Corpse Management Strategies in Social Insects

Authors

  • Anusree Asokan Department of Entomology, College of Agriculture, Padannakkad, Kerala Agricultural University, Kasaragod 671314, Kerala
  • Barikkad Ramesha Extension Training Centre, Manjeshwar,Kerala Agricultural University, Kasaragod 671323, Kerala
  • Seena S. M. Department of Entomology, College of Agriculture, Padannakkad, Kerala Agricultural University, Kasaragod 671314, Kerala
  • Anooj S. S. Department of Entomology, College of Agriculture, Padannakkad, Kerala Agricultural University, Kasaragod 671314, Kerala
  • Sreekumar K. M. Department of Entomology, College of Agriculture, Padannakkad, Kerala Agricultural University, Kasaragod 671314, Kerala

DOI:

https://doi.org/10.55446/IJE.2023.1237

Keywords:

Social insects, Hymenoptera, Isoptera, necrophoresis, necrophagy, burial behaviour, hygienic behaviour, death cues, CHCs, eusociality, division of labour

Abstract

Social insects are arthropods that lives in a community with other members of the same species. Eusocial insects frequently lose colony members as a result of living in big groupings. They perform cooperative corpse management to maintain the hygiene of the nest, exhibiting behavioural and physiological responses that promote disease resistance, nutrient reallocating and colony protection. Undertaking behaviour is most common in social insects belonging to Hymenoptera and Isoptera which adopts various mechanisms of death recognition, convergent and divergent behavioural responses towards dead items. Corpse removal, burial, cannibalism and avoidance are different solutions evolved by social insects, independently towards the problem of corpse management. Genetic studies and gene expression analysis related to social immune systems gives a better knowledge on behavioural and physiological disease defense in insects which could be considered a novel access to biological pest control. This article provides a comprehensive understanding of corpse management in social insects.

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Published

2023-11-01

How to Cite

Asokan, A., Ramesha, B., S. M., S., S. S., A., & K. M., S. (2023). Corpse Management Strategies in Social Insects. Indian Journal of Entomology, 86(2), 668–677. https://doi.org/10.55446/IJE.2023.1237

Issue

Volume 86, Issue 2, June 2024

Section

Review Articles
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Europe PMC

References

Bulmer M S, Franco B A, Fields E G. 2019. Subterranean termite social alarm and hygienic responses to fungal pathogens. Insects 10(8): 11-13. DOI: https://doi.org/10.3390/insects10080240

Cassidy S T, Chapa J, Tran T A, Dolezal N, Gerena C, Johnson G, Leyva A, Stein S, Wright C M, Keiser C N. 2021. Disease defences across levels of biological organization: individual and social immunity in acorn ants. Animal Behaviour 179: 73-81. DOI: https://doi.org/10.1016/j.anbehav.2021.06.028

Choe D H, Millar J G, Rust M K. 2009. Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proceedings of the National Academy of Sciences, Tucson University of Arizona. pp. 8251-8255. DOI: https://doi.org/10.1073/pnas.0901270106

Chouvenc T, Robert A, Semon E, Bordereau C. 2011. Burial behaviour by dealates of the termite Pseudacanthotermes spiniger (Termitidae, Macrotermitinae) induced by chemical signals from termite corpses. Insectes Sociaux 59(1): 119-125. DOI: https://doi.org/10.1007/s00040-011-0197-3

da Silva L H B, Haifig I, Costa-Leonardo A M. 2019. Facing death: How does the subterranean termite Coptotermes gestroi (Isoptera: Rhinotermitidae) deal with corpses?. Zoology 137: 125712. DOI: https://doi.org/10.1016/j.zool.2019.125712

Davis H E, Meconcelli S, Radek R, McMahon D P. 2018. Termites shape their collective behavioural response based on stage of infection. Scientific Reports 8: 14433. DOI: https://doi.org/10.1038/s41598-018-32721-7

Deeti S, Freas C, Murray T, Cheng K. 2023. Dumping behaviour of Australian desert ants (Melophorus bagoti) (Hymenoptera: Formicidae). Insectes Sociaux 70(2): 225-232. DOI: https://doi.org/10.1007/s00040-023-00911-w

Diez L, Deneubourg J L, Detrain C. 2012. Social prophylaxis through distant corpse removal in ants. The Science of Nature 99(10): 833-842. DOI: https://doi.org/10.1007/s00114-012-0965-6

Drees B M, Miller R W, Vinson B S, Georgis R. 1992. Susceptibility and behavioral response of red imported fire ant (Hymenoptera: Formicidae) to selected entomogenous nematodes (Rhabditida: Steinernematidae & Heterorhabditidae). Journal of Economic Entomology 85(2): 365-370. DOI: https://doi.org/10.1093/jee/85.2.365

Franks N R, Hooper J, Webb C, Dornhaus A. 2005. Tomb evaders: house-hunting hygiene in ants. Biology Letters 1(2): 190-192. DOI: https://doi.org/10.1098/rsbl.2005.0302

Gordon D M. 1989. Dynamics of task switching in harvester ants. Animal Behaviour 38(2): 194-204. Gordon D M. 1996. The organization of work in social insect colonies. Nature 380(6570): 121-124. DOI: https://doi.org/10.1016/S0003-3472(89)80082-X

Guarna M M, Melathopoulos A P, Huxter E, Iovinella I, Parker R, Stoynov N, Tam A, Moon K M, Chan Q W, Pelosi P, White R. 2015. A search for protein biomarkers links olfactory signal transduction to social immunity. BMC Genomics 16: 1-16. DOI: https://doi.org/10.1186/s12864-014-1193-6

Hart A G, Ratnieks F L. 2002. Waste management in the leaf-cutting ant Atta colombica. Behavioural Ecology 13(2): 224-231. DOI: https://doi.org/10.1093/beheco/13.2.224

Holldobler B, Wilson E O. 2009. The superorganism: the beauty elegance and strangeness of insect societies. WW Norton & Company.

Howard D F, Tschinkel W R. 1976. Aspects of necrophoric behavior in the red imported fire ant, Solenopsis invicta. Behaviour 56(2): 157-180. DOI: https://doi.org/10.1163/156853976X00334

Jouquet P, Bultelle A, Djouraev I, Caquineau S, Herve V, Vasseur-Cognet M. 2022. Termite graveyards. Hidden geochemical patches?. Soil Biology and Biochemistry 170: 108678. DOI: https://doi.org/10.1016/j.soilbio.2022.108678

Klett K, Zhang J J, Zhang Y Y, Wang Z, Dong S, Tan K. 2021. The Nasonov gland pheromone as a potential source of death cue in Apis cerana. Journal of Insect Physiology 131: 104238. DOI: https://doi.org/10.1016/j.jinsphys.2021.104238

Leclerc J B, Detrain C. 2018. Impact of colony size on survival and sanitary strategies in fungus-infected ant colonies. Behavioral Ecology and Sociobiology 72: 1-10. DOI: https://doi.org/10.1007/s00265-017-2415-0

Liu L, Yan F M, Zhao C C, Su L J, Huang Q Y, Tang Q B. 2023. microRNAs shape social immunity: a potential target for biological control of the termite Reticulitermes chinensis. Journal of Pest Science 96(1): 265-279. DOI: https://doi.org/10.1007/s10340-022-01495-3

Lopez-Riquelme G O, Fanjul-Moles M L. 2013. The funeral ways of social insects. Social strategies for corpse disposal. Trends in Entomology 9: 71-129.

Maak I, Camera J, Casacci L P, Barbero F, Trigos-Peral G, Slipinski P, Bonelli S, Zaccagno M, Witek M. 2019. The influence of colony traits on the collective behaviour of Myrmica scabrinodis ants. Insect Conservation and Diversity 12(6): 481-491. DOI: https://doi.org/10.1111/icad.12352

Maak I, Toth E, Lenda M, Lorinczi G, Kiss A, Juhasz O, Czechowski W, Torma A. 2020. Behaviours indicating cannibalistic necrophagy in ants are modulated by the perception of pathogen infection level. Scientific Reports 10(1): 1-13. DOI: https://doi.org/10.1038/s41598-020-74870-8

Mabelis A. 1978. Wood ant wars: the relationship between aggression and predation in the red wood ant (Formica polyctena Forst.). Netherlands Journal of Zoology 29: 451-620. DOI: https://doi.org/10.1163/002829679X00016

McAfee A, Chapman A, Iovinella I, Gallagher-Kurtzke Y, Collins T F, Higo H, Madilao L L, Pelosi P, Foster L J. 2018. A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.). Scientific Reports 8(1): 1-13. DOI: https://doi.org/10.1038/s41598-018-24054-2

McAfee A, Collins T F, Madilao LL, Foster L J. 2017. Odorant cues linked to social immunity induce lateralized antenna stimulation in honey bees (Apis mellifera L.). Scientific Reports 7(1): 46171. DOI: https://doi.org/10.1038/srep46171

Munday Z, Brown M J. 2018. Bring out your dead: quantifying corpse removal in Bombus terrestris, an annual eusocial insect. Animal Behaviour 138: 51-57. DOI: https://doi.org/10.1016/j.anbehav.2018.02.003

Neoh K B, Yeap B K, Tsunoda K, Yoshimura T, Lee C Y. 2012. Do termites avoid carcasses? Behavioral responses depend on the nature of the carcasses. PLoS One 7(4): 36375. DOI: https://doi.org/10.1371/journal.pone.0036375

Nilsson E, Bengtsson G. 2004. Death odour changes movement pattern of a Collembola. Oikos 104(3): 509-517. DOI: https://doi.org/10.1111/j.0030-1299.2004.12921.x

Oi D H, Pereira R M. 1993. Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Florida Entomologist. pp. 63-74. DOI: https://doi.org/10.2307/3496014

Park Y I, Raina A K. 2005. Light sensitivity in workers and soldiers of the formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae). Sociobiology 45(2): 367-376.

Pereira H, Detrain C. 2020. Pathogen avoidance and prey discrimination in ants. Royal Society Open Science 7(2): 191705. DOI: https://doi.org/10.1098/rsos.191705

Pereira H, Jossart M, Detrain C. 2020. Waste management by ants: the enhancing role of larvae. Animal Behaviour 168: 187-198. DOI: https://doi.org/10.1016/j.anbehav.2020.08.017

Pisno R M, Ferreira D V, Ferla J J, Serrao J E. 2023. Mite–termite interaction: does termite mortality mediate mite density?. Insectes Sociaux 70: 243-249. DOI: https://doi.org/10.1007/s00040-023-00913-8

Pratt S C. 2005. Quorum sensing by encounter rates in the ant Temnothorax albipennis. Behavioral Ecology 16(2): 488-496. DOI: https://doi.org/10.1093/beheco/ari020

Qiu H L, Cheng D F. 2017. A chemosensory protein gene Si-CSP1 associated with necrophoric behaviour in red imported fire ants (Hymenoptera: Formicidae). Journal of Economic Entomology 110(3): 1284-1290. DOI: https://doi.org/10.1093/jee/tox095

Qiu H L, Lu L H, ShiQX, Tu C C, Lin T, He Y R. 2015. Differential necrophoric behaviour of the ant Solenopsis invicta towards fungal-infected corpses of workers and pupae. Bulletin of Entomological Research 105(5): 607-614. DOI: https://doi.org/10.1017/S0007485315000528

Qiu H L, Qin C S, Fox E G, Wang D S, He Y R. 2020. Differential behavioral responses of Solenopsis invicta (Hymenoptera: Formicidae) workers toward nestmate and non-nestmate corpses. Journal of Insect Science 20(4): 11. DOI: https://doi.org/10.1093/jisesa/ieaa069

Rahman S, Hajong S R, Gevar J, Lenoir A, Darrouzet E. 2016. Cuticular hydrocarbon compounds in worker castes and their role in nestmate recognition in Apis cerana indica. Journal of Chemical Ecology 42(5): 444-451. DOI: https://doi.org/10.1007/s10886-016-0700-4

Renucci M, Tirard A, Provost E. 2011. Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insectes Sociaux 58(1): 9-16. DOI: https://doi.org/10.1007/s00040-010-0109-y

Rojas M G, Elliott R B, Morales-Ramos J A. 2018. Mortality of Solenopsis invicta workers (Hymenoptera: Formicidae) after indirect exposure to spores of three entomopathogenic fungi. Journal of Insect Science 18(3): 20-25. DOI: https://doi.org/10.1093/jisesa/iey050

Rollo C D, Borden J H, Casey I B. 1995. Endogenously produced repellent from American cockroach (Blattaria: Blattidae): function in death recognition. Environmental Entomology 24(1): 116-124. DOI: https://doi.org/10.1093/ee/24.1.116

Rosengaus R B, Jordan C, Lefebvre M L, Traniello J F A. 1999. Pathogen alarm behavior in a termite: a new form of communication in social insects. The Science of Nature 86(11): 544-548. DOI: https://doi.org/10.1007/s001140050672

Ross K G, Matthews R W (eds.). 1991. The social biology of wasps. Cornell University Press, New York. 601 pp. DOI: https://doi.org/10.7591/9781501718670

Sakiyama T. 2020. Interactions between worker ants may influence the growth of ant cemeteries. Scientific Reports 10(1): 2344. DOI: https://doi.org/10.1038/s41598-020-59202-0

Shibao H, Kutsukake M, Matsuyama S, Fukatsu T. 2022. Linoleic acid as corpse recognition signal in a social aphid. Zoological Letters 8(1): 1-10. DOI: https://doi.org/10.1186/s40851-021-00184-w

Shi J, Zhang C, Huang S, Merchant A, Sun Q, Zhou C, Haynes K F, Zhou X. 2021. Managing corpses from different castes in the eastern subterranean termite.Annals of the Entomological Society of America 114(5): 662-671. DOI: https://doi.org/10.1093/aesa/saaa060

Song D, Hu X P, Su N Y. 2006. Survivorship, cannibalism, body weight loss, necrophagy, and entombment in laboratory groups of the Formosan subterranean termite, Coptotermes formosanus under starvation (Isoptera: Rhinotermitidae). Sociobiology 47(1): 27-39.

Spivak M, Danka R G. 2021. Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie 52: 1-16. DOI: https://doi.org/10.1007/s13592-020-00784-z

Spivak M, Gilliam M. 1998. Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa: Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World 79: 169-186. DOI: https://doi.org/10.1080/0005772X.1998.11099408

Sun Q, Zhou X. 2013. Corpse management in social insects.International Journal of Biological Sciences 9(3): 313. DOI: https://doi.org/10.7150/ijbs.5781

Sun Q, Haynes K F, Zhou X. 2017. Dynamic changes in death cues modulate risks and rewards of corpse management in a social insect. Functional Ecology 31(3): 697-706. DOI: https://doi.org/10.1111/1365-2435.12754

Sun Q, Haynes K F, Zhou X. 2018. Managing the risks and rewards of death in eusocial insects. Philosophical Transactions of the Royal Society B: Biological Sciences 373(1754): 20170258. DOI: https://doi.org/10.1098/rstb.2017.0258

Swift K N, Marzluff J M. 2015. Wild American crows gather around their dead to learn about danger. Animal Behaviour 109: 187-197. DOI: https://doi.org/10.1016/j.anbehav.2015.08.021

Tallamy D W, Wood T K. 1986. Convergence patterns in subsocial insects. Annual review of entomology 31(1): 369-390. DOI: https://doi.org/10.1146/annurev.en.31.010186.002101

Ulyshen M D, Shelton T G. 2012. Evidence of cue synergism in termite corpse response behaviour. Naturwissenschafen 99: 89-93. DOI: https://doi.org/10.1007/s00114-011-0871-3

van Langevelde F, Kiggen F, Dooremalen C, Cornelissen B. 2020. Corpse removal increases when honey bee colonies experience high Varroa destructor infestation. Insectes Sociaux 67(4): 507-513. DOI: https://doi.org/10.1007/s00040-020-00789-y

Visscher P K. 1983. The honey bee way of death: necrophoric behavior in Apis mellifera colonies. Animal behaviour 31(4): 1070-1076. DOI: https://doi.org/10.1016/S0003-3472(83)80014-1

Walton A, Jandt J M, Dornhaus A. 2019. Guard bees are more likely to act as undertakers: variation in corpse removal in the bumble bee Bombus impatiens. Insectes Sociaux 66(4): 533-541. DOI: https://doi.org/10.1007/s00040-019-00718-8

Wen P. 2020. Death recognition by undertaker bees. BioRxiv 2020-03. DOI: https://doi.org/10.1101/2020.03.05.978262

Wen P, Chen J, Huang Z Y. 2023. Death recognition by undertaker honey bees based on reduced cuticular hydrocarbon emissions. Entomologia Generalis 43(2): 379-387. DOI: https://doi.org/10.1127/entomologia/2023/1607

Wilson E O, Durlach N I, Roth L M. 1958. Chemical releaser of necrophoric behavior in ants. Psyche 65(4): 108-114. DOI: https://doi.org/10.1155/1958/69391

Wilson E O. 1971. The Insect Societies. Harvard University Press, Cambridge. 716 pp.

Wilson E O. 1983. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) III. Ergonomic resiliency in foraging by A. cephalotes. Behavioral Ecology and Sociobiology 14: 47-54. DOI: https://doi.org/10.1007/BF00366655

Yanagawa A, Fujiwara-Tsujii N, Akino T, Yoshimura T, Yanagawa T, Shimizu S. 2011. Behavioural changes in the termite, Coptotermes formosanus (Isoptera), inoculated with six fungal isolates. Journal of Invertebrate Pathology 107(2): 100-106. DOI: https://doi.org/10.1016/j.jip.2011.03.003

Yamanaka Y, Iwata R, Kiriyama S. 2019. Cannibalism associated with artificial wounds on the bodies of Reticulitermes speratus workers and soldiers (Isoptera: Rhinotermitidae). Insectes Sociaux 66: 107-117. DOI: https://doi.org/10.1007/s00040-018-0661-4

Yao M, Rosenfeld J, Attridge S, Sidhu S, Aksenov V, Rollo C D. 2009. The ancient chemistry of avoiding risks of predation and disease. Evolutionary Biology 36: 267-281. DOI: https://doi.org/10.1007/s11692-009-9069-4