All Title Author
Keywords Abstract

PLOS ONE  2009 

Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars

DOI: 10.1371/journal.pone.0004796

Full-Text   Cite this paper   Add to My Lib


Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory.


[1]  Hutchings MR, Judge J, Gordon IJ, Athanasiadou S, Kyriazakis I (2006) Use of trade-off theory to advance understanding of herbivore-parasite interactions. Mammal Rev. 36: 1–16.
[2]  Janzen DH (1978) Complications in interpreting the chemical defense of trees against tropical arboreal plant-eating vertebrates. In: Montgomery GG, editor. The ecology of arboreal folivores. Washington: Smithsonian Institution Press. pp. 73–84.
[3]  Huffman MA (2003) Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants. Proc. Nutrit. Soc. 62: 371–381.
[4]  Huffman MA (2001) Self-medicative behavior in the African great apes: an evolutionary perspective into the origins of human traditional medicine. Bioscience 51: 651–661.
[5]  Huffman MA (1997) Current evidence for self-medication in primates: A multidisciplinary perspective. Yrbk. Phys. Anthro. 40: 171–200.
[6]  Lozano GA (1998) Parasitic stress and self-medication in wild animals. Adv. Stud. Behav. 27: 291–317.
[7]  Hutchings MR, Athanasiadou S, Kyriazakis I, Gordon IJ (2003) Can animals use foraging behaviour to combat parasites? Proc. Nutrit. Soc. 62: 361–370.
[8]  Wrangham RW, Nishida T (1983) Aspilia spp. leaves: A puzzle in the feeding behavior of wild chimpanzees. Primates 24: 276–282.
[9]  Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67: 169–176.
[10]  Clark L, Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77: 174–180.
[11]  Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M (2003) Evidence for collective medication in ants. Ecol. Lett. 6: 19–22.
[12]  Krishnamani R, Mahaney WC (2000) Geophagy among primates: adaptive significance and ecological consequences. Anim. Behav. 59: 899–915.
[13]  Engel C (2002) Wild health. London: Weidenfeld and Nicholson.
[14]  Wrangham RW (1995) Relationship of chimpanzee leaf-swallowing to a tapeworm infection. Am. J. Primatol. 37: 297–303.
[15]  Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, Towers GHN (1996) Leaf-swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections. Int. J. Primatol. 17: 475–503.
[16]  Huffman MA, Caton JM (2001) Self-induced increase of gut motility and the control of parasite infections in wild chimpanzees. Int. J. Primatol. 22: 329–346.
[17]  Villalba JJ, Provenza FD, Shaw R (2006) Sheep self-medicate when challenged with illness-inducing foods. Anim. Behav. 71: 1131–1139.
[18]  Bernays EA, Chapman RF, Hartmann T (2002) A taste receptor neurone dedicated to the perception of pyrrolizidine alkaloids in the medial galeal sensillum of two polyphagous arctiid caterpillars. Physiol. Entomol. 27: 312–321.
[19]  Boppré M (1984) Redefining “pharmacophagy.” J. Chem. Ecol. 10: 1151–1154.
[20]  Hartmann T, Theuring C, Beuerle T, Ernst L, Singer MS, Bernays EA (2004) Acquired and partially de novo synthesized pyrrolizidine alkaloids in two polyphagous arctiids and the alkaloid profiles of their larval food-plants. J. Chem. Ecol. 30: 229–254.
[21]  Hartmann T, Theuring C, Beuerle T, Bernays EA, Singer MS (2005) Acquisition, transformation and maintenance of plant pyrrolizidine alkaloids by the polyphagous arctiid Grammia geneura. Insect Biochem. Mol. Biol. 35: 1083–1099.
[22]  Singer MS, Carrière Y, Theuring C, Hartmann T (2004) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Am. Nat. 164: 423–429.
[23]  Stireman JO III, Singer MS (2002) Spatial and temporal variation in the parasitoid assemblage of an exophytic polyphagous caterpillar. Ecol. Entomol. 27: 588–600.
[24]  Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. Lond. B 273: 823–829.
[25]  Singer MS, Stireman JO III (2003) Does anti-parasitoid defense explain host-plant selection by a polyphagous caterpillar? Oikos 100: 554–562.
[26]  Dyer LA, Dodson CD, Stireman JO III, Tobler MA, Smilanich AM, Fincher RM, Letourneau DK (2003) Synergistic effects of three Piper amides on generalist and specialist herbivores. J. Chem. Ecol. 29: 2499–2514.
[27]  Hunter MD (2003) Effects of plant quality on the population ecology of parasitoids. Agric. For. Entomol. 5: 1–8.
[28]  Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51: 163–185.
[29]  Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock J, Harvey JA (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J. Chem. Ecol. 34: 132–143.
[30]  Lampert EC, Zangerl AR, Berenbaum MR, Ode PJ (2008) Tritrophic effects of xanthotoxin on the polyembryonic parasitoid Copidosoma sosares (Hymenoptera: Encyrtidae). J. Chem. Ecol. 34: 783–790.
[31]  Smilanich AM (2008) Variation in plant chemical defense and the physiological response of specialist and generalist herbivores. Tulane University. PhD thesis.
[32]  Eisner T (2003) For love of insects. Cambridge: Belknap Press.
[33]  Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton: Princeton University Press.
[34]  Hawkins BA (1994) Pattern and process in host-parasitoid Interactions. London: Cambridge University Press.
[35]  Mooney KA, Agrawal AA Tilmon KJ, editor. (2007) Phenotypic plasticity. Specialization, speciation, and radiation Berkeley: University of California Press. 43–57.
[36]  Karban R, English-Loeb G (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78: 603–611.
[37]  Chapuisat M, Oppliger A, Magliano P, Christe P (2007) Wood ants use resin to protect themselves against pathogens. Proc. R. Soc. London B 274: 2013–2017.
[38]  Rodriguez E, Wrangham R (1993) Zoopharmacognosy: The use of medicinal plants by animals. In: Downum KR, Romeo JT, Stafford H, editors. Recent Advances in Phytochemistry, vol. 27: Phytochemical potential of tropical plants. pp. 89–105.
[39]  Huffman MA, Hirata S (2004) An experimental study of leaf-swallowing in captive chimpanzees: insights into the origin of a self-medicative behavior and the role of social learning. Primates 45: 113–118.
[40]  Bernays EA, Singer MS (2005) Taste alteration and endoparasites. Nature 436: 476.
[41]  Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611–643.
[42]  Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu. Rev. Entomol. 48: 455–484.
[43]  Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294: 321–326.
[44]  Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu. Rev. Ecol. Evol. Syst. 35: 651–673.
[45]  Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol. Evol. 20: 685–692.
[46]  Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J. Exp. Biol. 209: 2377–2383.
[47]  Agrawal AA, et al. (2007) Filling key gaps in population and community ecology. Front. Ecol. Environ. 5: 145–152.
[48]  Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol. Lett. 7: 153–163.
[49]  Yamamoto RT (1969) Mass rearing of the tobacco hornworm II. Larval rearing and pupation. J. Econ. Entomol. 62: 1427–1431.
[50]  SAS Institute (2007) JMP version 7.0. (SAS Institute. Cary, NC).
[51]  Berenbaum MR, Zangerl AR (1992) Genetics of physiological and behavioural resistance to host furanocoumarins in the parsnip webworm. Evolution 46: 1373–1384.


comments powered by Disqus