Skip to main content
Log in

Age- and sex-related variation in defensive secretions of adult Chlaenius cordicollis and evidence for their role in sexual communication

  • Original Article
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Defensive secretions of adult Chlaenius cordicollis (Coleoptera: Carabidae) from Manitoba and Pennsylvania were analyzed across the life cycle in a multi-year study using solid phase microextraction and gas chromatography-mass spectrometry. In concurrent experiments using Y-tube olfactometry, we observed the response of each sex when male or female source beetles were induced to discharge defensive secretions. Almost all defensive secretion samples contained five alkylphenolic compounds, dominated by 3-methylphenol; frequently, two alkoxyphenolic compounds and one ester were also detected. As beetles aged, the composition of their defensive secretion shifted, showing an exponential decrease in the relative proportion of 2,3-dimethylphenol as a function of day of year. Previously reported differences observed in autumn between secretions of beetles from Manitoba and Pennsylvania are attributable to different times of onset of the decline of 2,3-dimethylphenol in the two locales. Regardless of airborne odor, responding beetles exhibited upwind anemotaxis in the olfactometer and, outside of the reproductive period, avoidance was the most frequent response to defensive secretions. Sexual dimorphism was evident in the major components of the defensive secretions during the reproductive period and resulted from an increase over time in 2,5-dimethylphenol in male beetles. In the reproductive period, neither sex avoided odor from male source beetles, females preferred clean air to odor from source females, and males were attracted to females that discharged defensive secretion but showed no preference when females had not discharged the secretion. The defensive secretion appears to function as a sex attractant during the reproductive period.

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

  • Aitchison J (1984) The mathematical analysis of geochemical compositions. Math Geol 16:531–564

    Article  CAS  Google Scholar 

  • Attygalle AB, Meinwald J, Liebherr JK, Eisner T (1991) Sexual dimorphism in the defensive secretion of a carabid beetle. Experientia 47:269–299

    Article  Google Scholar 

  • Balestrazzi E, Dazzini MLV, De Bernardi M, Vidari G, Vita-Finzi P, Mellerio G (1985) Morphological and chemical studies on the pygidial defense glands of some Carabidae (Coleoptera). Naturwissenschaften 72:482–484

    Article  Google Scholar 

  • Ballhorn DJ, Kautz S (2013) How useful are olfactometer experiments in chemical ecology research? Commun Integr Biol 6:4, e24787:1–3

  • Bell RT (1960) A revision of the genus Chlaenius Bonelli (Coleoptera, Carabidae) in North America. Misc Publ Entomol Soc Am 3:98–166

    Google Scholar 

  • Bishop YMM, Fienberg SE, Holland PW (2007) Discrete multivariate analysis: Theory and practice. MIT Press, Cambridge

    Google Scholar 

  • Bonacci T (2013) Chlaenius velutinus (Coleoptera: Carabidae): the conspicuous “polecat” among European carabid beetles. J Insect Behav 26:223–227

    Article  Google Scholar 

  • Bousquet Y (1987) Notes about the relationships of the Callistini (=Chlaeniini) (Coleoptera: Carabidae). Coleopt Bull 41:165–166

    Google Scholar 

  • Bousquet Y (2012) Catalogue of Geadephaga (Coleoptera, Adephaga) of America, north of Mexico. ZooKeys 245:1–1722

    Article  PubMed  Google Scholar 

  • Classen R, Dettner K (1983) Pygidial defensive titer and population structure of Agabus bipustulatus L. and Agabus paludosus F. (Coleoptera, Dytiscidae). J Chem Ecol 9:201–209

    Article  CAS  PubMed  Google Scholar 

  • Cortez V, Verdú JR, Ortiz AJ, Trigos ÁR, Favila ME (2015) Chemical diversity and potential biological functions of the pygidial gland secretions in two species of Neotropical dung roller beetles. Chemoecology 25:201–213

    Article  CAS  Google Scholar 

  • Daloze D, Pasteels JM (1979) Production of cardiac glycosides by chrysomelid beetles and larvae. J Chem Ecol 5:63–77

    Article  CAS  Google Scholar 

  • De Silva ECA, Silk PJ, Hillier NK, Magee D, Cutler GC (2013) Identification of sex pheromone components of blueberry spanworm Itame argillacearia (Lepidoptera: Geometridae). J Chem Ecol 39:1169–1181

    Article  PubMed  Google Scholar 

  • Dierckx F (1899) Étude comparée des glandes pygidiennes chez les carabides et les dytiscides avec quelques remarques sur le classement des carabides. Cellule 16:63–176

    Google Scholar 

  • Eggenberger F, Rowell-Rahier M (1991) Chemical defense and genetic variation, interpopulation study of Oreina gloriosa (Coleoptera: Chrysomelidae). Naturwissenschaften 78:317–320

    Article  CAS  PubMed  Google Scholar 

  • Eggenberger F, Rowell-Rahier M (1993) Physiological sources of variation in chemical defense of Oreina gloriosa (Coleoptera: Chrysomelidae). J Chem. Ecol. 19:395–410

    Article  CAS  PubMed  Google Scholar 

  • Eggenberger F, Heilporn S, Daloze D, Pasteels JM (1994) Sexual dimorphism in the lipid fraction of the defensive secretion of Gastrophysa viridula (Coleoptera: Chrysomelidae). Experientia 50:766–770

    Article  CAS  Google Scholar 

  • Eisner T, Hurst JJ, Meinwald J (1963) Defense mechanisms of arthropods. XI. The structure, function, and phenolic secretions of the glands of a chordeumoid millipede and a carabid beetle. Psyche 70:94–116

    Article  CAS  Google Scholar 

  • Environment Canada (2014) Hydrometric data for Lake Winnipeg at Gimli. Available at http://www.wsc.ec.gc.ca/applications/H2O/index-eng.cfm. Accessed 4 April 2014

  • Fockink DH, Mise KM, Zarbin PH (2013) Male-produced sex pheromone of the carrion beetles, Oxelytrum discicolle and its attraction to food sources. J Chem Ecol 39:1056–1065

    Article  CAS  PubMed  Google Scholar 

  • Forsythe DJ (1972) The structure of the pygidial defence glands of Carabidae (Coleoptera). Trans Zool Soc Lond 32:249–309

    Article  Google Scholar 

  • Giglio A, Brandmayr P, Talarico F, Zetto Brandmayr T (2011) Current knowledge on exocrine glands in carabid beetles: structure, function and chemical compounds. ZooKeys 100:193–201

    Article  PubMed  Google Scholar 

  • Hill CS, Tschinkel WR (1985) Defensive secretion production in the tenebrionid beetle, Zophobas atratus effects of age, sex, and milking frequency. J Chem Ecol 8:1083–1092

    Article  Google Scholar 

  • Holliday AE, Holliday NJ, Mattingly TM, Naccarato KM (2012) Defensive secretions of the carabid beetle Chlaenius cordicollis: chemical components and their geographic patterns of variation. J Chem Ecol 38:278–286

    Article  CAS  PubMed  Google Scholar 

  • Holliday AE, Mattingly TM, Holliday NJ (2015) Defensive secretions of larvae of a carabid beetle. Physiol Entomol 40:131–137

    Article  CAS  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–593

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa K, Murase M (1977) Comparative study of the pygidial defensive systems of carabid beetles. Appl Entomol Zool 12:225–235

    CAS  Google Scholar 

  • Larochelle A, Larivière M-C (2003) A natural history of the ground-beetles (Coleoptera: Carabidae) of America north of Mexico. Pensoft, Sofia, Bulgaria

    Google Scholar 

  • Lečić S, Ćurčić S, Vujisić L, Ćurčić B, Ćurčić N, Nikolić Z, Anđelković S, Telšević V, Makarov S (2014) Defensive secretions in three ground-beetle species (Insecta: Coleoptera: Carabidae). Ann Zool Fennici 51:285–300

    Google Scholar 

  • Lindroth CH (1969) The ground-beetles (Carabidae, excl. Cicindelinae) of Canada and Alaska. Part 6 Opuscula Entomol Suppl 34

  • Luff ML (1986) Aggregation of some Carabidae in pitfall traps. In: den Boer PJ, Luff ML, Mossakowski D, Weber F (eds) Carabid beetles their adaptations and dynamics. Gustav Fischer, Stuttgart, pp 385–397

    Google Scholar 

  • Moore BP (1979) Chemical defense in carabids and its bearing on phylogeny. In: Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) Carabid beetles: their evolution, natural history and classification. Junk, The Hague, pp 193–203

    Chapter  Google Scholar 

  • Moore BP, Wallbank BE (1968) Chemical composition of the defensive secretion in carabid beetles and its importance as a taxonomic character. Proc Royal Entomol Soc B 37:62–72

    Google Scholar 

  • Morrison DF (2004) Multivariate statistical methods, 4th edn. Duxbury Press, Pacific Grove, CA

    Google Scholar 

  • Newhart AT, Mumma RO (1979) Defensive secretions of three species of Acilius (Coleoptera: Dytiscidae) and their seasonal variations as determined by high-pressure liquid chromatography. J Chem Ecol 5:643–652

    Article  CAS  Google Scholar 

  • Pasteels JM, Gregoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:263–289

    Article  CAS  Google Scholar 

  • Pearson GA, Dillery S, Meyer JR (2004) Modeling intra-sexual competition in a sex pheromone system: how much can female movement affect female mating success? J Theor Biol 231:549–555

    Article  CAS  PubMed  Google Scholar 

  • Royer L, Boivin G (1999) Infochemicals mediating the foraging behaviour of Aleochara bilineata Gyllenhal adults: sources of attractants. Entomol Explic Appl 90:199–205

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. Freeman, New York

    Google Scholar 

  • Systat (2009) Systat 13 Statistics. Systat Software Inc., Chicago

    Google Scholar 

  • Ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179

    Article  Google Scholar 

  • Ter Braak CJF, Looman CWN (1994) Biplots in reduced rank regression. Biom J 36:983–1003

    Article  Google Scholar 

  • Ter Braak CJF, Šmilauer P (2002) CANOCO Reference manual and CanoDraw for Windows user’s guide: Software for canonical commmunity ordination (version 4.5). Microcomputer Power, Ithaca, NY

  • Tschinkel WR (1975) A comparative study of the chemical defensive system of tenebrionid beetles: chemistry of the secretions. J Insect Physiol 21:753–783

    Article  CAS  Google Scholar 

  • Turlings TCJ, Davison AC, Tamò C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29:45–55

    Article  Google Scholar 

  • Unruh LM, Xu R, Kramer KJ (1998) Benzoquinone levels as a function of age and gender of the red flour beetle, Tribolium castaneum. Insect Biochem Molec Biol 28:969–977

    Article  CAS  Google Scholar 

  • Vesović N, Ćurčić S, Vujisić L, Nenadić M, Krstić G, Perić-Mataruga V, Milosavljević S, Antić D, Mandić B, Petković I, Vučković I, Marković Đ, Vrbica M, Ćurčić B, Makarov S (2015) Molecular diversity of compounds from pygidial gland secretions of cave-dwelling ground beetles: the first evidence. J Chem Ecol 41:533–539

    Article  PubMed  Google Scholar 

  • Wäschke N, Hardge K, Hancock C, Hilker M, Obermaier E, Meiners T (2014) Habitats as complex odour environments: how does plant diversity affect herbivore and parasitoid orientation. PLoS One 9(1):e85152. doi:10.1371/journal.pone.0085152

    Article  PubMed  PubMed Central  Google Scholar 

  • Will KW, Attygalle AB, Herath K (2000) New defensive chemical data for ground beetles (Coleoptera: Carabidae): interpretations in a phylogenetic framework. Biol J Linn Soc 71:459–481

    Article  Google Scholar 

  • Will KW, Gill AS, Lee H, Attygalle AB (2010) Quantification and evidence for mechanically metered release of pygidial secretions in formic acid-producing carabid beetles. J Insect Sci 10:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Yusuf AA, Crewe RM, Pirk CWW (2014) Olfactory detection of prey by the termite-raiding ant Pachycondyla analis. J Insect Sci 14(53) Available online: http://www.insectscience.org/14.53

  • Zhang ZY, Pawliszyn J (1993) Headspace solid-phase microextraction. Anal Chem 65:1843–1852

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Manitoba Conservation and Water Stewardship for permission to collect insects in Manitoba Provincial Parks. Student summer funding (TMM and AAT) was provided by a Swarthmore College grant from the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. E. Holliday.

Additional information

Handling Editor: Günther Raspotnig.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Holliday, A.E., Mattingly, T.M., Toro, A.A. et al. Age- and sex-related variation in defensive secretions of adult Chlaenius cordicollis and evidence for their role in sexual communication. Chemoecology 26, 107–119 (2016). https://doi.org/10.1007/s00049-016-0210-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-016-0210-4

Keywords

Navigation