The Science of Nature

, 102:38 | Cite as

Earwigs (Labidura riparia) mimic rotting-flesh odor to deceive vertebrate predators

  • John A. ByersEmail author
Original Paper


Many insects repel predators with caustic chemicals, while insects mimicking odors of wastes/dead insects to fool predators have not been documented. We found that the shore earwig, Labidura riparia (Dermaptera: Labiduridae) when bitten by anole lizards, Anolis carolinenesus, spits a rotting-flesh odor that deceives these insectivores into rejecting prey. Once a lizard attacked and rejected an earwig, the lizard did not attack another earwig during several weeks despite consuming other prey, indicating associative learning after one trial. The fetid odor was found in the head-prothorax containing salivary glands of both male and female earwigs and was comprised of ∼100 ng dimethyl disulfide and ∼600 ng dimethyl trisulfide. Nymphs had <5 ng of either compound. Adults also spit odorous sulfides after prolonged attacks by harvester ants, Pogonomyrmex rugosus, who were only deterred by the earwig’s forceps. Sulfides released by the earwig are similar to odors of carrion/feces, which may be innately repulsive to some vertebrate predators. The mean initial discharge percentage (IDP) of sulfides from a cohort of earwigs was 62 %; however, IDPs of individuals were highly variable (3–99 %; mean 57 %). The discharge refill time (DRT) to refill 50 % of the earwig’s allomone reservoir was estimated at 13 h. A positive relationship in sulfide amounts with body weight was found only in females in 2009, suggesting metabolic cost tradeoffs were revealed when sulfide content was half that in 2010. This is the first report of insects releasing sulfur-containing compounds that may mimic carrion-fecal odors as a deceptive defense against vertebrate predators.


Associative learning Defensive allomones Innate aversion Mimicry Predators Vertebrate learning 



I thank Le Anne Elhoff for technical assistance. Mention of trade names or commercial products in this article is solely for providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

Data accessibility

Data deposited in figshare repository:

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

114_2015_1288_MOESM1_ESM.jpg (271 kb)
ESM 1 (JPEG 271 kb)


  1. Aihara Y, Yasuoka A, Iwamoto S, Yoshida Y, Misaka T, Abe K (2008) Construction of a taste-blind medaka fish and quantitative assay of its preference-aversion behavior. Genes Brain Behav 7:924–932PubMedCentralCrossRefPubMedGoogle Scholar
  2. Aldrich JR (1988) Chemical ecology of the heteroptera. Ann Rev Entomol 33:211–238CrossRefGoogle Scholar
  3. Ammar ED, Farrag SM (1974) Studies on the behaviour and biology of the earwig Labidura riparia Pallas (Derm., Labiduridae). Z Angew Entomol 75:189–196CrossRefGoogle Scholar
  4. Armstrong DM, Jones JK Jr (1972) Notiosorex crawfordi. Mamm Species 17:1–5Google Scholar
  5. Baker SE, Ellwood SA, Watkins R, MacDonald DW (2005) Non-lethal control of wildlife: using chemical repellents as feeding deterrents for the European badger Meles meles. J Appl Ecol 42:921–931CrossRefGoogle Scholar
  6. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry. WH Freeman, New YorkGoogle Scholar
  7. Blaul B, Ruther J (2012) Body size influences male pheromone signals but not the outcome of contests in Nasonia vitripennis. Anim Behav 84:1557–1563CrossRefGoogle Scholar
  8. Brand CJ, Windingstad RM, Siegfried LM, Duncan RM, Cook RM (1988) Avian morbidity and mortality from botulism, aspergillosis, and salmonellosis at Jamaica Bay wildlife refuge, New York, USA. Colonial Waterbirds 11:284–292CrossRefGoogle Scholar
  9. Brennan TC, Holycross AT (2006) A field guide to amphibians and reptiles in Arizona. Arizona Game and Fish Department, Phoenix, AZGoogle Scholar
  10. Byers JA (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92:69–72CrossRefPubMedGoogle Scholar
  11. Byers JA (2006) Production and predator-induced release of volatile chemicals by the plant bug Lygus hesperus. J Chem Ecol 32:2205–2218CrossRefPubMedGoogle Scholar
  12. Byers JA (2013) Modeling and regression analysis of semiochemical dose-response curves of insect antennal reception and behavior. J Chem Ecol 39:1081–1089CrossRefPubMedGoogle Scholar
  13. Byers JA, Levi-Zada A (2011) Individual variation of (S)-4-methyl-3-heptanone in heads of braconid wasp, Leiophron uniformis, and Pogonomyrmex ants indicates costs of semiochemical production. Chemoecology 21:35–44CrossRefGoogle Scholar
  14. Cooper WE Jr, Hardegen R (2000) Lingual and biting responses to prey chemicals by ingestively naive scincid lizards: discrimination from control chemicals, time course, and effect of method of stimulus presentation. Chemoecology 10:51–58CrossRefGoogle Scholar
  15. Crewe RM, Ross FP (1975) Pheromone biosynthesis: the formation of sulphides by the ant Paltothyreus tarsatus. Insect Biochem 5:839–843CrossRefGoogle Scholar
  16. Dugravot S, Thibout E, Abo-Ghalia A, Huignard J (2004) How a specialist and a non-specialist insect cope with dimethyl disulfide produced by Allium porrum. Entomol Exp Appl 113:173–179CrossRefGoogle Scholar
  17. Eisner T (1960) Defense mechanisms of arthropods. II. The chemical and mechanical weapons of an earwig. Psyche 67:62–70CrossRefGoogle Scholar
  18. Eisner T, Rossini C, Eisner M (2000) Chemical defense of an earwig (Doru taeniatum). Chemoecology 10:81–87CrossRefGoogle Scholar
  19. Garber JC, Barbee RW, Bielitzki JT, Clayton LA, Donovan JC, Hendriksen CFM et al (2011) Guide for care and use of laboratory animals. National Academies Press, Washington, DCGoogle Scholar
  20. Harari AR, Zahavi T, Thiéry D (2011) Fitness cost of pheromone production in signaling female moths. Evolution 65–6:1572–1582CrossRefGoogle Scholar
  21. Hile AG, Shan Z, Zhang SZ, Block E (2004) Aversion of European starlings (Sturnus vulgaris) to garlic oil treated granules: Garlic oil as an avian repellent. Garlic oil analysis by nuclear magnetic resonance spectroscopy. J Agric Food Chem 52:2192–2196CrossRefPubMedGoogle Scholar
  22. Hoffmeister DF (1986) Mammals of Arizona. Univ Arizona Press and Arizona Game Fish Depart 602 ppGoogle Scholar
  23. Hussain A, Saraiva LR, Ferrero DM, Ahuja G, Krishna VS, Liberles SD, Korshing SI (2013) High-affinity olfactory receptor for the death-associated odor cadaverine. Proc Natl Acad Sci U S A 110:19579–19584PubMedCentralCrossRefPubMedGoogle Scholar
  24. Jaffe K, Mirás B, Cabrera A (2007) Mate selection in the moth Neoleucinodes elegantalis: evidence for a supernormal chemical stimulus in sexual attraction. Anim Behav 73:727–734CrossRefGoogle Scholar
  25. Johri PK, Johri R (2012) The description of internal anatomy of Indian earwigs, Labidura riparia form bengalensis (Dohrn), Euborellia annulipes (Lucas) and Nala Lividipes (Dufour): Dermaptera with special reference to digestive, nervous, respiratory, circulatory and reproductive systems. J Exp Zool India 15:309–334Google Scholar
  26. Jürgens A, Wee SL, Shuttleworth A, Johnson SD (2013) Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms. Ecol Let 16:1157–1167CrossRefGoogle Scholar
  27. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503–508CrossRefPubMedGoogle Scholar
  28. Langston RL, Powell JA (1975) The Earwigs of California (Order Dermaptera). Bull Calif Insect Survey 20:1-25 Univ Calif PressGoogle Scholar
  29. Laska M, Metzker K (1998) Food avoidance learning in squirrel monkeys and common marmosets. Learn Mem 5:193–203PubMedCentralPubMedGoogle Scholar
  30. Lev-Yadun S, Ne’eman G, Shanas U (2009) A sheep in wolf’s clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores? Bioessays 31:84–88CrossRefPubMedGoogle Scholar
  31. Lovern MB, Holmes MM, Wade J (2004) The green anole (Anolis carolinensis): a reptilian model for laboratory studies of reproductive morphology and behavior. Inst Lab Anim Res J 45:54–64CrossRefGoogle Scholar
  32. Ming QL, Lewis SM (2010) Pheromone production by male Tribolium castaneum (Coleoptera: Tenebrionidae) is influenced by diet quality. J Econ Entomol 103:1915–1919CrossRefPubMedGoogle Scholar
  33. Moré M, Cocucci AA, Raguso RA (2013) The importance of oligosulfides in the attraction of fly pollinator to the brood-site deceptive species Jaborosa rotacea (Solanaceae). Intern J Plant Sci 174:863–876CrossRefGoogle Scholar
  34. Pan H, Lu Y, Wyckhuys KAG (2013) Repellency of dimethyl disulfide to Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae) under laboratory and field conditions. Crop Prot 50:40–45CrossRefGoogle Scholar
  35. Pasteels JM, Grégoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Ann Rev Entomol 28:263–289CrossRefGoogle Scholar
  36. Pudil F, Uvira R, Janda V (2014) Volatile compounds in stinkhorn (Phallus impudicus L. ex Pers.) at different stages of growth. Eur Sci J 10:163–171Google Scholar
  37. Radi RC, Linsenmair KE (1991) Maternal behavior and nest recognition in the subsocial earwig Labidura riparia Pallas (Dermaptera: Labiduridae). Ethology 89:287–296Google Scholar
  38. Reed TM, Rocke TE (1992) The role of avian carcasses in botulism epizootics. Wildl Soc Bull 20:175–182Google Scholar
  39. Robbins PS, Crocker RL, Nojima S, Morris BD, Roelofs WL, Villani MG (2003) Methyl 2-(methylthio)benzoate: the unique sulfur-containing sex pheromone of Phyllophaga crinita. Naturwissenschaften 90:517–520CrossRefPubMedGoogle Scholar
  40. Roggenbuck M, Schnell IB, Blom N, Baelum J, Bertelsen MF, Pontén TS, Sørensen SJ, Gilbert MTP, Graves GR, Hansen LH (2014) The microbiome of new world vultures. Nat Commun 5(5498):1–7Google Scholar
  41. Roper TJ, Marples NM (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim Behav 53:1241–1250CrossRefPubMedGoogle Scholar
  42. Rowe AH, Rowe MP (2006) Risk assessment by grasshopper mice (Onychomys spp.) feeding on neurotoxic prey (Centruroides spp.). Anim Behav 71:725–734CrossRefGoogle Scholar
  43. Ruberson JR, Herzog GA, Lambert WR, Lewis WJ (1994) Management of the beet armyworm (Lepidoptera: Noctuidae) in cotton: role of natural enemies. Fla Entomol 77:440–453CrossRefGoogle Scholar
  44. Schlinger EI, van den Bosch R, Dietrick EJ (1959) Biological notes on the predaceous earwig Labidura riparia (Pallas), a recent immigrant to California (Dermaptera: Labiduridae). J Econ Entomol 52:247–249CrossRefGoogle Scholar
  45. Shanbhag BA, Ammanna VHF, Saidapur SK (2010) Associative learning in hatchlings of the lizard Calotes versicolor: taste and colour discrimination. Amphibia-Reptilia 31:475–481CrossRefGoogle Scholar
  46. Shepard M, Waddill V, Kloft W (1973) Biology of the predaceous earwig Labidura riparia (Dermaptera: Labiduridae). Ann Entomol Soc Am 66:837–841CrossRefGoogle Scholar
  47. Sirugue D, Bonnard O, Le Quere J-L, Farine J-P, Brossut R (1992) 2-Methylthiazolidine and 4-ethylguaiacol, male sex pheromone components of the cockroach, Nauphoeta cinerea (Dictyoptera, Blaberidae): a reinvestigation. J Chem Ecol 18:2261–2276CrossRefPubMedGoogle Scholar
  48. Sreng L (1990) Seducin, male sex pheromone of the cockroach, Nauphoeta cinerea: isolation, identification, and bioassay. J Chem Ecol 16:2899–2912CrossRefPubMedGoogle Scholar
  49. Symonds MRE, Johnson TL, Elgar MA (2011) Pheromone production, male abundance, body size, and the evolution of elaborate antennae in moths. Ecol Evol 1:227–246Google Scholar
  50. Urru I, Stensmyr MC, Hansson BS (2011) Pollination by brood-site deception. Phytochemistry 72:1655–1666CrossRefPubMedGoogle Scholar
  51. Waddill VH (1978) Sexual differences in foraging on corn of adult Labidura riparia (Derm.: Labiduridae). Entomophaga 23:339–342CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  1. 1.USDA-ARS, US Arid-Land Agricultural Research CenterMaricopaUSA

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