recognition. Entomol. Exp. Appl. 31, 49–56. Ellis, D. V. 1985. ‘‘Animal Behavior and Its Applications.’’ Lewis, Chelsea, MI. Esselbaugh, C. O. 1948. Notes on the bionomics of some midwestern Pentatomidae. Entomol. Am. 28, 1–71.
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Hattingh, V., and Samways, M. J. 1992. Prey choice and substitution in Chilocorus spp. (Coleoptera: Coccinellidae). Bull. Entomol. Res. 82, 327–334. Haynes, K. F., and Birch, M. C. 1985. The role of other pheromones, allomones and kairomones in behavioral responses of insects. In ‘‘Comprehensive Insect Physiology, Biochemistry and Pharmacology (G. A. Kerkut and L. I. Gilbert, Eds.), Vol. 9, pp. 225–253. Pergamon Press, New York. Heimpel, G. E., and Hough-Goldstein, J. A. 1994a. Search tactics and responses to cues by predatory stink bugs. Entomol. Exp. Appl. 73, 193–197. Heimpel, G. E., and Hough-Goldstein, J. A. 1994b. Components of the functional response of Perillus bioculatus (Hemiptera: Pentatomidae). Environ. Entomol. 23, 855–859. Hough-Goldstein, J., and Keil, C. B. 1992. Prospects for integrated control of the Colorado potato beetle (Coleoptera: Chrysomelidae) using Perillus bioculatus (Hemiptera: Pentatomidae) and various pesticides. J. Econ. Entomol. 84, 1645–1651. Hough-Goldstein, J. A., Heimpel, G. E., Bechman, H. E., and Mason, C. E. 1993. Arthropod natural enemies of the Colorado potato beetle. Crop protec. 12, 324–334. Howard, N. F., and Landis, B. J. 1936. ‘‘Parasites and Predators of the Mexican Bean Beetle in the United States.’’ U.S. Dept. of Agriculture, circular 418, Washington DC. Hsiao, T. H. 1985. Feeding behavior. In ‘‘Comprehensive Insect Physiology, Biochemistry and Pharmacology’’ (G. A. Kerkut and L. I. Gilbert, Eds.), Vol. 9, pp. 471–512. Pergamon Press, New York. Jacques, R. L. 1988. ‘‘The Potato Beetles.’’ Brill, New York. ¨ ber einbu¨rgerungsversuche mit Perillus bioculatus Jermy, T. 1962. U Fabr. (Heteroptera, Pentatomidae) in Ungarn. Agronomski Glasnik. Zagreb 5–7, 558–562. Jermy, T. 1980. The introduction of Perillus bioculatus into Europe to control the Colorado beetle. EPPO Bull. 10, 475–479. Kennedy, J. S. 1978. The concept of olfactory ‘‘arrestment’’ and ‘‘attraction.’’ Physiol. Entomol. 3, 91–98. Kester, K. M., and Barbosa, P. 1991. Postemergence learning in the insect parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae). J. Insect Behav. 4, 727–741. Knight, H. H. 1923. Studies on the life history and biology of Perillus bioculatus Fab., including observations on the nature of color pattern (Hemiptera: Pentatomidae). 19th Rep. State Entomol. Minn. 50–96. Landis, B. J. 1937. Insect hosts and nymphal development of Podisus maculiventris Say and Perillus bioculatus F. (Hemiptera, Pentatomidae). Ohio J. Sci. 37, 252–259. Leppla, N. C., and Ashley, T. R. 1989. Quality control in insect mass production: A review and a model. Bull. ESA 35, 33–43. Lorenz, K. 1937. The companion in the bird’s world. Auk 54, 245–273. Marsh, H. O. 1913. The striped beet caterpillar. In Papers on insects affecting vegetables and truck crops. U.S. Bur. Ent. Bull. 127(part 2), 11–18. McCullagh, P., and Nelder, J. A. 1989. ‘‘Generalized Linear Models,’’ 2nd ed., pp. 13–14. Chapman & Hall, London. McPherson, J. E. 1982. ‘‘The Pentatomoidea (Hemiptera) of Northeastern North America with Emphasis on the Fauna of Illinois’’ (S. W. Smith, Ed.), pp. 98–99. Southern Illinois Univ. Press, Carbondale. Moens, R. 1965. Observations sur les exigences alimentaires de Perillus bioculatus Fabr. Med. Lan. Opz. van de Staat te Gent. 30, 1504–1515. Nash, C. W. 1912. The report of the entomological society of Ontario (Division No. 4, East Toronto) 36, 17–19. New, T. R. 1991. ‘‘Insects as Predators.’’ New South Wales Univ. Press, Kensington.
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Saint-Cyr, J.-F. 1995. ‘‘Pre´fe´rences Alimentaires chez Perillus bioculatus (Hemiptera: Pentatomidae), un Pre´dateur Ge´ne´raliste.’’ M.Sc. thesis, Laval University, Que´bec. Sas Institute. 1987. ‘‘SAS User’s Guide: Statistics.’’ SAS Inst., Cary, NC. Strickland, E. H. 1953. An annotated list of the Hemiptera (S.L.) of Alberta. Can. Entomol. 85, 193–214. Tamaki, G., and Butt, B. A. 1978. Impact of Perillus bioculatus on the Colorado potato beetle and plant damage. USDA Tech. Bull. 1581, 1–11.
Thompson, S. N. 1990. Nutritional considerations in propagation of entomophagous species. In ‘‘New Directions in Biological Control: Alternatives for Suppressing Agricultural Pests and Diseases,’’ pp. 389–404. A.R. Liss, New York. Thorpe, W. H. 1939. Further studies on pre-imaginal olfactory conditioning in insects. Proc. R. Soc. London B: 127, 424–433. Wardle, A. R., and Borden, J. H. 1985. Age-dependent associative learning by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Can. Entomol. 117, 605–616.
7, 251–258 (1996)
0091
Prey Preference by the Stinkbug Perillus bioculatus, a Predator of the Colorado Potato Beetle JEAN-FRANC¸OIS SAINT-CYR
AND
CONRAD CLOUTIER1
Centre de Recherche en Horticulture, De´partement de Biologie, Universite´ Laval, Cite´ Universitaire, Que´bec, Canada G1K 7P4 Received January 26, 1996; accepted May 31, 1996
INTRODUCTION Perillus bioculatus (F.) is sometimes considered a generalist but has most often been recorded as predator of Colorado potato beetle (CPB),Leptinotarsa decemlineata. (Say). This study was designed to analyze prey selection in P. bioculatus with respect to factors that may lead to specialization. To establish if parental prey determines preference in naı¨ve progeny, prey selection experiments were conducted with the CPB and two unusual prey, the yellow mealworm Tenebrio molitor (L.) and the house cricket Acheta domesticus (L.). Naı¨ve nymphs reared from yellow mealworm-fed parents in the absence of contact with the CPB initiated feeding more frequently on CPB (81.4%) than on cricket prey (69.6%) (P 5 0.038), suggesting genetically inheritable preference for CPB. Progeny from CPBfed parents initiated feeding more frequently on CPB prey (93.3%) than on yellow mealworm prey (76.6%) (P 5 0.0001), but progeny from yellow mealwormfed parents initiated feeding on yellow mealworm prey as frequently (89.2%) as on CPB (95.0%) (P 5 0.613). Similarly, progeny from CPB-fed parents established proboscis contact more frequently on CPB (39.2%) than on house cricket prey (25.0%) (P 5 0.008), whereas those from cricket-fed parents probed house cricket prey as frequently (12.5%) as CPB prey (15.4%) (P 5 0.416). Results confirm specialization of P. bioculatus toward CPB or related prey and suggest genetically inheritable as well as maternally reinforcible affinity toward CPB prey. However, affinity of naı¨ve nymphs for the CPB can be lowered by rearing parents on alternative prey, increasing their chances of survival when alternative prey must be relied upon. r 1996 Academic Press, Inc.
KEY WORDS: Perillus bioculatus; Leptinotarsa decemlineata; Acheta domestica; Tenebrio molitor; prey selection; maternal induction.
1 To whom correspondence should be addressed. Fax: 418-6562043. E-mail [email protected].
Generalist arthropod predators feed on various prey species from different families or even orders, among which they show no clear preference. The opposite is true for specialists, which feed mainly on one type of prey or a few closely related species (Hsiao, 1985). Preference is evident when predators select certain prey species among others that are equally available. Behavior leading to feeding is guided by intrinsic and extrinsic stimuli, including chemical cues from the environment (Kennedy, 1978; Haynes and Birch, 1985; Hsiao, 1985; New, 1991). Especially flexible prey selection behavior in generalist predators may result from a lesser need than specialists for specific cues from the environment, before potential prey is recognized. According to current theory, feeding behavior in predatory insects is largely stereotyped and programmed in the developing central nervous system as predetermined (at least in part) by the genetic code of the species (Bell, 1985; Thompson, 1990). Such programs are the basis of expressed behavior which permit the insect to find and catch prey. However, flexibility also is observed in actual feeding. Flexibility results from interaction between experiences and basic behavioral programs. Through experiences the insect may ‘‘learn’’ to discriminate between more and less significant cues leading to successful feeding, thus allowing more adapted exploitation of available resources. Conditioning and habituation are examples of simple learning that play an important role in predator searching behavior (Bell, 1991). Behavioral programming without actual learning also is possible through induction by chemical or other environmental cues during early development. Thorpe (1939) suggested that chemical cues deposited by the mother in or on an egg could later guide the chemosensory responses of newly hatched progeny. Selectivity could thus arise as a result of chemical cues acquired by the mother and transferred to its progeny via egg provisioning, to affect developing neural processes involved in food recognition (Bell, 1990). This is similar to
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the idea that ingestion of a certain food during immature stages would create a certain preference for the same food as an adult (Dethier, 1982), except that induction would be effective in the next generation as a sort of ‘‘chemical legacy’’ (Corbet, 1985). Induction refers to conditioning by simple contact and does not involve reinforcing or deterring (Bell, 1991). This phenomenon has been studied in parasitoids (Wardle and Borden, 1985; Kester and Barbosa, 1991). It is related to imprinting, which is described in vertebrates as a form of rapid, irreversible ‘‘learning,’’ characteristic of the early juvenile stages (Lorenz, 1937). This study was designed to better understand the prey selection behavior of Perillus bioculatus (Fabricius), a potentially useful predator whose feeding preferences are still unclear. P. bioculatus in potato fields seems to feed mostly if not exclusively on the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Knight, 1923; Tamaki and Butt, 1978; Hough-Goldstein and Keil, 1991; Biever and Chauvin, 1992; Hough-Goldstein et al., 1993), and some researchers have considered it oligophagous (Berre and Portier, 1963). However, in experimental conditions, P. bioculatus has been reared on diverse prey (Table 1). This confusion on the degree of polyphagy of P. bioculatus should be clarified. We consider two nonexclusive hypotheses regarding the determination of prey preference in P. bioculatus. They refer to the possibilities of: (1) genetic predisposition, toward CPB or related prey, and (2) a determining role for early experience of the prolarva with chemical cues within the egg. The first hypothesis implies that P. bioculatus could have developed through selection of a ‘‘taste’’ for the Colorado potato beetle, an inherent preference for the CPB. The second hypothesis states that prey preference by P. bioculatus is determined at least partly by specific components of its mother’s food during ovogenesis. The results should help establish if apparent preference for CPB in P. bioculatus is a specialized character with a large genetic component or if there is evidence that prey selection is determined environmentally through maternal induction. MATERIALS AND METHODS
The Predator P. bioculatus came from a laboratory colony maintained on eggs and larvae of the CPB. The colony was founded in 1992 from egg masses obtained from Dr. Mark Sears, Guelph University, and was supplemented yearly in late summer with adults from field plots where mass releases had been made several weeks earlier (Cloutier and Bauduin, 1995). Second instars that were naı¨ve with no feeding experience or direct
TABLE 1 Prey Recorded under Natural and Artificial Rearing Conditions for the Asopine Pentatomid Perillus bioculatus Species Coleoptera Bruchidae Acanthoscelides obtectus (Say) Chrysomelidae Cassida nebulosa (L.) Chrysomela sanguinolenta (L.) Chrysomela scripta (F.) Crioceris asparagi (L.) Disonycha xanthomelas (Dalm.) Galeruca pomonae (Scop.) Gastroidea polygoni (L.) Gastroidea viridula (Deg.) Lema trilineata (Oliv.) Leptinotarsa decemlineata (Say) Leptinotarsa lineolata (Stal.) Lina scripta (F.) Phytodecta fornicata (Bru¨ggm.) Trirhabda canadensis (Kirby) Zigogramma suturalis (F.) Zigogramma heterothecae Linell Coccinellidae Epilachna corrupta Epilachna varivestis (Mulsant) Subcoccinella 24-punctata (L.) Curculionidae Phytonomus variabilis (Hbst.) Homoptera Centrotinae (Microcentrus) Hymenoptera Athalia rosae (L.) Lepidoptera Ascia rapae (L.) Loxostege sticticalis (L.) Polia oleracea (L.) Trichoplusia ni (HBN.) Mamestra trifolii (Rott.) a Cabbage worms Pierid caterpillars Tussock moth larvae
Reference
Jermy (1962) Jermy (1962) Jermy (1980) Burkot and Bemjamin (1979) Landis (1937) Landis (1937) Jermy (1962) Jermy (1962) Jermy (1980) Landis (1937) Knight (1923) Jacques (1988) Strickland (1953) Jermy (1962) McPherson (1982) Altieri and Whitcomb (1979a) Altieri and Whitcomb (1979b) Bruneteau (1937) Howard and Landis (1936) Jermy (1962) Jermy (1962) Bruneteau (1937) Jermy (1962) Esselbaugh (1948) McPherson (1982) Jermy (1962) Landis (1937) Marsh (1913) Bruneteau (1937) Moens (1965) Nash (1912)
a Cited as Mamestra (Ceramica) picta (Harris) by Esselbaugh (1948).
contact with any potential source of food were evaluated [first instar nymphs do not normally feed (Knight, 1923; Landis, 1937; Tamaki and Butt, 1978)]. They were deprived of food for 45–50 h following molting to the second stage. Fasting time was adjusted so that nymphs would be hungry enough to readily examine and initiate feeding on usual prey, while not attacking all accessible but potential prey. Nymphs were held in a climatic chamber with a 16:8 h L:D photoperiod and temperature cycling according to a sine wave pattern between 15 and 25°C.
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Prey To test the hypotheses two unusual alternate prey species for P. bioculatus, in addition to the CPB, were used. Alternate prey were selected to satisfy two conditions: (1) P. bioculatus should have no particular predisposition or ecological link with prey; and (2) that alternate prey should allow P. bioculatus full development and reproduction. Alternate prey used were the yellow mealworm, Tenebrio molitor (L.), and the house cricket, Acheta domesticus (L.), which were easily available. The alternate prey are not likely to be ecologically linked to P. bioculatus, a foliage inhabiting hunter, and are unlikely to have played any role in the evolution of its prey selection behavior. The performance of P. bioculatus on yellow mealworm and house cricket prey was suboptimal compared to that of the CPB, but good enough to allow full development and reproduction as required (Saint-Cyr, 1995). However, both alternate prey had to be cut into pieces to be usable as food by P. bioculatus. The yellow mealworm is too vigorous to be handled and its exoskeleton is difficult to pierce by P. bioculatus nymphs. The house cricket is too large and mobile to be subdued successfully by P. bioculatus. The CPB prey were fourth larval stages that were also cut to eliminate any bias. Yellow mealworms were reared on flour and house crickets were fed pelleted rabbit food, potato tuber slices, and grass. Preference Test Predator preference data were obtained from observations on prey examination behavior by individual P. bioculatus nymphs in a small arena 1.5 cm in diameter in the center of a plastic cup half filled with water. A test involved several repetitions of alternate presentation of two kinds of prey. A single prey was accessible during any presentation but because both were briefly available at short interval, it was assumed that discrimination and preference would become apparent after several consecutive presentations. A test lasted 20 min, during which each nymph had an opportunity to examine 10 prey. Prey was alternated between presentations for five presentations of each species. Behavior recorded included antennation, proboscis contact or probing, and feeding indicated by stylets penetration and proboscis retraction. If no prey examination had occurred after 2 min, a nymph was moved to a new arena for a subsequent presentation involving succeeding prey. Nymphs that started feeding were immediately removed to a new arena, to limit positive conditioning through food ingestion. The prey species presented first in the sequence was alternated between individuals. To reduce variability in size and shape and to eliminate defense reactions, only the excised abdomen of each prey was presented; thus, all prey were ca. 5 mm
in length. Prey standardization presumably ensured that a nymph could not discriminate between prey on the basis of shape, size, or resistance of the exoskeleton and was thus more likely to use chemical cues, which were of particular interest. Experimental Design and Data Analysis Three different experiments were conducted (Table 2). The first hypothesis, that P. bioculatus would favor the CPB because of evolved affinity toward this prey, was evaluated by rearing parents on the yellow mealworm and then testing the F1 progeny (n 5 45 F1 nymphs) for preference for the CPB over the house cricket (Table 2). By rearing parents on the yellow mealworm, any bias toward either of the tested prey that might be due to a maternal influence (as supposed to exist according to the second hypothesis) presumably would be avoided. Therefore, any residual preference for the CPB in this test would likely be due to genetically inheritable affinity toward CPB. The second hypothesis, that there is prehatching preference induction by chemicals from the mother’s food, was evaluated in two steps. First, we reared P. bioculatus from egg to adult on the yellow mealworm and then tested F1 progeny (n 5 52 F1 nymphs) for preference toward CPB when presented the yellow mealworm as alternative prey. Second, we reared P. bioculatus on CPB larvae and tested the F1 for any preference toward the CPB, again with the yellow mealworm as alternative prey (n 5 52 F1 nymphs). A similar experiment was repeated this time with F1 progeny from house cricket-reared parents and using the house cricket as alternative prey to the CPB (n 5 48 F1 nymphs) (Table 2). For these two tests, we predicted that if there is a determining maternal influence on prey selectivity, it would appear as preference for an alternative prey. However, there also is the possibility that such maternal influence would interact with genetic predisposal of P. bioculatus toward the CPB (first hypothesis). Accordingly, preference of F1 nymphs whose parents were reared on CPB should be TABLE 2 Experimental Design for Investigating Genetic Predisposition and Maternal Induction as Determinants of Preference for the CPB in the Pentatomid Predator P. bioculatus Experiment
Parental prey
Prey choice test
Genetic predisposition Maternal predisposition
Yellow mealworm
House cricket/CPB
Yellow mealworm
Yellow mealworm/CPB Yellow mealworm/CPB House cricket/CPB House cricket/CPB
CPB House cricket CPB
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stronger, due to summation of genetic and maternal predispositions or to positive synergism between them. Data compiled were incidences of probing and feeding by F1 progeny on each prey. Data were analyzed using a generalized linear model with a binomial response, namely, a probit model (McCullagh and Nelder, 1989). The model considered up to three factors (main effects) possibly affecting the feeding behavior of naı¨ve nymphs: (i) the parental prey (Pa), which varied only in the maternal induction tests (see Table 2); (ii) the individual nymph tested (In) which, in the maternal induction tests, is nested within Pa [expressed as In(Pa)] for F1 nymphs from different parental background had to be different individuals; and (iii) the prey species presented to F1 progeny (Pr). The full statistical model for the induction tests also included a term for the interaction between parental prey and the prey presented to the progeny (symbolized by an asterisk joining the two factors below). Note that this interaction is expected under the hypothesis that the progeny’s preference for a particular prey is affected by parental prey. The full model is summarized by the equation f21(Iresp) 5 Pa 1 In (Pa) 1 Pr 1 Pa p Pr, where f21 stands for the probit link function (inverse of the cumulative normal distribution function) and Iresp is the incidence (probability) of responding to prey. Incidences of probing and feeding were modeled separately. The incidence of antennation was not analyzed, for all nymphs antennated prey that were placed in front of them. The incidence of probing of a prey was calculated for all presentations of that prey, but feeding incidence was calculated for only those presentations resulting in a nymph first responding by probing. The model was fitted using the SAS statistical package, using PROC GENMOD (SAS Institute 1987). Wald x2 was used for evaluating statistical significance at the 5% error rate level.
this and house cricket prey (Fig. 1; x2 5 3.23, df 5 1, P 5 0.036 for probing; and x2 5 3.17, df 5 1, P 5 0.038 for feeding). Because our a priori hypothesis specifically stated that P. bioculatus is genetically predisposed to the CPB, the P values reported for this test are for a one-tail x2 distribution (a more general null hypothesis would have doubled the P values, raising them slightly above the 5% error threshold). The results suggest that, without showing very strong preference, nymphs were able to discriminate potential prey at both stages of predation. Based on similar observations of P. bioculatus, Heimpel and Hough-Goldstein (1994b) suggested that P. bioculatus nymphs may recognize prey primarily by touch. Nymphs may have to contact prey with their proboscis because specific receptors providing information for the decision to proceed to feeding are probably located on that organ. However, ability to discriminate from a short distance by vision or smell would explain the unequal frequencies of probing observed here. These results are compatible with the idea that there is a genetic basis for P. bioculatus preference toward CPB prey, because nymphs tested were totally naı¨ve with respect to CPB prey, as they had neither direct nor indirect (maternal) prior contact with CPB. Any maternal influence in this experiment would predispose the F1 progeny to feed on the yellow mealworm, which was not available as prey. Maternal Induction These experiments revealed differences in prey selectivity by P. bioculatus nymphs that can be partly
RESULTS AND DISCUSSION
Average probing incidences varied between 10 and 40% but incidences of feeding were higher, varying from 70 to 100% for prey that were probed. Statistical analysis indicated that individual variation among nymphs was sometimes highly significant, justifying including this effect in the model. Results are described separately below for genetic predisposition and maternal induction tests. Genetic Predisposition P. bioculatus nymphs born from parents fed yellow mealworm showed significantly higher incidences for probing and feeding on the CPB with choices between
FIG. 1. Incidences of probing and feeding by naı¨ve second instar Perillus bioculatus reared from parents fed yellow mealworm prey, for the Colorado potato beetle (CPB) over house cricket prey. Each nymph (n 5 45 F1 tested) was presented with 5 CPBs and 5 house crickets alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
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TABLE 3 Statistical Analysis of Incidences of Probing and Feeding by P. bioculatus Nymphs in Preference Tests with the Colorado Potato Beetle and Alternate Prey (see text for details) Alternate prey Yellow mealworm Probing
Feeding
House cricket Probing
Source
DF
x2
P value
Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr
1 102 1 1 1 38 1 1
0.0 88.16 0.26 5.11 0.0 262.40 9.04 5.11
0.999 0.834 0.612 0.050 1.0 0.0 0.003 0.024
Parental prey (Pa) Individual (In) Prey presented (Pr) Pa p Pr
1 94 1 1
0.0 82.25 2.27 7.64
0.999 0.801 0.132 0.006
explained by prey used by their parents but again, there was evidence of intrinsic affinity for the CPB prey. Statistical modeling results are reported in Table 3 for both probing and feeding in the case of yellow mealworm as alternate prey, but only for probing with house cricket as alternate prey. In this case, feeding incidence was nearly 100% (Fig. 2), with insufficient variation to allow statistical modeling. For all three responses that could be modeled, interaction was significant, indicating that nymphs exhibited a different pattern of prey preference depending on prey used by their parent (Table 3). Therefore, statistical analysis was completed by contrasting responses to prey separately for progeny of each parental background (Figs. 2 and 3). In the experiment with the yellow mealworm as
alternate prey, F1 progeny from parents fed CPB tended to probe CPB prey selectively when presented with the yellow mealworm and the CPB, the difference being very close to statistical significance (Fig. 2; x2 5 3.18, df 5 1, P 5 0.074). However, evidence for preferred feeding on CPB prey was quite clear, as nymphs probing both prey initiated feeding on the CPB significantly more frequently (Fig. 2, x2 5 15.23, df 5 1, P 5 0.0001). In contrast to F1 progeny from CPB-fed parents, those from parents fed on yellow mealworm showed no sign of preference between these two prey, either by probing (Fig. 2, x2 5 1.01, df 5 1, P 5 0.314) or feeding (Fig. 2, x2 5 0.26, df 5 1, P 5 0.613). Results of testing the house cricket as alternate prey to CPB were similar, except that only probing could be modeled as mentioned (Fig. 3). Nymphs from CPB-fed parents selectively probed the CPB prey (x2 5 11.31, df 5 1, P 5 0.008), while progeny from house cricketfed parents showed no preference (x2 5 0.663, df 5 1, P 5 0.416). Statistical contrasts are thus consistent between results of both tests in showing that while nymphs from parents fed CPB preferred this prey, those from parents reared on alternate prey showed no selectivity toward maternal prey, in agreement with finding a significant Pa p Pr interaction (Table 3). Just as important as the fact that there was no evidence of selectivity for alternate prey despite maternal background, there is the other fact that the CPB was not preferred either, suggesting that the expression of any genetic predisposition toward this prey is affected by rearing parents on alternate prey. CONCLUSIONS
The first experiment suggests that the P. bioculatus population that we used probably has genetic predispo-
FIG. 2. Incidences of probing and feeding by naı¨ve second instar P. bioculatus reared from parents fed CPB prey (A) or yellow mealworm prey (B). For A and B, N 5 52 F1 tested, each with 5 CPBs and 5 yellow mealworms alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
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FIG. 3. Incidences of probing and feeding by naı¨ve second instar P. bioculatus reared from parents fed CPB prey (A) or house cricket prey (B). For A and B, N 5 48 F1 tested, each with 5 CPBs and 5 house crickets alternating in 2-min presentations. Means represented by columns with the same letter are not significantly different (P . 0.05).
sition to feed on the CPB. This does not exclude the possibility of P. bioculatus also having genetic affinity toward other prey species that are closely related to the CPB, particularly other Chrysomelid species (Heimpel and Hough-Goldstein, 1994b). The results also are compatible with the idea that prey consumed by adult P. bioculatus females can induce or raise acceptance for that prey in their progeny, although the efficiency of this modification of food selectivity seems to be greater when the prey is the CPB. This form of induction in P. bioculatus would be adaptive in helping young nymphs to focus on the CPB when it is available, but to exhibit no strong preference for it when different prey is available. We saw an apparent intrinsic affinity of P. bioculatus nymphs toward the CPB, as evidenced by results of the first experiment, that was not overcome by maternal induction with alternate prey. The CPB remained just as acceptable as maternal prey in tests involving yellow mealworm or house cricket as maternal prey, indicating that the supposed effect of maternal feeding on alternate prey does not eliminate inherent affinity toward the CPB. Intrinsic predisposition toward CPB was enhanced by maternal feeding on the CPB, suggesting additive interaction between genetic and maternally derived preference when prey is CPB. The function of induction in arthropod predators can be compared with imprinting that occurs in vertebrates, which is thought to be useful in circumstances in which individuals need to develop quick recognition of a complex environmental configuration that is critical to their survival (Ellis, 1985). Maternal induction in P. bioculatus could play a similar a role in helping this versatile predator to recognize and accept an alternative prey that is temporarily available. Such prey would be nutritionally suitable, as indicated by the presence of specific traces in the mother’s diet.
A close parallel can be made between our results with P. bioculatus and those obtained with some phytophagous insects. For example, larvae of Spodoptera littoralis (Boisd.) from parents reared on potato show high acceptance of this foodplant (Anderson et al., 1995). This type of epigenetically inherited preference gives the progeny the possibility of recognizing and more readily accepting a new prey after a single generation on this alternative food. In natural conditions, predators such as P. bioculatus would occasionally be forced to temporarily survive on suboptimal prey. Acceptability of a new prey could be quickly established by prey-specific chemical traces passed on from the adult female to the nymphs of the next generation. Eventually, maternally inherited preference could also be enhanced by selection, resulting in genetic changes that could lead to bias of a predator for a particular prey species, as may have occurred as P. bioculatus followed the CPB expansion in North America over the last 150 years. In accordance with the studies of several observers, including the recent ones by Heimpel and HoughGoldstein (1994a,b), our results based on intergeneration switching of prey species indicate that P. bioculatus is probably closer to the specialist than the generalist end of the prey specificity spectrum. Nevertheless, it does exhibit clear adaptability through maternal influence and possibly also through typical learning during nymphal development, which was not studied here. More should be known of the extent and nature of prey relationships with this predator, as such knowledge may directly increase the possibility of developing its exploitation for the biological control of the Colorado potato beetle. Indeed, finding that a predator’s prey preference can be partly under maternal influence is very important in the context of biological control. We know that diet
PREY PREFERENCE IN Perillus bioculatus
changes can alter development (Hattingh and Samways, 1992), and we saw here that predators from parents fed on alternate prey behaved differently from those reared from parents fed with a normal prey. This would affect the efficacy of mass-reared predators, and we must know the consequences of this kind of variation in predator quality (Leppla and Ashley, 1989). ACKNOWLEDGMENTS We thank France Bauduin, Christine Jean, and Claude Carpentier for technical assistance and Jean-Se´bastien Brien for help with statistical analysis, all from Laval University. This study was supported by an NSERC grant to C.C.
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