Abstract
Chrysomelid larvae of the subfamily Galerucinae, tribe Galerucini, are known to contain 1,8-dihydroxylated 9,10-anthraquinones. Since nonhydroxylated 9,10-anthraquinone is the active agent in several commercial products sold to protect seeds against birds, we suggested that the naturally occurring dihydroxylated anthraquinones of galerucine larvae may also act as protective devices against bird predation. Tits (Parus spp.) are potential predators of larvae of the tansy leaf beetle, Galeruca tanaceti, and the elm leaf beetle, Xanthogaleruca luteola. To investigate the palatability of these chrysomelid larvae to birds, we offered them with mealworms and Calliphora pupae, respectively, as controls in dual choice bioassays to eight singly kept, naive tits (five P. major and three P. ater individuals). The bioassays were limited to 5 days, during which larvae were offered daily for 2 h (X. luteola) and 3 h (G. tanaceti), respectively. Every day, the birds significantly avoided uptake of G. tanaceti and X. luteola. More than 98% of the control food was consumed daily, whereas the percentage of chrysomelid larvae totally eaten never surpassed 6.6% for G. tanaceti and 51.8% for X. luteola. In order to determine whether this avoidance was due to the anthraquinones of the chrysomelid larvae, mealworms and Calliphora pupae, respectively, were treated with these compounds in concentrations equivalent to the natural ones. Dual choice bioassays with treated and untreated prey were conducted, again for 5 days with a daily 2- or 3-h test period, respectively. The tits ate all or nearly all treated and untreated food items every day. However, during the 5-day test period the tits learnt to take up the control insects significantly earlier than the treated ones; the food containing anthraquinones was not consumed as readily as the control, which suggest aversive learning based on distastefulness. The efficiency of anthraquinones in protecting galerucine larvae against bird predation is discussed with special respect to learning behavior and factors which might delay or mask learning of avoidance.
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References
Begossi A, Benson WW (1988) Host plants and defense mechanisms in Oedionychina (Alticinae). In: Jolivet P, Petitpierre E, Hsiao TH (eds) Biology of Chrysomelidae. Kluwer Academic, Dordrecht, pp 57–71
Bowers MD, Farley S (1990) The behaviour of grey jays, Perisoreus canadensis, towards palatable and unpalatable Lepidoptera. Anim Behav 39: 699–705
Brower LP, Nelson CJ, Seiber JN, Fink LS, Bond C (1988) Exaptation as an alternative to coevolution in the cardenolide-based chemical defense of monarch butterflies (Danaus plexippus L.) against avian predators. In: Spencer KC (ed) Chemical mediation of coevolution. Academic Press, San Diego, pp 447–476
Coppinger RP (1969). The effect of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. Part I: Reactions of wild-caught adult blue jays to novel insects. Behavior 35: 45–60
Daloze D, Braekman JC, Pasteels JM (1986) A toxic dipentide from the defense glands of the Colorado beetle. Science 233: 221–223
Evans DL, Schmidt JO (1990) Insect defenses. Adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany
Goodwin TW (1971) Pigments — Arthropoda. In: Florkin M, Scheer BT (eds) Chemical zoology, vol. VI, Arthropoda Part B. Academic Press, New York, pp 279–306
Hilker M (1992) Protective devices of early developmental stages in Pyrrhalta viburni (Coleoptera, Chrysomelidae). Oecologia 92: 71–75
Hilker M, Schulz S (1991) Anthraquinones in different developmental stages of Galeruca tanaceti (Coleoptera, Chrysomelidae). J Chem Ecol 17: 2323–2332
Hilker M, Eschbach U, Dettner K (1992) Occurrence of anthraquinones in eggs and larvae of several Galerucinae (Coleoptera: Chrysomelidae). Naturwissenschaften 79: 271–274
Hough-Goldstein JA, Geiger J, Chang D, Saylor W (1993) Palatability and toxicity of the Colorado potato beetle (Coleoptera: Chrysomelidae) to domestic chickens. Ann Entomol Soc Am 86: 158–164
Howard DF, Phillips DW, Jones TH, Blum MS (1982) Anthraquinones and anthrones: occurrence and defensive function in a Chrysomelid beetle. Naturwissenschaften 69:91–92
Hsiao TH, Fraenkel G (1969) Properties of leptinotarsin a toxic hemoplymph protein from the Colorado potato beetle. Toxicon 7: 119–130
Kayser H (1985) Pigments. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 10. Pergamon Press, Oxford, pp 367–415
Kimoto SH (1989) Chrysomelidae of Thailand, Cambodia, Laos, and Vietnam. IV. Galerucinae. Esakia 27: 1–241
Kippenberg H (1994) Chrysomelidae. In: Lohse GA, Lucht WH (eds) Die Käfer Mitteleuropas, vol 14. Goecke&Evers, Krefeld, pp 17–91
Kristín A (1989) Bedeutung von Lepidoptera in Vogelnahrung. Pr Slov Entomol Spol SAV Bratislava 7: 227–232
Marples NM (1993) Toxicity assay of ladybirds using natural predators. Chemoecology 4: 33–38
Mason JR, Neal J, Oliver JE, Lusby WR (1991) Bird repellent properties of secretions from nymphs of the azalea lace bug. Ecol Appl 1: 226–230
Meier M (1978) Das Gimpelproblem. Schweiz Z Obst-Weinbau 114: 209–213
Pasteels JM, Grégoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28: 263–289
Rowell-Rahier M, Pasteels JM, Alonso-Mejia A, Brower LP (1994) Relative unpalatability of leaf-beetles with either biosynthesized or sequestered chemical defense. Anim Behavior (in press)
SAS (1988) SAS/STAT guide for personal computers, version 6.03. SAS Institute, Cary
Schuler W (1980) Zum Meidenlernen ungenießbarer Beute bei Vögeln: der Einfluß der Faktoren Umlernen, neue Alternativbeute und Ähnlichkeit der Alternativbeute. Z Tierpsychol 54: 105–143
Schuler W (1990) Avian predatory behavior and prey distribution. In: Evan DL, Schmidt JO (eds) Insect defenses. Adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 151–172
Schuler W, Hesse E (1985) On the function of warning coloration: a black and yellow pattern inhibits prey-attack by naive domestic chicks. Behav Ecol Sociobiol 16: 249–255
Thomson RH (1987) Naturally occurring quinones. III. Recent advances. Chapman and Hall, London
Thorpe WH (1963) Learning and instinct in animals. Methuen, London
Tinbergen L (1960) The natural control of insects in pine woods. Arch Neerl Zool 13: 265–343
Whelan CJ, Holmes RT, Smith HR (1989) Bird predation on gypsy moth (Lepidoptera: Lymantriidae) larvae: an aviary study. Environ Entomol 18: 43–45
Zbinden W (1976) Knospenschäden verursacht durch den Gimpel (Dompfaff). Schweiz Zv Obst-Weinbau 112:42–45
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Hilker, M., Köpf, A. Evaluation of the palatability of chrysomelid larvae containing anthraquinones to birds. Oecologia 100, 421–429 (1994). https://doi.org/10.1007/BF00317864
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DOI: https://doi.org/10.1007/BF00317864