Wound-dependent leg amputations to combat infections in an ant society

Abstract

Open wounds pose major infection and mortality risks in animals.1Hart B.L. Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans.Philos. Trans. R. Soc. B. 2011; 366: 3406-3417Google Scholar,2Kessler S.E. Why Care: Complex Evolutionary History of Human Healthcare Networks.Front. Psychol. 2020; 11: 199Google Scholar To reduce these risks, many animal species apply antimicrobial compounds on their wounds.1Hart B.L. Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans.Philos. Trans. R. Soc. B. 2011; 366: 3406-3417Google Scholar,2Kessler S.E. Why Care: Complex Evolutionary History of Human Healthcare Networks.Front. Psychol. 2020; 11: 199Google Scholar,3Mascaro A. Southern L.M. Deschner T. Pika S. Application of insects to wounds of self and others by chimpanzees in the wild.Curr. Biol. 2022; 32: 112-113Google Scholar,4de Roode J.C. Lefèvre T. Hunter M.D. Ecology. Self-medication in animals.Science. 2013; 340: 150-151Google Scholar Ant societies use antimicrobial secretions from the metapleural gland to combat pathogens,5Cremer S. Armitage S.A. Schmid-Hempel P. Social immunity.Curr. Biol. 2007; 17: 693-702Google Scholar,6Cremer S. Pull C.D. Fürst M.A. Social Immunity: Emergence and Evolution of Colony-Level Disease Protection.Annu. Rev. Entomol. 2018; 63: 105-123Google Scholar,7Pull C.D. Ugelvig L.V. Wiesenhofer F. Grasse A.V. Tragust S. Schmitt T. Brown M.J. Cremer S. Destructive disinfection of infected brood prevents systemic disease spread in ant colonies.Elife. 2018; 7e32073Google Scholar,8Frank E.T. Wehrhahn M. Linsenmair K.E. Wound treatment and selective help in a termite-hunting ant.Proc. Biol. Sci. 2018; 28520172457Google Scholar,9Frank E.T. Kesner L. Liberti J. Helleu Q. LeBoeuf A.C. Dascalu A. Sponsler D.B. Azuma F. Economo E.P. Waridel P. et al.Targeted treatment of injured nestmates with antimicrobial compounds in an ant society.Nat. Commun. 2023; 14: 8446Google Scholar,10Frank E.T. Schmitt T. Hovestadt T. Mitesser O. Stiegler J. Linsenmair K.E. Saving the injured: Rescue behavior in the termite hunting ant Megaponera analis.Sci. Adv. 2017; 3e1602187Google Scholar but this gland has been lost over evolutionary time in several genera, including Camponotus.11Yek S.H. Mueller U.G. The metapleural gland of ants.Biol. Rev. 2011; 86: 774-791Google Scholar To understand how infected wounds are handled without the use of antimicrobial secretions from the metapleural gland, we conducted behavioral and microbiological experiments in Camponotus floridanus. When we experimentally injured a worker’s leg at the femur, nestmates amputated the injured limb by biting the base (trochanter) of the leg until it was severed, thereby significantly increasing survival compared to ants that did not receive amputations. However, when the experimental injury was more distal (at the tibia), nestmates did not amputate the leg and instead directed more wound care to the injury site. Experimental amputations also failed to improve survival in ants with infected tibia injuries unless the leg was amputated immediately after pathogen exposure. Micro-CT scans revealed that the muscles likely responsible for leg hemolymph circulation are predominantly in the femur. Thus, it is likely that femur injuries, by attenuating hemolymph flow, provide sufficient time for workers to perform amputations before pathogen spread. Overall, this study provides the first example of the use of amputations to treat infected individuals in a non-human animal and demonstrates that ants can adapt their type of treatment depending on the location of wounds.

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