Abstract
We investigated aspects of resistance to entomopathogenic fungi in the social insect Solenopsis invicta, the red imported fire ant (RIFA). RIFA reared individually were significantly more susceptible to the entomopathogenic fungi Metarhizium anisopliae var. anisopliae M09 than reared in groups. Fungus exposed ants performed more self-grooming behavior when isolated as individuals and received more allo-grooming when accompanied with four healthy nestmates. Using fluorescence microscopy, we counted the number of fluorescein isothiocyanate (FITC)-labeled conidia on the cuticle of fungus exposed ants reared individually or as groups. The number of conidia on the surface of grouped ants decreased more rapidly than on isolated individuals. Allo-grooming behavior appears to be important in removing the conidia on the surface of RIFA. Individuals help fungus exposed ants by performing intensive grooming behaviors, which either risk infecting themselves or get them immunized as social immunity. We show evidence that contacting with fungus exposed ants would decrease susceptibility of nestmates to the fungus. All these results indicate that RIFA benefit from grooming behavior to fight against the fungal pathogens. Future advances in biological control of RIFA with entomopathogenic fungi are also discussed.
Similar content being viewed by others
References
Baracchi D, Turillazzi S (2010) Differences in venom and cuticular peptides in individuals of Apis mellifera (Hymenoptera: Apidae) determined by MALDI-TOF MS. J Insect Physiol 56:366–375
Baracchi D, Francese S, Turillazzi S (2011) Beyond the antipredatory defence: honey bee venom function as a component of social immunity. Toxicon 58:550–557
Baracchi D, Fadda A, Turillazzi S (2012a) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J Insect Physiol 58:1589–1596
Baracchi D, Mazza G, Turillazzi S (2012b) From individual to collective immunity: the role of the venom as antimicrobial agent in the Stenogastrinae wasp societies. J Insect Physiol 58:188–193
Bos N, Lefèvre T, Jensen A, d’Ettorre P (2012) Sick ants become unsociable. J Evol Biol 25:342–351
Chapuisat M, Oppliger A, Magliano P, Christe P (2007) Wood ants use resin to protect themselves against pathogens. Proc R Soc Lond B Biol Sci 274:2013–2017
Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M (2003) Evidence for collective medication in ants. Ecol Lett 6:19–22
Cremer S, Armitage SA, Schmid-Hempel P (2007) Social immunity. Curr Biol 7:693–702
Driver F, Milner RJ, Trueman JW (2000) A taxonomic revision of based on a phylogenetic analysis of rDNA sequence data. Mycol Res 104:134–150
Hamilton C, Lejeune BT, Rosengaus RB (2011) Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biol Lett 7:89–92
Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20:249–252
Hughes WO, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B Biol Sci 269:1811–1819
Hung SY, Boucias D (1992) Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua. J Invertebr Pathol 60:152–158
Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S, Klatt M, Drescher V, Marr C, Ugelvig LV, Cremer S (2012) Social transfer of pathogenic fungus promotes active immunization in ant colonies. PLoS Biol 10:e1001300
Lacey LA (1997) Manual of techniques in insect pathology. Academic, San Diego
Mburu D, Ochola L, Maniania N, Njagi P, Gitonga L, Ndung’u M, Wanjoya A, Hassanali A (2009) Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisoplia and Beauveria bassiana to the termite Macrotermes michaelseni. J Insect Physiol 55:774–780
Morrison LW, Porter SD, Daniels E, Korzukhin MD (2004) Potential global range expansion of the invasive fire ant, Solenopsis invicta. Biol Invasions 6:183–191
Oi DH, Pereira RM (1993) Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Fla Entomol 76:63–74
Okuno M, Tsuji K, Sato H, Fujisaki K (2012) Plasticity of grooming behavior against entomopathogenic fungus Metarhizium anisopliae in the ant Lasius japonicus. J Ethol 30:23–27
Pereira RM, Stimac JL (1992) Transmission of Beauveria bassiana within nests of Solenopsis invicta (Hymenoptera: Formicidae) in the laboratory. Environ Entomol 21:1427–1432
Reber A, Chapuisat M (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS One 7:e35372
Reber A, Purcell J, Buechel S, Buri P, Chapuisat M (2011) The expression and impact of antifungal grooming in ants. J Evol Biol 24:954–964
Rosengaus RB, Maxmen AB, Coates LE, Traniello JF (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125–134
Rosengaus RB, Cornelisse T, Guschanski K, Traniello JF (2007) Inducible immune proteins in the dampwood termite Zootermopsis angusticollis. Naturwissenschaften 94:25–33
Rosengaus RB, Traniello JF, Bulmer MS (2011) Ecology, behavior and evolution of disease resistance in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, pp 165–191
Rust MK, Su NY (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375
Sadd B, Schmid-Hempel P (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 16:1206–1210
Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton
Simone FM, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311
Sumana A, Starks PT (2004) Grooming patterns in the primitively eusocial wasp Polistes dominulus. Ethology 110:825–833
Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S (2013) Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr Biol 23:76–82
Traniello JF, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. PNAS 99:6838–6842
Ugelvig LV, Cremer S (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 17:1967–1971
Vanderwoude C, Elson-Harris M, Hargreaves J, Harris E, Plowman K (2003) An overview of the red imported fire ant (Solenopsis invicta Buren) eradication plan for Australia. Rec Aust Mus 7:11–16
Vinson SB (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biology, and impact. Am Entomol 43:23–39
Walker TN, Hughes WO (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448
Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). Am Entomol 49:150–163
Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423
Xu Y, Huang J, Zhou A, Zeng L (2012) Prevalence of Solenopsis invicta (Hymenoptera: Formicidae) Venom Allergic Reactions in Mainland China. Fla Entomol 95:961–965
Yanagawa A, Shimizu S (2007) Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52:75–85
Yanagawa A, Yokohari F, Shimizu S (2008) Defense mechanism of the termite, Coptotermes formosanus Shiraki, to entomopathogenic fungi. J Invertebr Pathol 97:165–170
Yanagawa A, Yokohari F, Shimizu S (2010) Influence of fungal odor on grooming behavior of the termite, Coptotermes formosanus. J Insect Sci 10:1–10
Zhang R, Li Y, Liu N, Porter SD (2007) An overview of the red imported fire ant (Hymenoptera: Formicidae) in mainland China. Fla Entomol 90:723–731
Acknowledgments
We thank anonymous reviewers and Meron P. Zalucki for valuable edit and comments on this manuscript. We also thank D.S. Wang for help in analyzing the data. This research was financially supported by International Science & Technology Cooperation Program of China (N0. 2011DFB30040), Science & Technology Planning Program of Guangdong Province, China (2011B031500020) and Science & Technology Planning Program of Guangzhou City, Guangdong Province, China (2013J4500032).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Qiu, Hl., Lu, Lh., Shi, Qx. et al. Fungus Exposed Solenopsis invicta Ants Benefit from Grooming. J Insect Behav 27, 678–691 (2014). https://doi.org/10.1007/s10905-014-9459-z
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-014-9459-z