Skip to main content
Log in

Hiding in Plain Sight: Cuticular Compound Profile Matching Conceals a Larval Tortoise Beetle in its Host Chemical Cloud

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Larvae of tortoise beetles are postulated to have fecal shields as the main defensive strategy against predators. Such a device protects beetles both physically and chemically. In order to examine how larvae Chelymorpha reimoseri are protected against predatory ants, which frequently visit extrafloral nectaries in their host plant, the morning glory Ipomoea carnea, we conducted anti-predation bioassays with live 5th instars. In the field, larvae in contact with ants had survival between 40 and 73 %, independently of shield presence. In the laboratory, when exposed to Camponotus crassus, larvae with shields had significantly higher survival (85 %) than those without shields (64 %). In both scenarios, larval survival was significantly higher when compared with palatable Spodoptera frugiperda larvae, as the latter were all consumed. We also observed that when C. reimoseri larvae showed no movement, the ants walked on them without attacking. We hypothesized that if the larval integument has a pattern of cuticular compounds (CCs) similar to that of its host plant, larvae would be rendered chemically camouflaged. In the field and laboratory, the freeze-dried palatable larvae of S. frugiperda treated with CCs of 5th instar C. reimoseri and left on I. carnea leaves were significantly less removed by ants than controls without these compounds. We also found a similarity of approximately 50 % between the CCs in C. reimoseri larvae and I. carnea host leaves. Both findings provide evidence in support of the hypothesis that chemical camouflage plays an important role in larval defense, which is reported for the first time in an ectophagous leaf beetle larva.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akino T (2005) Chemical and behavioral study on the phytomimetic giant geometer Biston robustum Butler (Lepidoptera: Geometridae). Appl Entomol Zool 40:497–505

    Article  Google Scholar 

  • Akino T (2008) Chemical strategies to deal with ants: a review of mimicry, camouflage, propaganda and phytomimesis by ants (Hymenoptera: Formicidae) and other arthropods. Myrmecol News 11:173–181

    Google Scholar 

  • Akino T, Nakamura K-I, Wakamura S (2004) Diet induced chemical phyomimesis by twig-like caterpillars of Biston robustum Butler (Lepidoptera: Geometridae). Chemoecology 14:165–174

    Article  CAS  Google Scholar 

  • Austin D, Huáman Z (1996) A synopsis of Ipomoea (Convolvulaceae) in the Americas. Taxon 45:3–38

    Article  Google Scholar 

  • Bacher S, Luder S (2005) Picky predators and the function of the faecal shield of a cassidine larva. Funct Ecol 19:263–272

    Article  Google Scholar 

  • Bachmann AO, Cabrera N (2010) A catalog of the types of Chrysomelidae sensu lato (Insecta, Coleoptera, Polyphaga) deposited in the Museo Argentino de Ciencias Naturales, Buenos Aires. Rev Mus Argent Cienc Nat 12:57–80

    Google Scholar 

  • Borowiec L (1999) World catalogue of Cassidinae (Coleoptera:Chrysomelidae). Biologica Silesiae, Wroclaw

    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 

  • Budzikiewicz H, Djerassi C, Williams DH (1967) Mass spectrometry of organic compounds. Holden-Day Inc, San Francisco

    Google Scholar 

  • Carlson DA, Roan C-S, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571

    Article  CAS  Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865

    Article  CAS  Google Scholar 

  • Chaboo CS (2007) Biology and phylogeny of the Cassidinae (tortoise and leaf-mining beetles) (Coleoptera: Chrysomelidae). Bull Am Mus Nat Hist 305:1–250

    Article  Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972

    Article  CAS  PubMed  Google Scholar 

  • Eisner T, Tassel E, Carrel JE (1967) Defensive use of ‘fecal shield’ by a beetle larva. Science 158:1471–1473

    Article  CAS  PubMed  Google Scholar 

  • Fernández F (2003) Introducción a las hormigas de la región Neotropical. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá

  • Gomes CCG, Trigo JR, Eiras AE (2008) Sex pheromone of the American warble fly, Dermatobia hominis: the role of cuticular hydrocarbons. J Chem Ecol 34:636–646

    Article  Google Scholar 

  • Guimarães PR, Raimundo RLG, Bottcher C, Silva RR, Trigo JR (2006) Extrafloral nectaries as a deterrent mechanism against seed predators in the chemically defended weed Crotalaria pallida (Leguminosae). Austral Ecol 31:776–782

    Article  Google Scholar 

  • Haase R (1999) Seasonal growth of “algodão-bravo” (Ipomoea carnea spp. fistulosa). Pesq Agrop Brasileira 34:159–163

    Article  Google Scholar 

  • Haraguchi M, Gorniak SL, Ikeda K, Minami Y, Kato A, Watson AA, Nash RJ, Molyneux RJ, Asano N (2003) Alkaloidal components in the poisonous plant, Ipomoea carnea (Convolvulaceae). J Agric Food Chem 51:4995–5000

    Article  CAS  PubMed  Google Scholar 

  • Heckman CW (1998) The Pantanal of Poconé. Biota and ecology in the northern section of the world’s largest pristine wetland. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: Chemistry, biochemistry and biology. University of Nebraska Press, Lincoln, pp 179–226

    Google Scholar 

  • Krebs CJ (1999) Ecological methodology. Addison-Wesley Educational, Menlo Park

    Google Scholar 

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

    Google Scholar 

  • Labandeira CC (2002) The history of associations between plants and animals. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions. An evolutionary approach. Blackwell Science, Oxford, pp 26–74

    Google Scholar 

  • Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603

    Article  PubMed  Google Scholar 

  • Mccullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, London

    Book  Google Scholar 

  • Menéndez RD, Marrero D, Más R, Fernández I, González L, González RM (2005) In vitro and in vivo study of octacosanol metabolism. Arch Med Res 36:113–119

    Article  PubMed  Google Scholar 

  • Müller C, Hilker M (1999) Unexpected reactions of a generalist predator towards defensive devices of cassidine larvae (Coleoptera, Chrysomelidae). Oecologia 118:166–172

    Article  Google Scholar 

  • Müller C, Hilker M (2004) Ecological relevance of fecal matter in Chrysomelidae. In: Jolivet PH, Santiago-Blay JA, Schmitt M (eds) New contributions to the biology of Chrysomelidae. SPC Academic Publishers, The Hague, pp 693–705

    Google Scholar 

  • Nelson DR, Sukkestad DR, Zaylskie RG (1972) Mass spectra of methyl-branched hydrocarbons from eggs of the tobacco hornworm. J Lipid Res 13:413–421

    CAS  PubMed  Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92

    Article  CAS  PubMed  Google Scholar 

  • Nogueira-de-Sá F (2004) Defesas de larvas de Plagiometriona flavescens e Stolas areolata (Coleoptera: Chrysomelidae: Cassidinae) contra predadores. Ph.D. Thesis. Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Brasil

  • Nogueira-de-Sá F, Trigo JR (2005) Faecal shield of the tortoise beetle Plagiometriona aff. flavescens (Chrysomelidae: Cassidinae) as chemically mediated defence against predators. J Trop Ecol 21:189–194

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Piskorski R, Trematerra P, Dorn S (2010) Cuticular hydrocarbon profiles of codling moth larvae, Cydia pomonella (Lepidoptera: Tortricidae), reflect those of their host plant species. Biol J Linn Soc 101:376–384

    Article  Google Scholar 

  • Portugal AHA, Trigo JR (2005) Similarity of cuticular lipids between a caterpillar and its host plant: a way to make prey undetectable for predatory ants? J Chem Ecol 31:2551–2561

    Article  PubMed  Google Scholar 

  • Price PW, Denno RF, Eubanks MD, Finke DL (2011) Insect ecology: Behavior, populations and communities. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rowe C, Halpin C (2013) Why are warning displays multimodal? Behav Ecol Sociobiol 67:1425–1439

    Article  Google Scholar 

  • Ruxton GD (2009) Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than vision. Phil Trans R Soc B 364:549–557

    Article  PubMed Central  PubMed  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. Oxford University Press, New York

    Book  Google Scholar 

  • Silveira HCP, Oliveira PS, Trigo JR (2010) Attracting predators without falling prey: chemical camouflage protects honeydew-producing treehoppers from ant predation. Am Nat 175:261–268

    Article  PubMed  Google Scholar 

  • Statsoft, Inc. (2004) Statistica (data analysis software system), version 7. www.statsoft.com

  • Steward JL, Keeler KH (1988) Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)? Oikos 53:79–86

    Article  Google Scholar 

  • Świętojańska J (2009) The immatures of tortoise beetles with bibliographic catalogue of all taxa (Coleoptera: Chrysomelidae: Cassidinae). Polish Taxonomical Monographs vol. 16. Biologica Silesiae, Wrocław

    Google Scholar 

  • van den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr 11:463–471

    Article  Google Scholar 

  • Vane-Wright RI (1976) An unified classification of mimetic resemblances. Biol J Linn Soc 8:25–56

    Article  Google Scholar 

  • Vasconcellos-Neto J (1988) Genetics of Chelymorpha cribraria, Cassidinae: Colour patterns and their ecological meaning. In: Jolivet PH, Petitpierre E, Hsiao TH (eds) Biology of chrysomelidae. Kluwer Academic Publishers, Dordrecht, pp 217–232

    Chapter  Google Scholar 

  • Vasconcellos-Neto J, Jolivet PH (1988) Une nouvelle stratégie de défense: la stratégie de défense annulaire (cycloalexie) chez quelquez larves de Chrysomélides brésiliens. Bull Soc Entomol Fr 92:291–299

    Google Scholar 

  • Vencl FV, Srygley RB (2013) Enemy targeting, trade-offs, and the evolutionary assembly of a tortoise beetle defense arsenal. Evol Ecol 27:237–252

    Article  Google Scholar 

  • Vencl FV, Nogueira-de-Sá F, Allen BJ, Windsor DM, Futuyma DJ (2005) Dietary specialization influences the efficacy of larval tortoise beetle shield defenses. Oecologia 145:404–414

    Article  PubMed  Google Scholar 

  • Vencl FV, Gómez NE, Ploss K, Boland W (2009) The chlorophyll catabolite, pheophorbide a, confers predation resistance in a larval tortoise beetle shield defense. J Chem Ecol 35:281–288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vencl FV, Trillo PA, Geeta R (2011) Functional interactions among tortoise beetle larval defenses reveal trait suites and escalation. Behav Ecol Sociobiol 65:227–239

    Article  Google Scholar 

  • Walters DW (2011) Plant defense: Warding off attack by pathogens, herbivores, and parasitic plants. Blackwell Publishing, Oxford

    Google Scholar 

Download references

Acknowledgments

This work is part of KFM’s Dr. Sc. thesis and was funded by grants from FAPESP (2008/04241-4). JRT acknowledges grants from FAPESP (2011/17708-0) and CNPq (2009/304473-0). José Carlos da Silva and Claudia Bottcher kindly assisted with the fieldwork reported in this study. Sebastian Sendoya helped with ant identification. We thank Daniela Rodrigues, Adriano Cavalleri, Flávia Nogueira de Sá and two anonymous reviewers for their comments on the early draft of this manuscript. We are thankful with UFMS for permission to work at Base de Estudos do Pantanal.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Roberto Trigo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Massuda, K.F., Trigo, J.R. Hiding in Plain Sight: Cuticular Compound Profile Matching Conceals a Larval Tortoise Beetle in its Host Chemical Cloud. J Chem Ecol 40, 341–354 (2014). https://doi.org/10.1007/s10886-014-0424-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0424-2

Keywords

Navigation