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Differential necrophoric behaviour of the ant Solenopsis invicta towards fungal-infected corpses of workers and pupae

Published online by Cambridge University Press:  17 June 2015

H.-L. Qiu
Affiliation:
College of Resources and Environment, South China Agricultural University, Guangdong, Guangzhou 510642, China
L.-H. Lu
Affiliation:
Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangdong, Guangzhou 510640, China
Q.-X. Shi
Affiliation:
College of Resources and Environment, South China Agricultural University, Guangdong, Guangzhou 510642, China
C.-C. Tu
Affiliation:
College of Resources and Environment, South China Agricultural University, Guangdong, Guangzhou 510642, China
T. Lin
Affiliation:
College of Resources and Environment, South China Agricultural University, Guangdong, Guangzhou 510642, China
Y.-R. He*
Affiliation:
College of Resources and Environment, South China Agricultural University, Guangdong, Guangzhou 510642, China
*
*Author for correspondence Phone: +86-020-85283985 E-mail: yrhe@scau.edu.cn

Abstract

Necrophoric behaviour is critical sanitation behaviour in social insects. However, little is known about the necrophoric responses of workers towards different developmental stages in a colony as well as its underlying mechanism. Here, we show that Solenopsis invicta workers display distinct necrophoric responses to corpses of workers and pupae. Corpses of workers killed by freezing (dead for <1 h) were carried to a refuse pile, but pupal corpses would take at least 1 day to elicit workers’ necrophoric response. Metarhizium anisopliae-infected pupal corpses accelerated the necrophoric behaviour of resident workers, with 47.5% of unaffected corpses and 73.8% infected corpses discarded by 1 day post-treatment). We found that fungus-infected pupal corpses had a higher concentration of fatty acids (palmitic acid, oleic acid and linoleic acid) on their surface. We experimentally confirmed that linoleic and oleic acids would elicit a necrophoric response in workers. The appearance of linoleic and oleic acids appeared to be chemical signals involved in recognition of pupal corpses, and M. anisopliae infection could promote the accumulation of fatty acids on surface of pupal corpses resulting in accelerated necrophoric responses of workers.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

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References

Akino, T. & Yamaoka, R. (1996) Origin of oleic acid, corpse recognition signal in the ant, Formica japonica Motschlsky (Hymenoptera: Formicidae). Japanese Journal of Applied Entomology and Zoology 40, 265271.Google Scholar
Asensio, L., Lopez-Llorca, L.V. & Lopez-Jimenez, J.A. (2005) Use of light, scanning electron microscopy and bioassays to evaluate parasitism by entomopathogenic fungi of the red scale insect of palms (Phoenicococcus marlatti Ckll., 1899). Micron 36, 169175.Google Scholar
Baracchi, D., Fadda, A. & Turillazzi, S. (2012) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. Journal of Insect Physiology 58, 15891596.Google Scholar
Bos, N., Lefèvre, T., Jensen, A. & D'ettorre, P. (2012) Sick ants become unsociable. Journal of Evolutionary Biology 25, 342351.Google Scholar
Brütsch, T. & Chapuisat, M. (2014) Wood ants protect their brood with tree resin. Animal Behaviour 93, 157161.CrossRefGoogle Scholar
Castella, G., Chapuisat, M. & Christe, P. (2008) Prophylaxis with resin in wood ants. Animal Behaviour 75, 15911596.Google Scholar
Chapuisat, M., Oppliger, A., Magliano, P. & Christe, P. (2007) Wood ants use resin to protect themselves against pathogens. Proceedings of the Royal Society B: Biological Sciences 274, 20132017.Google Scholar
Choe, D.H., Millar, J.G. & Rust, M.K. (2009) Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proceedings of National Academic Science of the United States of America 106, 82518255.Google Scholar
Dall'Aglio-Holvorcem, C.G., Benson, W.W., Gilbert, L.E., Trager, J.C. & Trigo, J.R. (2009) Chemical tools to distinguish the fire ant species Solenopsis invicta and S. saevissima (Formicidae: Myrmicinae) in Southeast Brazil. Biochemical Systematics and Ecology 37, 442451.Google Scholar
Diez, L., Deneubourg, J.L., Hoebeke, L. & Detrain, C. (2011) Orientation in corpse-carrying ants: memory or chemical cues? Animal Behaviour 81, 11711176.Google Scholar
Diez, L., Deneubourg, J.L. & Detrain, C. (2012) Social prophylaxis through distant corpse removal in ants. Naturwissenschaften 99, 833842.Google Scholar
Diez, L., Moquet, L. & Detrain, C. (2013) Post-mortem changes in chemical profile and their influence on corpse removal in ants. Journal of Chemical Ecology 39, 14241432.Google Scholar
Diez, L., Lejeune, P. & Detrain, C. (2014) Keep the nest clean: survival advantages of corpse removal in ants. Biology Letters 10, 20140306.CrossRefGoogle ScholarPubMed
Eliyahu, D., Ross, K.G., Haight, K.L., Keller, L. & Liebig, J. (2011) Venom alkaloid and cuticular hydrocarbon profiles are associated with social organization, queen fertility status, and queen genotype in the fire ant Solenopsis invicta . Journal of Chemical Ecology 37, 12421254.Google Scholar
Fan, Y., Pereira, R.M., Kilic, E., Casella, G. & Keyhani, N.O. (2012) Pyrokinin beta-neuropeptide affects necrophoretic behavior in fire ants (S. invicta), and expression of beta-NP in a mycoinsecticide increases its virulence. PLoS ONE 7, e26924.Google Scholar
Gilby, A. (1965) Lipids and their metabolism in insects. Annual Review of Entomology 10, 141160.Google Scholar
Gordon, D.M. (1983) Dependence of necrophoric response to oleic acid on social context in the ant, Pogonomyrmex badius . Journal of Chemical Ecology 9, 105111.Google Scholar
Haskins, C.P. & Haskins, E.F. (1974) Notes on necrophoric behavior in the archaic ant Myrmecia vindex (Formicidae: Myrmeciinae). Psyche 81, 258267.Google Scholar
Heinze, J. & Walter, B. (2010) Moribund ants leave their nests to die in social isolation. Current Biology 20, 249252.Google Scholar
Hölldobler, B. and Wilson, E.O. (1990) The Ants. Cambridge, MA, Harvard University Press.Google Scholar
Howard, D.F. & Tschinkel, W.R. (1976) Aspects of necrophoric behavior in the red imported fire ant, Solenopsis invicta . Behaviour 56, 157180.Google Scholar
Hughes, W.O., Eilenberg, J. & Boomsma, J.J. (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proceedings of the Royal Society of London B: Biological Sciences 269, 18111819.Google Scholar
Lach, L., Parr, C.L. & Abott, K.L. (2010) Ant Ecology. Oxford University Press.Google Scholar
Maák, I., Markó, B., Erős, K., Babik, H., Ślipiński, P. & Czechowski, W. (2014) Cues or meaningless objects? Differential responses of the ant Formica cinerea to corpses of competitors and enslavers. Animal Behaviour 91, 5359.Google Scholar
Renucci, M., Tirard, A. & Provost, E. (2010) Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insectes Sociaux 58, 916.Google Scholar
Richard, F.J. & Hunt, J.H. (2013) Intracolony chemical communication in social insects. Insectes Sociaux 60, 275291.Google Scholar
Rollo, C., Czvzewska, E. & Borden, J. (1994) Fatty acid necromones for cockroaches. Naturwissenschaften 81, 409410.Google Scholar
Schrank, A. & Vainstein, M.H. (2010) Metarhizium anisopliae enzymes and toxins. Toxicon 56, 12671274.Google Scholar
Simone-Finstrom, M. & Spivak, M. (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41, 295311.Google Scholar
Simone, M., Evans, J.D. & Spivak, M. (2009) Resin collection and social immunity in honey bees. Evolution 63, 30163022.Google Scholar
Sturgis, S.J. & Gordon, D.M. (2012) Nestmate recognition in ants (Hymenoptera: Formicidae): a review. Myrmecological News 16, 101110.Google Scholar
Sun, Q. & Zhou, X. (2013) Corpse management in social insects. International Journal of Biological Science 9, 313321.Google Scholar
Tschinkel, W.R. (2006) The Fire Ants. Cambridge, MA, Harvard University Press.Google Scholar
Ugelvig, L.V. & Cremer, S. (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Current Biology 17, 19671971.Google Scholar
Ulyshen, M.D. & Shelton, T.G. (2012) Evidence of cue synergism in termite corpse response behavior. Naturwissenschaften 99, 8993.Google Scholar
Walsh, J.P. & Tschinkel, W.R. (1974) Brood recognition by contact pheromone in the red imported fire ant, Solenopsis invicta . Animal Behaviour 22, 695704.Google Scholar
Yanagawa, A. & Shimizu, S. (2007) Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52, 7585.Google Scholar
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