Advertisement

The Science of Nature

, 103:70 | Cite as

Ants detect but do not discriminate diseased workers within their nest

  • Jean-Baptiste Leclerc
  • Claire Detrain
Original Paper

Abstract

Social insects have evolved an array of individual and social behaviours that limit pathogen entrance and spread within the colony. The detection of ectoparasites or of fungal spores on a nestmate body triggers their removal by allogrooming and appears as a primary component of social prophylaxis. However, in the case of fungal infection, one may wonder whether ant workers are able to detect, discriminate and keep at bay diseased nestmates that have no spores over their cuticle but which constitute a latent sanitary risk due to post-mortem corpse sporulation. Here, we investigate the ability of Myrmica rubra workers to detect and discriminate a healthy from a diseased nestmate infected by the entomopathogen Metarhizium anisopliae. During dyadic encounters in a neutral location, workers were more aggressive towards isolated sick nestmates on the 3rd post-infection day. However, no such detection or discrimination of fungus-infected nestmates occurred in a social context inside the nest or at the nest entrance. Gatekeepers never actively rejected incoming diseased nestmates that rather spontaneously isolated themselves outside the nest. Our study reveals that ant workers may detect health-dependent cues and that their ‘acceptance level’ of sick nestmates is tunable depending on the social context. This raises questions about possible trade-offs between a social closure to pathogens and risks of erroneous rejection of healthy nestmates. Social isolation of moribund ants also appears as a widespread prophylactic strategy of social insects allowing them to reduce exposure to pathogens and to spare costs associated with the management of infected individuals.

Keywords

Ants Social immunity Entomopathogenic fungi Context-dependence Nestmate recognition 

Notes

Acknowledgments

We thank the anonymous referees for their comments and Julien Hendrickx for helping to collect ants. This study was funded by a Ph.D. grant to Mr. Leclerc from FRIA (Fonds pour la Recherche dans l’Industrie et dans l’Agriculture) and by a research credit (CDR J.0092.16) from FRS-FNRS (Fonds de la Recherche Scientifique). C.D. is Research Director from the Belgian National Fund for Scientific Research (FNRS).

Compliance with ethical standards

We declare that the experiments comply with the current laws of Belgium.

References

  1. Arthurs S, Thomas MB (2001) Effects of temperature and relative humidity on sporulation of Metarhizium anisopliae var. acridum in Mycosed cadavers of Schistocerca gregaria. J Invertebr Pathol 78:59–65CrossRefPubMedGoogle Scholar
  2. Baracchi D, Fadda A, Turillazzi S (2012) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J Insect Physiol 58:1589–1596CrossRefPubMedGoogle Scholar
  3. Berlese A (1903) Diagnosi di alcune nuove specie di Acari italiani mirmecofili e liberiGoogle Scholar
  4. Bidochka MJ, Clark DC, Lewis MW, Keyhani NO (2010) Could insect phagocytic avoidance by entomogenous fungi have evolved via selection against soil amoeboid predators? Microbiology 156:2164–2171CrossRefPubMedGoogle Scholar
  5. Boecking O, Spivak M (1999) Behavioural defences of honey bees against Varroa jacobsoni oud. Apidologie 30:141–158CrossRefGoogle Scholar
  6. Boecking O, Rath W, Drescher W (1992) Apis mellifera removes Varroa jacobsoni and Tropilaelaps clareae from sealed brood cells in the tropics. ABJ (USA)Google Scholar
  7. Boomsma JJ, Schmid-Hempel P, Hughes WOH, Fellowes MDE, Holloway GJ, Rolff J (2005) Life histories and parasite pressure across the major groups of social insects. Insect Evol Ecology Proc R Entomol Soc 22:139–175Google Scholar
  8. Bos N, Lefevre T, Jensen AB, D’Ettorre P (2012) Sick ants become unsociable. J Evol Biol 25:342–351CrossRefPubMedGoogle Scholar
  9. Boucias DG, Pendland JC (1998) Entomopathogenic fungi: fungi imperfecti. In: Principles of insect pathology. Springer, USAGoogle Scholar
  10. Boulay R, Hefetz A, Soroker V, Lenoir A (2000) Camponotus fellah Colony integration: worker individuality necessitates frequent hydrocarbon exchanges. Anim Behav 59:1127–1133CrossRefPubMedGoogle Scholar
  11. Boulay R, Lenoir A (2001) Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behav Proc. 55:67–73Google Scholar
  12. Boulay R, Katzav-Gozansky T, Hefetz A, Lenoir A (2004) Odour convergence and tolerance between nestmates through trophallaxis and grooming in the ant Camponotus fellah. Insect Soc 51:55–61CrossRefGoogle Scholar
  13. Buczkowski G, Silverman J (2005) Context-dependent nestmate discrimination and the effect of action 445 thresholds on exogenous cue recognition in the argentine ant. Anim Behav 69:741–749CrossRefGoogle Scholar
  14. Butt TM, Carreck NL, Ibrahim L, Williams IH (1998) Honey-bee-mediated infection of pollen beetle (Meligethes aeneus Fab.) by the insect-pathogenic fungus, Metarhizium anisopliae. Biocontrol Sci Tech 8:533–538CrossRefGoogle Scholar
  15. Calleri DV, Reid EM, Rosengaus RB, Vargo EL, Traniello JF (2006) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc R Soc Lond B Biol Sci 273:2633–2640CrossRefGoogle Scholar
  16. 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 274:2013–2017CrossRefGoogle Scholar
  17. Choe DH, Millar JG, Rust MK (2009) Chemical signals associated with life inhibit necrophoresis in argentine ants. Proc Natl Acad Sci 106:8251–8255CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cotter SC, Kilner RM (2010) Personal immunity versus social immunity. Behav Ecol 21:663–668CrossRefGoogle Scholar
  19. Couvillon MJ, Ratnieks FL (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system. Behav Ecol Sociobiol 62:1099–1105CrossRefGoogle Scholar
  20. Cremer S, Sixt M (2009) Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond Ser B Biol Sci 364:129–142CrossRefGoogle Scholar
  21. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702CrossRefGoogle Scholar
  22. Dalecky A, Renucci M, Tirard A, Debout G, Roux M, Kjellberg F, Provost E (2007) Changes in composition of cuticular biochemicals of the facultatively polygynous ant Petalomyrmex phylax during range expansion in Cameroon with respect to social, spatial and genetic variation. Mol Ecol 16:3778–3791CrossRefPubMedGoogle Scholar
  23. Diez L, Moquet L, Detrain C (2013) Post-mortem changes in chemical profile and their influence on corpse removal in ants. J Chem Ecol 39:1424–1432CrossRefPubMedGoogle Scholar
  24. Downs SG, Ratnieks FL (2000) Adaptive shifts in honey bee (Apis mellifera L.) guarding behaviour support predictions of the acceptance threshold model. Behav Ecol 11:326–333CrossRefGoogle Scholar
  25. El-Awami IO, Dent DR (1995) The interaction of surface and dust particle size on the pick-up and grooming behaviour of the German cockroach Blattella germanica. Entomol Exp Appl 77:81–87CrossRefGoogle Scholar
  26. Elmes GW (1973) Observations on density of queens in natural colonies of Myrmica rubra L.(hymenoptera: formicidae). J Anim Ecol 42:761–771CrossRefGoogle Scholar
  27. Errard C, Hefetz A (1997) Label familiarity and discriminatory ability of ants reared in mixed groups. Insect Soc 44:189–198CrossRefGoogle Scholar
  28. Evans HC, Groden E, Bischoff JF (2010) New fungal pathogens of the red ant, Myrmica rubra, from the UK and implications for ant invasions in the USA. Fungal Biology. 114:451–466Google Scholar
  29. Evans JD, Spivak M (2010) Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 103:62–72CrossRefGoogle Scholar
  30. Fürst MA, Durey M, Nash DR (2011) Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc R Soc Lond B Biol Sci. rspb20110581Google Scholar
  31. Gamboa GJ, Reeve HK, Holmes WG (1991) Conceptual issues and methodology in kin recognition research, a critical discussion. Ethology 88:109–127CrossRefGoogle Scholar
  32. Gillespie JP, Burnett C, Charnley AK (2000) The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum. J Insect Physiol 46:429–437CrossRefPubMedGoogle Scholar
  33. Gonzalez-Tokman DM, Gonzalez-Santoyo I, Lanz-Mendoza H, Aguilar AC (2010) Territorial damselflies do not show immunological priming in the wild. Physiol Entomol 35:364–372CrossRefGoogle Scholar
  34. Gratwick M (1957) The contamination of insects of different species exposed to dust deposits. Bull Entomol Res 48:741–753CrossRefGoogle Scholar
  35. Greene MJ, Gordon DM (2003) Social insects: cuticular hydrocarbons inform task decisions. Nature 423:32–32CrossRefPubMedGoogle Scholar
  36. Groden E (2005) The impact of nest soil on Metarhizium anisopliae infection of the European fire ant, Myrmica rubra (Hymenoptera; Formicidae). In: The 2005 ESA Annual Meeting and Exhibition Google Scholar
  37. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Palaeontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  38. Hänel H (1982) The life cycle of the insect pathogenic fungus Metarhizium anisopliae in the termite Nasutitermes exitiosus. Mycopathologia 80:137–145CrossRefGoogle Scholar
  39. Haskins CP, Haskins EF (1974) Notes on necrophoric behaviour in the archaic ant Myrmecia vindex. Psyche 81:258–267CrossRefGoogle Scholar
  40. Hauton C, Smith VJ (2007) Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. BioEssays 29:1138–1146CrossRefPubMedGoogle Scholar
  41. Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20:249–252CrossRefPubMedGoogle Scholar
  42. Hlavac TF (1975) Grooming systems of insects: structure, mechanics. Ann Entomol Soc Am 68:823–826CrossRefGoogle Scholar
  43. Hölldobler B, Wilson EO (1990) The ants. Harvard: Harvard University PressGoogle Scholar
  44. Hughes WOH (2005) Life histories and parasite pressure across the major groups of social insects. Insect Evol Ecol Proc R Entomol Soc 211:139–139Google Scholar
  45. Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leafcutting ant societies. Evolution 58:1251–1260CrossRefPubMedGoogle Scholar
  46. Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B 269:1811–1819CrossRefGoogle Scholar
  47. Hughes DP, Araujo JPM, Loreto RG, Quevillon L, De Bekker C, Evans HC (2016) Chapter eleven-from so simple a beginning: the evolution of behavioral manipulation by fungi. Adv Genet 94:437–469CrossRefPubMedGoogle Scholar
  48. Hung SY, Boucias DG (1992) Influence of Beauveria bassiana on the cellular defence response of the beet armyworm, Spodoptera exigua. J Invertebr Pathol 60:152–158CrossRefGoogle Scholar
  49. Ichinose K (1991) Seasonal variation in nestmate recognition in Paratrechina flavipes (smith) worker ants (hymenoptera: formicidae). Anim Behav 41:1–6CrossRefGoogle Scholar
  50. Jutsum AR, Saunders TS, Cherrett JM (1979) Intraspecific aggression in the leafcutting ant Acromyrmex octospinosus. Anim Behav 27:839–844CrossRefGoogle Scholar
  51. Kurtti TJ, Keyhani NO (2008) Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae. Microbiology 154:1700–1709CrossRefPubMedGoogle Scholar
  52. Lahav S, Soroker V, Vander Meer RK, Hefetz A (1998) Nestmate recognition in the ant Cataglyphis niger: do queens matter? Behav Ecol Sociobiol 43:203–212CrossRefGoogle Scholar
  53. Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants: the emergence of the social representation concept. In: Information processing in social insects. Basel: BirkhäuserGoogle Scholar
  54. Lenoir A, Cuisset D, Hefetz A (2001) Effects of social isolation on hydrocarbon pattern and nestmate recognition in the ant Aphaenogaster senilis (Hymenoptera, Formicidae). Insect Soc 48:101–109CrossRefGoogle Scholar
  55. Liang D, Silverman J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the argentine ant, Linepithema humile. Naturwissenschaften 87:412–416CrossRefPubMedGoogle Scholar
  56. Liu Z, Yamane S, Wang Q, Yamamoto H (1998) Nestmate recognition and temporal modulation in the patterns of cuticular hydrocarbons in natural colonies of japanese carpenter ant Camponotus japonicus mayr (formicidae). J Ethol 16:57–65CrossRefGoogle Scholar
  57. Marikovsky PI (1962) On some features of behaviour of the ants Formica rufa L. Infected with fungous disease. Insect Soc 9:173–179CrossRefGoogle Scholar
  58. Martin SJ, Helanterä H, Drijfhout FP (2011) Is parasite pressure a driver of chemical cue diversity in ants? Proc R Soc Lond B Biol Sci. 278:496–503CrossRefGoogle Scholar
  59. McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16:295–300CrossRefPubMedGoogle Scholar
  60. Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155CrossRefGoogle Scholar
  61. Myers JH, Rothman LE (1995) Virulence and transmission of infectious diseases in humans and insects: evolutionary and demographic patterns. Trends Ecol Evol 10:194–198CrossRefPubMedGoogle Scholar
  62. Oi DH, Pereira RM (1993) Ant behaviour and microbial pathogens (Hymenoptera: Formicidae). Fla Entomol:63–74Google Scholar
  63. Okuno M, Tsuji K, Sato H, Fujisaki K (2012) Plasticity of grooming behaviour against entomopathogenic 537 fungus Metarhizium anisopliae in the ant Lasius japonicus. J Ethol 30:23–27CrossRefGoogle Scholar
  64. Oron AP, Hoff PD (2006) Kruskal-Wallis and Friedman type tests for nested effects in hierarchical designs. Working paper 68. In: Center for Statistics and the social sciences. University of Washington, Seattle (USA)Google Scholar
  65. Osborne LS, Landa Z (1992) Biological control of whiteflies with entomopathogenic fungi. Fla Entomol:456–471Google Scholar
  66. Reber A, Chapuisat M (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS One 7:353–353Google Scholar
  67. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M (2011) The expression and impact of antifungal grooming in ants. J Evol Biol 24:954–964CrossRefPubMedGoogle Scholar
  68. Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat.133:407–435Google Scholar
  69. Richard FJ, Aubert A, Grozinger CM (2008) Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6:50–50CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rodrigues S, Peveling R, Nagel P, Keller S (2005) The natural distribution of the entomopathogenic soil fungus Metarhizium anisopliae in different regions and habitat types in Switzerland. In: Insect Pathogens Insect Parasit Nematodes Melolontha, pp 185–188Google Scholar
  71. Rueppell O, Hayworth MK, Ross NP (2010) Altruistic self-removal of health compromised honey bee workers from their hive. J Evol Biol 23:1538–1546CrossRefPubMedGoogle Scholar
  72. Salvy M, Martin C, Bagneres AG, Provost E, Roux M, Le Conte Y, Clement JL (2001) Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells. Parasitology 122:145–159CrossRefPubMedGoogle Scholar
  73. Schlüns H, Crozier RH (2009) Molecular and chemical immune defences in ants. Myrmecol News 12:237–249Google Scholar
  74. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, PrincetonGoogle Scholar
  75. Schmid-Hempel P (2005) Evolutionary ecology of insect immune defences. Annu Rev Entomol 50:529–551CrossRefPubMedGoogle Scholar
  76. Schmidt AM, D'Ettorre P, Pedersen JS (2010) Research low levels of nestmate discrimination despite high genetic differentiation in the invasive pharaoh antGoogle Scholar
  77. Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Tauer: LutraGoogle Scholar
  78. Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423CrossRefPubMedGoogle Scholar
  79. Siva-Jothy MT, Moret Y, Rolff J (2005) Insect immunity: an evolutionary ecology perspective. Adv 566 Insect Physiol 32:1201–1248Google Scholar
  80. Spivak M, Reuter GS (2001) Varroa destructor infestation in untreated honey bee (hymenoptera: Apidae) colonies selected for hygienic behaviour. J Econ Entomol 94:326–331CrossRefPubMedGoogle Scholar
  81. Starks PT, Fischer DJ, Watson RE, Melikian GL, Nath SD (1998) Context-dependent nestmate discrimination in the paper wasp, Polistes dominulus: a critical test of the optimal acceptance threshold model. Anim Behav 56:449–458CrossRefPubMedGoogle Scholar
  82. Steiner FM, Schlick-Steiner BC, Moder K, Stauffer C, Arthofer W, Buschinger A, Espadaler X, Christian E, Einfinger K, Lorbeer E (2007) Abandoning aggression but maintaining self-nonself discrimination as a first stage in ant supercolony formation. Curr Biol 17:1903–1907CrossRefPubMedGoogle Scholar
  83. Stuart RJ, Herbers JM (2000) Nest mate recognition in ants with complex colonies: within-and between-population variation. Behav Ecol 11:676–685CrossRefGoogle Scholar
  84. Tanner CJ, Adler FR (2009) To fight or not to fight: context-dependent interspecific aggression in competing ants. Anim Behav 77:297–305CrossRefGoogle Scholar
  85. Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313CrossRefPubMedGoogle Scholar
  86. Tsuji K (2010) What brings peace to the world of ants (Hymenoptera: Formicidae)? Myrmecol News 13:130–132Google Scholar
  87. Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci 100:1078–1083CrossRefPubMedPubMedCentralGoogle Scholar
  88. Ugelvig LV, Cremer S (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 17:1967–1971CrossRefPubMedGoogle Scholar
  89. Ugelvig LV, Kronauer DJ, Schrempf A, Heinze J, Cremer S (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc Lond B Biol Sci. 277:2821–2828CrossRefGoogle Scholar
  90. Wagner D, Brown MJ, Broun P, Cuevas W, Moses LE, Chao DL, Gordon DM (1998) Task-related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. J Chem Ecol 24:2021–2037CrossRefGoogle Scholar
  91. Walker TN, Hughes W (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behaviour in ants. Psyche 65:108–114CrossRefGoogle Scholar
  93. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423CrossRefPubMedGoogle Scholar
  94. Yan S (2005) Evaluation of local pathogenic fungi, boric acid, and their potential synergism for control of the European fire ant, Myrmica rubra (L.)Google Scholar
  95. Yek SH, Muller UG (2011) The metapleural glands of ants. Biol Rev 86:774–779CrossRefPubMedGoogle Scholar
  96. Zhukovskaya M, Yanagawa A, Forschler BT (2013) Grooming behaviour as a mechanism of insect disease defence. Insects 4:609–630CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Unit of Social EcologyUniversité Libre de BruxellesBrusselsBelgium

Personalised recommendations