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Are Aristolochic Acids Responsible for the Chemical Defence of Aposematic Larvae of Battus polydamas (L.) (Lepidoptera: Papilionidae)?

  • Ecology, Behavior and Bionomics
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Abstract

Aristolochic acids (AAs) are thought to be responsible for the chemical protection of the aposematic larvae Battus polydamas (L.) (Papilionidae: Troidini) against predators. These compounds are sequestered by larvae from their Aristolochia (Aristolochiaceae) host plants. Studying the role of the chemical protection of the second and fifth instars of B. polydamas against potential predators, we found that the consumption of larvae by the carpenter ant Camponotus crassus Mayr and young chicks Gallus gallus domesticus was dependent on larval developmental stage. Second instars were more preyed upon than fifth instars; however, the assassin bug Montina confusa Stål was not deterred by chemical defences of the fifth instar B. polydamas. Laboratory bioassays with carpenter ants and young chicks using palatable baits topically treated with a pure commercial mixture of AAs I and AAs II in concentrations up to 100 times those previously found in B. polydamas larvae showed no activity. Similar results were found in field bioassays, where palatable baits treated as above were exposed to the guild of predators that attack B. polydamas larvae and were also consumed irrespective of the commercial AA concentration used. These results suggest that the mixture of AAs I and AAs II have no defensive role against predators, at least against those investigated in the present work. Other compounds present in Aristolochia host plants such as O-glycosylated AAs; benzylisoquinoline alkaloids; and mono-, sesqui-, di-, and triterpenes, which can be sequestered by Troidini, could act as deterrents against predators.

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References

  • Arab A, Trigo JR, Lourenção AL, Peixoto AM, Ramos F, Bento JMS (2007) Differential attractiveness of potato tuber volatiles to Phthorimaea operculella (Gelechiidae) and the predator Orius insidiosus (Anthocoridae). J Chem Ecol 33:1845–1855

    Article  PubMed  CAS  Google Scholar 

  • Bottcher A, Zolin JP, Nogueira-de-Sá F, Trigo JR (2009) Faecal shield chemical defence is not important in larvae of the tortoise beetle Chelymorpha reimoseri (Chrysomelidae: Cassidinae: Stolaini). Chemoecology 19:63–66

    Article  Google Scholar 

  • Bowers MD (1991) The iridoid glycosides. In: Rosenthal G (ed) Herbivores; their interactions with secondary plant metabolites, vol 1, The chemical participants. Academic, New York, pp 297–325

    Chapter  Google Scholar 

  • Brower JVZ (1958) Experimental studies of mimicry in some north American butterflies. Part II. Battus philenor and Papilio troilus, P. polyxenes and P. glaucus. Evolution 12:123–136

    Article  Google Scholar 

  • Brower LP, Brower JVZ (1964) Birds, butterflies, and plant poisons: a study in ecological chemistry. Zoologica 49:137–159

    CAS  Google Scholar 

  • Brower LP, Nelson CJ, Seiber JN, Fink LS, Bond C (1988) Exaptation as an alternative to coevolution in cardenolide-based chemical defence of monarch butterflies (Danaus plexippus L.) against avian predators. In: Spencer KC (ed) Chemical mediation of coevolution. Academic, New York, pp 447–475

    Google Scholar 

  • Brown KS, Damman AJ, Feeny P (1981) Troidini swallowtails (Lepidoptera: Papilionidae) in south eastern Brazil: natural history and foodplant relationships. J Res Lep 19:199–266

    Google Scholar 

  • Carrell JE (2001) Response of predaceous arthropods to chemically defended larvae of the pyralid moth Uresiphita reversalis (Guenee) (Lepidoptera: Pyralidae). J Kansas Entomol Soc 74:128–135

    Google Scholar 

  • Chai P (1986) Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rain forest. Biol J Linn Soc 29:161–189

    Article  Google Scholar 

  • Codella SG, Lederhouse RC (1989) Intersexual comparison of mimetic protection in the black swallowtail butterfly, Papilio polyxenes: experiments with captive blue jay predators. Evolution 43:410–420

    Article  Google Scholar 

  • Durán J, Fagua G, Robles J, Gil E (2012) Sequestration of aristolochic acid I from Aristolochia pilosa by Mapeta xanthomelas Walker, 1863. J Chem Ecol 38:1285–1288

    Article  PubMed  Google Scholar 

  • Dyer LA (1995) Tasty generalists and nasty specialists? Antipredator mechanisms in tropical lepidopteran larvae. Ecology 76:1483–1496

    Article  Google Scholar 

  • Dyer LA, Bowers MD (1996) The importance of sequestered iridoid glycosides as a defence against an ant predator. J Chem Ecol 22:1527–1539

    Article  CAS  Google Scholar 

  • Dyer LA, Floyd T (1993) Determinants of predation on phytophagous insects: the importance of diet breadth. Oecologia 96:575–582

    Article  Google Scholar 

  • Egelhaaf A, Cölln K, Schmitz B, Buck M, Wink M, Schneider D (1990) Organ specific storage of dietary pyrrolizidine alkaloids in the arctiid moth Creatonotos transiens. Z Naturforsch 45c: 115–120

    Google Scholar 

  • Engler-Chaouat HS, Gilbert LE (2007) De novo synthesis vs. sequestration: negatively correlated metabolic traits and the evolution of host plant specialization in cyanogenic butterflies. J Chem Ecol 33:25–42

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich, Raven (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Ferro VG, Guimarães PR, Trigo JR (2006) Why do larvae of Utetheisa ornatrix penetrate and feed in pods of Crotalaria species? Larval performance vs. chemical and physical constraints. Entomol Exp Appl 121:23–29

    Article  Google Scholar 

  • Floren A, Biun A, Linsenmair KE (2002) Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia 131:137–144

    Article  Google Scholar 

  • Glendinning JI, Brower LP, Montgomery CA (1990) Responses of three mouse species to deterrent chemicals in monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline. Chemoecology 1:114–123

    Article  CAS  Google Scholar 

  • Houghgoldstein 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

    Google Scholar 

  • Janz N (2011) Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Ann Rev Ecol Evol Syst 42:71–89

    Article  Google Scholar 

  • Klitzke CF, Brown KS (2000) The occurrence of aristolochic acids in neotropical troidine swallowtails (Lepidoptera: Papilionidae). Chemoecology 10:99–102

    Article  CAS  Google Scholar 

  • Kusnezov N (1951) El género Camponotus en la Argentina. Acta Zool Lilloana 11:183–255

    Google Scholar 

  • Massuda KF, Trigo JR (2009) Chemical defence of the warningly coloured Methona themisto caterpillar (Lepidoptera: Nymphalidae: Ithomiinae). Eur J Entomol 106:253–259

    Google Scholar 

  • Mebs D, Schneider M (2002) Aristolochic acid content of South-East Asian troidine swallowtails (Lepidoptera: Papilionidae) and of Aristolochia plant species (Aristolochiaceae). Chemoecology 12:11–13

    Article  CAS  Google Scholar 

  • Morais ABB (1997) Interações tritróficas no sistema Aristolochia arcuata (Aristolochiaceae), Battus polydamas (Lepidoptera: Papilionidae: Troidini), e alguns de seus inimigos naturais. Dr Sc. Thesis, Universidade Estadual de Campinas, Campinas, São Paulo, Brasil, p 138

  • Morais ABB, Brown KS (1991) Larval foodplant and other effects on troidine guild composition (Papilionidae) in south eastern Brazil. J Res Lep 30:19–37

    Google Scholar 

  • Müller C, Agerbirk N, Olsen CE, Boeve JL, Schaffner U, Brakefield PM (2001) Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J Chem Ecol 27:2505–2516

    Article  PubMed  Google Scholar 

  • Nishida R, Fukami H (1989) Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous, to aristolochic acids. J Chem Ecol 15:2549–2563

    Article  CAS  Google Scholar 

  • Oliveira PS, Silva AF, Martins AB (1987) Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents. Oecologia 74:228–230

    Article  Google Scholar 

  • Ômura H, Honda K, Feeny P (2006) From terpenoids to aliphatic acids: further evidence for late-instar switch in osmeterial defense as a characteristic trait of swallowtail butterflies in the tribe Papilionini. J Chem Ecol 32:1999–2012

    Article  PubMed  Google Scholar 

  • Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154

    Article  CAS  Google Scholar 

  • Opitz SEW, Boevé J-L, Nagy ZT, Sonet G, Koch F, Müller C (2012) Host shifts from Lamiales to Brassicaceae in the sawfly genus Athalia. PLoS ONE 7:e33649. doi:10.1371/journal.pone.0033649

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro CEG (1996) Palatability and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae). Biol J Linn Soc 59:351–365

    Article  Google Scholar 

  • Pinto CF, Urzúa A, Niemeyer HM (2011) Sequestration of aristolochic acids from meridic diets by larvae of Battus polydamas archidamas (Papilionidae: Troidini). Eur J Entomol 108:41–45

    CAS  Google Scholar 

  • Platt AP, Coppinger RP, Brower LP (1971) Demonstration of the selective advantage of mimetic Limenitis butterflies presented to caged avian predators. Evolution 25:692–701

    Article  Google Scholar 

  • Priestap HA, Velandia AE, Johnson JV, Barbieri MA (2012) Secondary metabolite uptake by the Aristolochia-feeding papilionoid butterfly Battus polydamas. Biochem Syst Ecol 40:126–137

    Article  CAS  Google Scholar 

  • Ronquist F, Nylin S (1990) Process and pattern in the evolution of species associations. Syst Zool 39:323–344

    Article  Google Scholar 

  • Rossini C, Bezzerides A, González A, Eisner M, Eisner T (2003) Chemical defence: incorporation of diet-derived pyrrolizidine alkaloid into the integumental scales of a moth (Utetheisa ornatrix). Chemoecology 13:199–205

    Article  CAS  Google Scholar 

  • Rothschild M, Reichstein T, von Euw J, Aplin R, Harman RRM (1970) Toxic lepidoptera. Toxicon 8:293–299

    Article  PubMed  CAS  Google Scholar 

  • Rothschild M, Von Euw J, Reichstein T (1972) Aristolochic acids stored by Zerynthia polyxena (Lepidoptera). Insect Biochem 2:334–343

    Article  CAS  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Book  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect–plant biology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Silva KL, Trigo JR (2002) Structure–activity relationships of pyrrolizidine alkaloids in insect chemical defence against the orb-weaving spider Nephila clavipes. J Chem Ecol 28:637–648

    Article  Google Scholar 

  • Silva-Brandão KL, Solferini VN, Trigo JR (2006) Chemical and phylogenetic relationships among Aristolochia L. (Aristolochiaceae) from south eastern Brazil. Biochem Syst Ecol 34:291–302

    Article  Google Scholar 

  • Sime KR (2002) Chemical defence of Battus philenor larvae against attack by the parasitoid Trogus pennator. Ecol Entomol 27:337–345

    Article  Google Scholar 

  • Sime KR, Feeny PP, Haribal MM (2000) Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L.): evidence and ecological implications. Chemoecology 10:169–178

    Google Scholar 

  • Tullberg BS, Gamberale-Stille G, Solbreck C (2000) Effects of food plant and group size on predator defence: differences between two co-occurring aposematic Lygaeinae bugs. Ecol Entomol 25:220–225

    Article  Google Scholar 

  • Trigo JR (2000) The chemistry of antipredator defence by secondary compounds in neotropical aposematic Lepidoptera: facts, perspectives and caveats. J Braz Chem Soc 11:551–561

    Article  CAS  Google Scholar 

  • Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98

    Article  CAS  Google Scholar 

  • Tyler HA, Brown KS, Wilson K (1994) Swallowtail butterflies of the Americas. Scientific, Gainesville

    Google Scholar 

  • Urzúa A, Priestap HA (1985) Aristolochic acids from Battus polydamas. Biochem Syst Ecol 13:169–170

    Google Scholar 

  • Von Euw J, Reichstein T, Rothschild M (1968) Aristolochic acid-I in the swallowtail butterfly Pachlioptera aristolochiae (Fabr.) (Papilionidae). Israel J Chem 6:659–670

    Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New Jersey

    Google Scholar 

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Acknowledgments

We thank Fundação José Pedro de Oliveira for the permission to work in the Santa Genebra Reserve. Financial support was provided by FAPESP (98/01065-7, 11/17708-0) and CNPq (304969/2009-0) to JRT. This work is part of the Doctor Thesis of ABBM.

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Correspondence to J R Trigo.

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Edited by Stefano Colazza – Univ of Palermo

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Morais, A.B.B., Brown, K.S., Stanton, M.A. et al. Are Aristolochic Acids Responsible for the Chemical Defence of Aposematic Larvae of Battus polydamas (L.) (Lepidoptera: Papilionidae)?. Neotrop Entomol 42, 558–564 (2013). https://doi.org/10.1007/s13744-013-0163-z

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