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Aposematic Caterpillars: Life-Styles of the Warningly Colored And 330 / Stamp and Wilkens Waage, J.K. 1983. Aggregation in field parasitoid populations: foraging time allocation 10 a population of Diadegma (Hymenoptera: Ichneumonidae). Ecol. Entomol. 8:447­ 453. Washburn, J.O. 1984. Mutualism between a cynipid wasp and ants. Ecology 65:654­ Aposematic Caterpillars: 656. Welty, J.C., and Baptista, L. 1988. The Life of Birds, 4th ed. Saunders, Philadelphia. Life-Styles of the Warningly Colored Werner, E.E., and Gilliam, J.F. 1984. The ontogenetic niche and species interactions in and Unpalatable size-structured populations. Annu.Rev. Ecol. Syst. 15:393-425. Werner, T. K., and Sherry, T. W. 1987. Behavioral feeding specialization in Pinaroloxias M. Deane Bowers inornata, the HDarwin's Finch" of Cocos Island, Costa Rica. Proc. Natl. Acad. Sci. U.S.A. 84:5506-5510. Weseloh, R.M. 1977. Behavioral responses of the parasite, Apanteles melanoscelus, to gypsy moth silk. Environ. Entomol. 5:1128-1132. Weseloh, R.M. 1988. Effects of microhabitat, time of day, and weather on predation of gypsy moth larvae. Oecologia 77:250-254. Introduction Weseloh, R. M. 1989. Behavioral responses of gypsy moth (Lepidoptera: Lymantriidae) larvae to abiotic environmental factors. Environ. Entomol. 18:361-367. Caterpillars have an impressive array of defenses to avoid being eaten. For Wiedenmann, R.N., and O'Neil, R.J. 1991. Searching behavior and time budgets of the example, they may blend in extremely well with their background (Cott 1940; predator Podisus maculiventris. Entomol. Exp. Appl. 60:83-93. Edmunds 1974, 1990), they may mimic potential predators of their own predators Yamasaki, M., Hirose, Y. and Takagi, M. 1978. Repeated visits of Polistes jadwigae (Nentwig 1985; Pough 1988), they may construct shelters (Fitzgerald 1980; Dalla Torre (Hymenoptera: Vespidae) to its hunting site. J. Appl. Entomol. Zoo!. Fitzgerald and Willer 1983; Damman 1987), and they may be unpalatable due to 22:51-55 (in Japanese with English summary). urticating hairs (Kawamoto and Kumada 1984), defensive glands such as osmete­ Yeargan, K.V., and Braman, S.K. 1989a. Comparative behavioral studies of indigenous ria (Honda 1983; Damman 1986), or chemicals sequestered from their host hemipteran predators and hymenopteran parasites ofthe green cloverworm (Lepidoptera: Noctuidae). J. Kansas Entomol. Soc. 62: 156-163. plants (Duffey 1980; Blum 1983; Bowers 1990). Insects that are unpalatable are particularly interesting in that they not only use their bad taste or unpleasant odor Yeargan, K. V., and Braman, S. K. 1989b. Life history of the hyperparasitoid Mesochorus as a defense, but they usually also advertise this defense to would-be predators discitergus (Hymenoptera: Ichneumonidae) and tactics used to overcome the defensive by attributes such as conspicuous coloration, gregariousness, and sedentary be­ behavior of the green cloverworm (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 82:393-398. havior. Possession of unpalatable qualities coupled with advertisement of those quali­ Ydenberg, R.C., and Dill, L.M. 1986. The economics of fleeing from predators. Adv. ties has many consequences for the life history features, population biology, Study Behav. 16:229-249. physiology, and foraging behavior of aposematic caterpillars. For example, apo­ Young, A.M. 1971. Wing coloration and reflectance in Morpho butterflies as related to sematic caterpillars need not hide from most potential predators and so, on a reproductive behavior and escape from avian predators. Oecologia 7:209-222. basis, may be able to spend more time feeding than cryptic caterpillars that must Young, A.M. 1972. Adaptive strategies of feeding and predator-avoidance in the larvae behave in ways that reduce their susceptibility to predators. Sequestration of of the neotropical butterfly, Morpho peleides limpida (Lepidoptera: Morphidae). J. defense compounds from larval host plants may require particular physiological N.Y. Entomol. Soc. 80:66-82. adaptations by larvae to ingest, accumulate, and store those compounds (Brattsten D.R., and Smith, W. K. 1979. Influence of sunflecks on the temperature and water 1986; Bowers 1992). In addition, unpalatable caterpillar species may be mimicked relations of two subalDine understory congeners. Oecologia 43: 195-205. palatable caterpillar species, and the presence of varying proportions of palat­ able look-alikes could affect the efficacy of aposematism, and the population dynamics of both model and mimic. Conspicuously colored, unpalatable insects have been referred to as warningly 331 332 I Bowers Aposematic Caterpillars ! 333 colored or aposematic. The terms warning coloration and aposematism are often Table 10.1. Families of Lepidoptera That Have Species with Stinging or Irritating a used synonymously, but their meanings are quite different. The term aposematic Hairs or Spines and the Life Stage in Which the Defense Occurs was first defined by Poulton (1890) as "an appearance which warns off enemies Family Life stage because it denotes something unpleasant or dangerous, or which directs the Anthelidae Larvae attention of an enemy to some specially defended or merely non-vital part, or Arctiidae Larvae which warns off other individuals of the same species" (Poulton 1890, table Eupterotidae Larvae (common) and adults (rare) following p. 338). Current appropriate usage of the term aposematic employs the Lasiocampidae Larvae first part ofPoulton's definition ("an appearance which warns offenemies because Limacodidae Larvae it denotes something unpleasant or dangerous"), and thus links an unpleasant or Lymantriidae Larvae (common) and adults (rare) Megalopygidae Larvae toxic quality of a prey (unpalatability) with an advertisement of this feature Noctuidae Larvae (warning coloration). It is this definition that is used in this chapter. The term Nolidae Larvae warning coloration refers to coloration that enhances the conspicuousness of an Nymphalidae Larvae individual. A conspicuously colored animal is therefore not necessarily apose­ Satumiidae Larvae (common) and adults (rare) matico For example, a brightly colored mimic may be said to exhibit warning Thaumetopoedae Larvae Zygaenidae Larvae coloration, but because it is palatable, it is not aposematic. Unpalatability is used in this chapter to refer to a noxious taste or odor that facilitates rejection by aFrom Kawamoto and Kumuda (1984). predators (Brower 1984). Prior to Poulton (1890) defining aposematism, Charles Darwin had considered biology, to suggest some questions that remain in the study of unpalatable aposematic caterpillars to be an enigma in his investigation of bright coloration caterpillars, and to indicate where future research in these areas may take us. in animals, which he explained as important in courtship, and thus reproductive success (Darwin 1878). Because caterpillars are the immature stages of Lepido­ ptera, and thus do not reproduce, brightly colored larvae did not fit with Darwin's Mechanisms of Unpalatability and Their Consequences theory. Puzzled, Darwin asked Alfred Russell Wallace if he could suggest any explanation, and Wallace hypothesized that these caterpillars were protected by Unpalatability in caterpillars may be due to any of several mechanisms: a nauseous taste or smell and that they advertised this by their bright colors stinging or irritating hairs or spines, (2) osmeteria and other eversible glands, (3) (Wallace 1867, pp. 146--148 in Marchant 1975). Darwin responded very posi­ regurgitation, (4) presence of toxic leaf material in the gut, and (5) sequestration tively to Wallace's suggestion: "You are the man to apply to in a difficulty. I of phytochemicals from the host plant. Use of a particular mode of defense by never heard anything more ingenious than your suggestion, and I hope you may aposematic caterpillars may have consequences for their foraging behavior, as be able to prove it true" (Darwin 1867, p. 148 in Marchant 1975). This exchange well as for their life history patterns in general. In addition, there may be costs sparked several investigators to perform feeding trials with many different species (as well as the benefit of predator deterrence) to the employment of certain of caterpillars (Poulton 1890 and references therein), and these trials showed that, defenses instead of others. indeed, brightly colored caterpillars were usually rejected by potential predators. We have progressed a long way since Darwin and Poulton began writing about Urticating Hairs and Spines warning coloration and unpalatability in caterpillars (and other insects). For example, experiments by many researchers have shown that some species of Urticating (irritating), stinging, or venomous hairs are found on the larvae of Lepidoptera are unpalatable, and that this unpalatability protects them against many species of Lepidoptera. Twelve families of moths and one family of potential predators. In addition, advances in analytical chemical techniques have butterflies have been reported to have representatives with such hairs or spines permitted isolation, identification, and quantification of chemical compounds (Maschwitz and Kloft 1971; Pesce and Delgado 1971; Kawamoto and Kumada, involved in unpalatability ofmany insect species. The evolution ofunpalatability, 1984) (Table 10.1). Poisoning by these caterpillars is called "erucism" (from the warning coloration, and mimicry has been addressed from both theoretical and Latin "eruca" for caterpillar), or "lepidopterism." Reactions to these hairs by empirical perspectives. The goal of this chapter is to examine the
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