Abstract
Accumulating evidence in the literature suggests that oleic acid functions as a necromone across widely divergent insect taxa. The prevelance of this phenomenon has not been fully explored, and its application to pest management remains underdeveloped. Khapra beetle (KB), Trogoderma granarium, is a pest of stored grains, with larvae that can enter facultative diapause and remain cryptic in warehouses. Here, we examine how death affects oleic acid content of Trogoderma spp. cuticular extracts, and whether the compound causes a behavioral response. To assess the generalizability of patterns, many experiments were repeated with warehouse beetle (WB), Trogoderma variabile, and larger cabinet beetle (LCB), Trogoderma inclusum. Extracts of larvae that were first killed by being frozen had greater oleic acid content than those derived from live insects. Two-choice behavioral assays compared responses of solvent controls to these extracts, at both low (~ 2 µg) and high (68–131 µg) oleic acid content. The natural extracts also contained cuticular hydrocarbons and other unidentified chemicals. High oleic acid in the extracts repelled the larvae of all three species. Lower levels of oleic acid did not affect KB and LCB movement, but were attractive to WB. We also performed the assay using a large range of doses of oleic acid alone. At the lower doses, oleic acid had no effect on movement, but it became strongly repellant at higher doses, beginning at 100 µg. These results indicate that necromones may be an overlooked aspect of stored product insect biology, which if further researched could improve pest management.
Similar content being viewed by others
References
Abbott KR (2006) Bumblebees avoid flowers containing evidence of past predation events. Can J Zool 84:1240–1247
Adeesan C, Tamhankar AJ, Rahalkar GW (1977) Influence of larval diapause on pheromone communication in the khapra beetle. Trogoderma granarium everts. Experientia 33:45–46
Akino T, Yamaoka R (1996) Origin of oleic acid, corpse recognition signal in the ant, Formica japonica MOTSCHLSKY. (Hymenoptera: Formicidae). Jpn J Appl Entomol Z 40:265–271
Aksenov V, David Rollo C (2017) Necromone death cues and risk avoidance by the cricket Acheta domesticus: efects of sex and duration of exposure. J Insect Behav 30:259–272
Armitage HM (1956) The khapra beetle problem in California. J Econ Entomol 49:490–493
Arthur FH, Ghimire M, Myers SW, Phillips TW (2018) Evaluation of pyrethroid insecticides and insect growth regulators applied to different surfaces for control of Trogoderma granarium everts the khapra beetle. J Econ Entomol 111:612–619
Athanassiou CG, Kavallieratos NG, Boukouvala MC, Mavroforos ME, Kontodimas DC (2015) Efficacy of alpha-cypermethrin and thiamethoxam against Trogoderma granarium Everts (Coleoptera: Dermestidae) and Tenebrio molitor L. (Coleoptera: Tenebrionidae) on concrete. J Stored Prod Res 62:101–107
Athanassiou CG, Phillips TW, Wakil W (2019) Biology and control of the khapra beetle, Trogoderma granarium, a major quarantine threat to global food security. Ann Rev Entomol 64:131–148
Barak AV (1989) Development of a new trap to detect and monitor khapra beetle (Coleoptera: Dermestidae). J Econ Entomol 82:1470–1477
Blomquist GJ, Tittiger C, Jurenka R (2018) Cuticular hydrocarbons and pheromones of arthropods. In: Wilkes H (ed) Hydrocarbons, oils and lipids: diversity, origin, chemistry and fate. Springer, Cham, pp 1–32
Burges HD (1962) Diapause, pest status and control of the khapra beetle, Trogoderma granarium everts. Ann Appl Biol 50:614–617
Burges H (1963) Studies on the Dermestid beetle Trogoderma granarium Everts. VI.—factors inducing diapause. Bull Entomol Res 54:571–587
Chouvenc T, Robert A, Sémon E, Bordereau C (2012) Burial behaviour by dealates of the termite Pseudacanthotermes spiniger (Termitidae, Macrotermitinae) induced by chemical signals from termite corpses. Insectes Soc 59:119–125
Cobb RD (1958) Seed germination after fumigation with methyl bromide for Khapra beetle control. Bull Calif Dep Agr 47:1–19
Cohen E, Stanic V, Shulov A (1974) Olfactory and gustatory response of Trogoderma granarium, Dermestes maculatus and Tribolium castaneum to various straight chain fatty acid. Z Angew Entomol 76:303–311
Dubis E, Maliński E, Hebasupwska E, Świçeka M, Nawrot J, Pihlaja K, Szafranek J, Warnke Z (1987) The composition of cuticular hydrocarbons of the khapra beetles, Trogoderma granarium. Comp Biochem Phys B 88:911–915
Edde PA, Eaton M, Kells SA, Phillips TW, Hagstrum DW (2012) Biology, behavior, and ecology of pests in other durable commodities. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection. Kansas State University Press, Manhatten, pp 45–61
Fields PG, White NDG (2002) Alternatives to Methyl Bromide Treatments for Stored-Product and Quarantine Insects. An Rev Entomol 47:331–359
Ghimire MN, Arthur FH, Myers SW, Phillips TW (2016) Residual efficacy of deltamethrin and cyfluthrin against Trogoderma variabile and Trogoderma inclusum (Coleoptera: Dermestidae). J Stored Prod Res 66:6–11
Gordon DM (1983) Dependence of necrophoric response to oleic acid on social context in the ant, Pogonomyrmex badius. J Chem Ecol 9:105–111
Gothi KK, Tamhankar AJ, Rahalkar GW (1984) Influence of larval diapause on male response to female sex pheromone in Trogoderma granarium, Everts (Coleoptera: Dermestidae). J Stored Prod Res 20:65–69
Hadaway AB (1955) The biology of dermestid beetles, Trogoderma granarium Everts and Trogoderma versicolor (Creutz). Bull Entomol Res 46:781–796
Hinton HE (1945) A monograph of the beetles associated with stored products. Trustees of the British Museum, London, pp 234–401
Howard RW (1982) Chemical ecology and biochemistry of insect hydrocarbons. Ann Rev Entomol 27:149–172
Ikan R, Stanić V, Cohen E, Shulov A (1970) The function of fatty acids in the diapause of the khapra beetle Trogoderma granarium everts. Comp Biochem Phys 37:205–214
Jood S, Kapoor AC, Singh R (1993) Evaluation of some plant products against Trogoderma granarium Everts in stored wheat and their effects on nutritional composition and organoleptic characteristics of treated grains. J Stored Prod Res 32:345–352
Karnavar GK, Nair KSS (1969) Some preliminary observation on the influence of faecal lipids on the induction of larval diapause in an insect. Life Sci N Y 8:559
Khan ZR, Midega CAO, Bruce TJA, Hooper AM, Pickett JA (2010) Exploiting phytochemicals for developing a ‘push-pull’ crop protection strategy for cereal farmers in Africa. J Exp Bot 61:4185–4196
Klein JA, Beck SD (1980) Nutritional and developmental factors in larval growth and retrogression of Trogoderma glabrum. J Insect Physiol 26:591–599
Levinson AR, Levinson HZ, Schwaiger H, Cassidy RF Jr, Silverstein RM (1978) Olfactory behavior and receptor potentials of the khapra beetle Trogoderma granarium (Coleoptera: Dermestidae) induced by the major components of its sex pheromone, certain analogues, and fatty acid esters. J Chem Ecol 4:95–108
Loschiavo SR (1960) Life-history and behaviour of Trogoderma variabile beal (Coleoptera: Dermestidae). Can Entomol 92:611–618
Maliński E, Hebasupwska E, Świçeka M, Nawrot J (1986) The composition of hydrocarbons of the larvae of the khapra beetles Trogoderma granarium. Comp Biochem Phys 84:211–215
Mcafee A, Chapman A, Iovinella I, Gallagher-Kurtzke Y, Collins T, Higo H, Madilao LL, Pelosi P, Foster L (2018) A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.). Sci Rep 8:5719. https://doi.org/10.1038/s41598-018-24054-2
Morrison WR, Bruce A, Wilkins RV, Albin CE, Arthur FH (2019) Sanitation improves stored product insect pest management. Insects 10:77
Morrison WR, Grosdidier RF, Arthur FH, Myers SW, Domingue MJ (2020) Attraction, arrestment, and preference by immature Trogoderma variabile and Trogoderma granarium to food and pheromonal stimuli. J Pest Sci 93:135–147. https://doi.org/10.1007/s10340-019-01171-z
Myers SW, Hagstrum DH (2012) Quarantine. In: Hagstrum DH, Philips TW, Cuperus G (eds) Stored product protection. Kansas State University, Manhattan, pp 297–304
Nayak M, Daglish G, Phillips TW, Ebert PR (2020) Resistance to the fumigant phosphine and its management in insect pests of stored products: a global perspective. Ann Rev Entomol 65:333–350
Nilsson E, Bengtsson G (2004) Endogenous free fatty acids repel and attract Collembola. J Chem Ecol 30:1431–1443
Partida GJ, Strong RG (1975) Comparative studies on the biologies of six species of Trogoderma: T. variabile. Ann Entomol Soc Am 68:115–125
Rollo CD, Borden JH, Casey I (1995) Endogenously produced repellent from American cockroach (Blattaria: Blattidae): Function in death recognition. Environ Entomol 24:116–124
Rollo CD, Czyewska E, Borden JH (1994) Fatty acid necromones for cockroaches. Naturwissenschaften 81:400–410
Shephard AM, Aksenov V, Rollo CD (2018) Conspecific mortality cues mediate associative learning in crickets, Acheta domesticus (Orthoptera: Gryllidae). J Orthopt Res 27:187
Spangler HG (1965) Reactions of the larvae of the khapra beetle and Trogoderma varabile to certain food substances and organic compounds. J Econ Entomol 58:212–218
Stanic V, Shaaya E, Shulov A (1963) The effect of larval excrements on the growth of Trogoderma granarium (Everts.). Riv Parassit 24:13–17
Strong RG (1975) Comparative studies on the biologies of six species of Trogoderma: T. inclusum. Ann Entomol Soc Am 68:91–104
Wilches DM, Laird RA, Floate KD, Fields PG (2016) A review of diapause and tolerance to extreme temperatures in dermestids (Coleoptera). J Stored Prod Res 68:50–62
Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114
Yao M, Rosenfeld J, Attridge S, Sidhu S, Aksenov V, Rollo CD (2009) Ancient chemistry of avoiding risks of predation and disease. Evol Biol 36:267–281
Acknowledgements
Damon Crook of USDA-APHIS-PPQ provided assistance with maintaining equipment and other aspects of analysis of the extracts by GC–MS. Amanda Davila-Flores of USDA-APHIS-PPQ provided assistance with the rearing of the insects. Funding to support this project was provided through the USDA Agriculture, Quarantine and Inspection (AQI) User Fee program. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). The USDA is an equal opportunity provider and employer.
Author information
Authors and Affiliations
Contributions
MD, WM, and SM conceived and designed research. MD conducted experiments. KY and MD analyzed data. MD wrote the manuscript. All authors read, revised, and approved the manuscript.
Corresponding author
Additional information
Communicated by Günther Raspotnig.
Rights and permissions
About this article
Cite this article
Domingue, M.J., Morrison, W.R., Yeater, K. et al. Oleic acid emitted from frozen Trogoderma spp. larvae causes conspecific behavioral aversion. Chemoecology 30, 161–172 (2020). https://doi.org/10.1007/s00049-020-00307-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-020-00307-3