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Behaviours indicating cannibalistic necrophagy in ants are modulated by the perception of pathogen infection level

  • 1.

    Fox, L. R. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6, 87–106 (1975).

    Article  Google Scholar 

  • 2.

    Polis, G. A. The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Evol. Syst. 12, 225–251 (1981).

    Article  Google Scholar 

  • 3.

    Elgar, M. A. & Crespi, B. J. Ecology and evolution of cannibalism. In Cannibalism: ecology and evolution among diverse taxa (eds Elgar, M. A. & Crespi, B. J.) 1–12 (Oxford University Press, Oxford, 1992).

    Google Scholar 

  • 4.

    Richardson, M. L., Mitchell, R. F., Reagel, P. F. & Hanks, L. M. Causes and consequences of cannibalism in noncarnivorous insects. Annu. Rev. Entomol. 55, 39–53 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 5.

    Vilaça, A. Relations between funerary cannibalism and warfare cannibalism: The question of predation. Ethnos 65, 83–106 (2000).

    Article  Google Scholar 

  • 6.

    Lopez-Riquelme, G. O. & Fanjul-Moles, M. L. The funeral ways of social insects. Social strategies for corpse disposal. Trends Entomol. 9, 71–129 (2013).

    Google Scholar 

  • 7.

    Walls, S. C. & Roudebush, R. E. Reduced aggression toward siblings as evidence of kin recognition in cannibalistic salamanders. Am. Nat 138, 1027–1038 (1991).

    Article  Google Scholar 

  • 8.

    Pfennig, D. W. Cannibalistic tadpoles that pose the greatest threat to kin are most likely to discriminate kin. Proc. R. Soc. Lond. B 266, 57–61 (1999).

    Article  Google Scholar 

  • 9.

    Bilde, T. & Lubin, Y. Kin recognition and cannibalism in a subsocial spider. J. Evolut. Biol. 14, 959–966 (2001).

    Article  Google Scholar 

  • 10.

    Santana, A. F. K., Roselino, A. C., Cappelari, F. A. & Zucoloto, F. S. Cannibalism in insects. In Insect bioecology and nutrition for integrated pest management (eds Panizzi, A. R. & Parra, J. R. P.) 177–190 (CRC Press, Boca Raton, 2012).

    Google Scholar 

  • 11.

    Hölldobler, B. & Wilson, E. O. The ants (The Belknap Press of Harvard University, London, 1990).

    Google Scholar 

  • 12.

    Schmickl, T. & Crailsheim, K. Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortage. J. Comput. Physiol. A 187, 541–547 (2001).

    CAS  Article  Google Scholar 

  • 13.

    Sun, Q. & Zhou, X. Corpse management in social insects. Int. J. Biol. Sci. 9, 313–321 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 14.

    Davis, H. E., Meconcelli, S., Rudek, R. & McMahon, D. P. Termites shape their collective behavioural response based on stage of infection. Sci. Rep. 8, 14433. https://doi.org/10.1038/s41598-018-32721-7 (2018).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 15.

    Mabelis, A. A. Wood ant wars: the relationship between aggression and predation in the red wood ant (Formica polyctena Först.). Neth. J. Zool. 29, 451–620 (1979).

    Article  Google Scholar 

  • 16.

    Driessen, G. J. J., Van Raalte, ATh. & De Bruyn, G. Cannibalism in the red wood ant, Formica polyctena (Hymenoptera: Formicidae). Oecologia 63, 13–22 (1984).

    ADS  PubMed  Article  Google Scholar 

  • 17.

    Yao, M. et al. The ancient chemistry of avoiding risks of predation and disease. Evol. Biol. 36, 267–281 (2009).

    Article  Google Scholar 

  • 18.

    Visscher, P. K. The honey bee way of death: Necrophoric behaviour in Apis mellifera colonies. Anim. Behav. 31, 1070–1076 (1983).

    Article  Google Scholar 

  • 19.

    Oi, D. H. & Pereira, R. M. Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Florida Entomol. 76, 63–74 (1993).

    Article  Google Scholar 

  • 20.

    Nazzi, F., Della Vedova, G. & D’Agaro, M. A semiochemical from brood cells infested by Varroa destructor triggers hygienic behaviour in Apis mellifera. Apidologie 35, 65–70 (2004).

    CAS  Article  Google Scholar 

  • 21.

    Renucci, M., Tirrard, A. & Provost, E. Complex undertaking behavior in Temnothorax lichtensteini ant colonies: From corpse-burying behavior to necrophoric behavior. Insect. Soc. 58, 9–16 (2011).

    Article  Google Scholar 

  • 22.

    Diez, L., Le Borgne, H., Lejeune, P. & Detrain, C. Who brings out the dead? Necrophoresis in the red ant Myrmica rubra. Anim. Behav. 6, 1259–1264 (2013).

    Article  Google Scholar 

  • 23.

    Baracchi, D., Fadda, A. & Turillazzi, S. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect. Physiol. 58, 1589–1596 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 24.

    Pull, Ch. D. et al. Destructive disinfection of infected brood prevents systemic disease spread in ant colonies. eLife 7, e32073. https://doi.org/10.7554/eLife.32073 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • 25.

    Leclerc, J.-B. & Detrain, C. Ants detect but do not discriminate diseased workers within their nest. Sci. Nat. 103, 70. https://doi.org/10.1007/s00114-016-1394-8 (2016).

    CAS  Article  Google Scholar 

  • 26.

    Williams, T. & Hernandez, O. Costs of cannibalism in the presence of an iridovirus pathogen of Spodoptera frugiperda. Ecol. Entomol. 31, 106–113 (2006).

    Article  Google Scholar 

  • 27.

    Rudolf, V. H. W. & Antonovics, J. Disease transmission by cannibalism: rare event or common occurrence?. Proc. R. Soc. Lond. B 274, 1205–1210 (2007).

    Google Scholar 

  • 28.

    Sadeh, A. & Rosenheim, J. A. Cannibalism amplifies the spread of vertically transmitted pathogens. Ecology 97, 1994–2002 (2016).

    PubMed  Article  Google Scholar 

  • 29.

    Claessen, D., de Roos, A. M. & Persson, L. Population dynamic theory of size-dependent cannibalism. Proc. R. Soc. Lond. B 271, 333–340 (2004).

    Article  Google Scholar 

  • 30.

    Pfennig, D. W., Ho, S. G. & Hoffman, E. A. Pathogen transmission as a selective force against cannibalism. Anim. Behav. 55, 1255–1261 (1998).

    CAS  PubMed  Article  Google Scholar 

  • 31.

    Loreto, R. G. & Hughes, D. P. Disease in the society: infectious cadavers result in collapse of ant sub-colonies. PLoS ONE 11, e0160820 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 32.

    Hughes, W. H., Eilenberg, J. & Boomsmal, J. J. Trade-offs in group living: Transmission and disease resistance in leaf-cutting ants. Proc. R. Soc. Lond. B 269, 1811–1819 (2002).

    Article  Google Scholar 

  • 33.

    Cremer, S. & Sixt, M. Analogies in the evolution of individual and social immunity. Proc. R. Soc. Lond. B 364, 129–142 (2009).

    Google Scholar 

  • 34.

    Konrad, M. et al. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS ONE 10, 1–15 (2012).

    Google Scholar 

  • 35.

    Liu, L., Ganghua, L., Pengdong, S., Chaoliang, L. & Quiying, H. Experimental verification and molecular basis of active immunization against fungal pathogens in termites. Sci. Rep. 5, 15106. https://doi.org/10.1038/srep15106 (2015).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 36.

    Marikovsky, P. I. On some features of behaviour of the ants Formica rufa L. infected with fungus disease. Insect. Soc. 2, 173–179 (1962).

    Article  Google Scholar 

  • 37.

    Rutkowski, T. et al. Ants trapped for years in an old bunker; survival by cannibalism and eventual escape. J. Hymenopt. Res. 72, 177–184 (2019).

    Article  Google Scholar 

  • 38.

    Seifert, B. Die Ameisen Mittel- und Nordeuropas (Lutra-Verlags-und Vertriebsgesellschaft, Görlitz, 2007).

    Google Scholar 

  • 39.

    Czechowski, W., Radchenko, A., Czechowska, W. & Vepsäläinen, K. The ants of Poland with reference to the myrmecofauna of Europe. Fauna Poloniae (n.s.) 4. (Natura Optima Dux Foundation, 2012).

  • 40.

    Meyling, N. V. & Eilenberg, J. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biol. Control 43, 145–155 (2007).

    Article  Google Scholar 

  • 41.

    Reber, A. & Chapuisat, M. Diversity, prevalence and virulence of fungal entomopathogens in colonies of the ant Formica selysi. Insect. Soc. 59, 231–239 (2012).

    Article  Google Scholar 

  • 42.

    Hajek, A. E. & St. Leger, R. J. Interactions between fungal pathogens and insect hosts. Annu. Rev. Entomol. 39, 293–322 (1994).

    Article  Google Scholar 

  • 43.

    Maák, I. et al. Cues or meaningless objects? Differential responses of the ant Formica cinerea to corpses of competitors and enslavers. Anim. Behav. 91, 53–59 (2014).

    Article  Google Scholar 

  • 44.

    Csata, E. & Dussutour, A. Nutrient regulation in ants (Hymenoptera: Formicidae): A review. Myrmecol. News 29, 111–124 (2019).

    Google Scholar 

  • 45.

    Nonacs, P. Death in the distance: Mortality risk as information for foraging ants. Behaviour 112, 23–35 (1990).

    Article  Google Scholar 

  • 46.

    Roces, F. & Núṅez, J. A. Information about food quality influences load-size selection in recruited leaf-cutting ants. Anim. Behav. 45, 135–143 (1993).

    Article  Google Scholar 

  • 47.

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

    Google Scholar 

  • 48.

    Heifig, I., Lima, J. T., Janei, V. & Costa-Leonardo, A. M. Effects of group size and starvation on survival of the Asian subterranean termite Coptotermes gestroi (Isoptera: Rhinotermitidae). Austral Entomol. 57, 279–284 (2017).

    Article  Google Scholar 

  • 49.

    Pompilio, L., Kacelnik, A. & Behmer, S. T. State-dependent learned valuation drives choice in an invertebrate. Science 311, 1613–1615 (2006).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 50.

    Akino, T. & Yamaoka, R. Origin of oleic acid: Corpse recognition signal in the ant Formica japonica Motschlsky (Hymenoptera: Formicidae). Jpn. J. Appl. Entomol. Z. 40, 265–271 (1996).

    CAS  Article  Google Scholar 

  • 51.

    Chouvenc, T., Robert, A., Sémon, E. & Bordereau, C. Burial behaviour by dealates of the termite Pseudacanthotermes spiniger (Termitidae, Macrotermitinae) induced by chemical signals from termite corpses. Insect. Soc. 59, 119–125 (2012).

    Article  Google Scholar 

  • 52.

    Kok-Boon, N., Beng-Keok, Y., Kunio, T., Tsuyoshi, Y. & Chow-Yang, L. Do termites avoid carcasses? Behavioral responses depend on the nature of the carcasses. PLoS ONE 7, 1–11 (2012).

    Google Scholar 

  • 53.

    Diez, L., Moquet, L. & Detrain, C. Post-mortem changes in chemical profile and their influence on corpse removal in ants. J. Chem. Ecol. 39, 1424–1432 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 54.

    Bignell, D. E., Roisin, Y. & Lo, N. Biology of Termites: A modern synthesis (Springer, Berlin, 2010).

    Google Scholar 

  • 55.

    Dlusskij, G. M. Ants of the genus Formica (Hymenoptera, Formicidae, g. Formica) (Nauka, Moscow, 1967) (in Russian).

    Google Scholar 

  • 56.

    Czechowski, W. Ants cemeteries. Przegląd Zoologiczny 20, 417–427 (1976) (in Polish with English summary).

    Google Scholar 

  • 57.

    Czechowski, W. Around nest cemeteries of Myrmica schencki Em. (Hymenoptera: Formicidae): their origin and a possible significance. Pol. J. Ecol. 56, 359–363 (2008).

    Google Scholar 

  • 58.

    Gibb, H. Experimental evidence for mediation of competition by habitat succession. Ecology 92, 1871–1878 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 59.

    Chouvenc, T., Su, N.-Y. & Elliott, M. L. Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. J. Econ. Entomol. 101, 885–893 (2008).

    CAS  PubMed  Article  Google Scholar 

  • 60.

    Yanagawa, A., Yokohari, F. & Shimizu, S. The role of antennae in removing entomopathogenic fungi from cuticle of the termite Coptotermes formosanus. . J. Insect Sci. 9, 1–9 (2009).

    Article  Google Scholar 

  • 61.

    Tranter, Ch., LeFevre, L., Evison, S. E. F. & Hughes, W. O. H. Threat detection: Contextual recognition and response to parasites by ants. Behav. Ecol. 26, 396–405 (2015).

    Article  Google Scholar 

  • 62.

    Bonadies, E., Wcislo, W. T., Gálvez, D., Hughes, W. O. H. & Fernández-Marin, H. Hygiene defense behaviors used by a fungus-growing ant depend on the fungal pathogen stages. Insects 10, 130 (2019).

    PubMed Central  Article  PubMed  Google Scholar 

  • 63.

    Simone-Finstrom, M. D. & Spivak, M. Increased resin collection after parasite challenge: A case of self-medication in honey bees?. PLoS ONE 7, e34601. https://doi.org/10.1371/journal.pone.0034601 (2012).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 64.

    Brütsch, T. & Chapuisat, M. Wood ants protect their brood with tree resin. Anim. Behav. 93, 157–161 (2014).

    Article  Google Scholar 

  • 65.

    Ormond, E. L., Thomas, A. P. M., Pell, J. K., Freeman, S. N. & Roy, H. E. Avoidance of a generalist entomopathogenic fungus by the ladybird Coccinella septempunctata. FEMS Microbiol. Ecol. 77, 229–237 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 66.

    Fernández-Marín, H., Zimmerman, J. K., Rehner, S. A. & Wcislo, W. T. Active use of the metapleural glands by ants in controlling fungal infection. Proc. R. Soc. Lond. B 273, 1689–1695 (2006).

    Google Scholar 

  • 67.

    Tragust, S. et al. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr. Biol. 23, 1–7 (2013).

    Article  CAS  Google Scholar 

  • 68.

    Tragust, S., Herrmann, C., Häfner, J., Braasch, R., Tilgen, Ch., Hoock, M., Milidakis, M. A., Gross, R. & Feldhaar, H. Formicine ants swallow their highly acidic poison for gut microbial selection and control. bioRxiv preprint https://doi.org/10.1101/2020.02.13.947432 (2020).

  • 69.

    Cremer, S., Pull, Ch. D. & Fürst, M. A. Social immunity: emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 70.

    Rosengaus, R. B., Jordan, C., Lefebvre, M. L. & Traniello, J. F. A. Pathogen alarm behavior in a termite: A new form of communication in social insects. Naturwissenschaften 86, 544–548 (1999).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 71.

    Hernandez-Lopez, J., Reissberger-Gallé, U., Crailsheim, K. & Schuehly, W. Cuticular hydrocarbon cues of immune-challenged workers elicit immune activation in honeybee queens. Mol. Ecol. 26, 3062–3073 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 72.

    Chouvenc, T. & Su, N.-Y. When subterranean termites challenge the rules of fungal epizootics. PLoS ONE 7, 84. https://doi.org/10.1371/journal.pone.0034484 (2012).

    CAS  Article  Google Scholar 

  • 73.

    Csata, E., Erős, K. & Markó, B. Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: changes in host mortality and behavior. Insect. Soc. 61, 247–252 (2014).

    Article  Google Scholar 

  • 74.

    Diez, L., Urbain, L., Lejeune, Ph. & Detrain, C. Emergency measures: adaptive response to pathogen intrusion in the ant nest. Behav. Process. 116, 80–86 (2015).

    Article  Google Scholar 

  • 75.

    Qui, H.-L. et al. Differential necrophoric behaviour of the ant Solenopsis invicta towards fungal infected corpses of workers and pupae. Bull. Entomol. Res. 105, 607–614 (2015).

    Article  CAS  Google Scholar 

  • 76.

    Pereira, H. & Detrain, C. Pathogen avoidance and prey discrimination in ants. R. Soc. Open Sci. 7, 191705 (2020).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 77.

    Cremer, S., Armitage, S. A. O. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, 693–702 (2007).

    Article  CAS  Google Scholar 

  • 78.

    Pull, Ch. D. & Cremer, S. Co-founding ant queens prevent disease by performing prophylactic undertaking behaviour. BMC Evol. Biol. 219, 17. https://doi.org/10.1186/s12862-017-1062-4 (2017).

    Article  Google Scholar 

  • 79.

    Kramm, K. R., West, D. F. & Rockenbach, P. G. Pathogens of termites: transfer of the entomopathogen Metarhizium anisopliae between the termites of Reticulitermes sp.. J. Invertebr. Pathol. 40, 1–6 (1982).

    Article  Google Scholar 

  • 80.

    Kesäniemi, J., Koskimäki, J. J. & Jurvansuu, J. Corpse management of the invasive Argentine ant inhibits growth of pathogenic fungi. Sci. Rep. 9, 7593. https://doi.org/10.1038/s41598-019-44144-z (2019).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 81.

    Greenwald, E. E., Baltiansky, L. & Feinerman, O. Individual crop loads provide local control for collective food intake in ant colonies. eLife 7, e31730 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 82.

    Horstmann, K. Untersuchungen über den Nahrungserwerb der Waldameisen (Formica polyctena Foerster) im Eichenwald. Oecologia 5, 138–157 (1970).

    ADS  PubMed  Article  Google Scholar 

  • 83.

    Bhatkar, A. & Whitcomb, W. H. Artificial diet for rearing various species of ants. Florida Entomol. 53, 229–232 (1970).

    Article  Google Scholar 

  • 84.

    Choe, D. H. & Rust, M. K. Horizontal transfer of insecticides in laboratory colonies of the argentine ant (Hymenoptera: Formicidae). J. Econ. Entomol. 101, 1397–1405 (2008).

    CAS  PubMed  Article  Google Scholar 

  • 85.

    Pereira, R. M. & Stimac, J. L. Transmission of Beauveria bassiana within nests of Solenopsis invicta (Hymenoptera: Formicidae) in the laboratory. Environ. Entomol. 21, 1427–1432 (1992).

    Article  Google Scholar 

  • 86.

    Liu, H., Skinner, M., Parker, B. L. & Brownbridge, M. Pathogenicity of Beauveria bassiana, Metarhizium anisopliae (Deuteromycotina: Hyphomycetes), and other entomopathogenic fungi against Lygus lineolaris (Hemiptera: Miridae). J. Econ. Entomol. 95, 675–681 (2002).

    PubMed  Article  Google Scholar 

  • 87.

    Loreto, R. G. & Hughes, D. P. Disease dynamics in ants. Adv. Genet. 94, 287–306. https://doi.org/10.1016/bs.adgen.2015.12.005 (2016).

    CAS  Article  PubMed  Google Scholar 

  • 88.

    R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2017). https://www.R-project.org/.

  • 89.

    Therneau, T. coxme: Mixed Effects Cox Models. R package version 2.2-5. https://CRAN.R-project.org/package=coxme (2015).

  • 90.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-5. https://CRAN.R-project.org/package=lme4 (2013).

  • 91.

    Bartoń, K. MuMIn: Multi-model inference. R package version 1.9.13. https://CRAN.R-project.org/package=MuMIn (2013).

  • 92.

    Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: Challenges and solutions. J. Evol. Biol. 24, 699–711 (2011).

    CAS  PubMed  Article  Google Scholar 


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