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Behavioral Ecology and Sociobiology

, Volume 70, Issue 1, pp 27–39 | Cite as

The placid slavemaker: avoiding detection and conflict as an alternative, peaceful raiding strategy

  • Isabelle Kleeberg
  • Susanne Foitzik
Original Article

Abstract

Host entry is a crucial step in a parasite’s life cycle. When parasites manage to circumvent host detection, exploitation of host resources is facilitated, as host defenses have not to be counteracted. Social parasites exploit animal societies and, likewise, detection avoidance can be beneficial. Yet, due to strong selection pressures, hosts of socially parasitic slavemaking ants often recognize them as enemies, so that slavemakers use open force to raid host colonies. These fights, however, prohibit the enslavement of adult host workers (eudulosis), which cannot be manipulated to work for them. Instead, they steal brood during raids, and enslave those upon emergence. In contrast to the violent raids of most slavemakers, no aggression occurs during most of the raids of the newly described slavemaker Temnothorax pilagens. Thereby, T. pilagens regularly induces adult host workers to be part of their slave workforce. We demonstrate that non-enslaved colonies of its host species respond to this slavemaker with little aggression. We further investigate how the slavemaker circumvents recognition and show that chemical resemblance of host profiles might explain the low aggressive responses. But, which parameters determine whether slave raids escalate, resulting in carnage among defenders? Our experiments reveal that host aggression is counterproductive as aggressive host colonies suffer from more fatalities during raids, but cannot save more brood. The slavemaker, however, benefits from not eliciting fights, as it doubles its enslaved workforce by capturing brood plus adult host workers. Hence, undercutting recognition allows the slavemaker to avoid raid escalation with its associated fitness benefits.

Keywords

Social parasite Host–parasite co-evolution Aggression Cuticular hydrocarbons Eudulosis Conflict management 

Notes

Acknowledgments

We are thankful to the Sleeping Bear National Lakeshore in Michigan for allowing us to collect ants (Permit no: SLBE-2014-SCI-0005), as well as to the Ohio metro parks and the Edmund Niles Huyck Preserve in New York. We thank Sylwester Job for helping in the field. Sylwester Job and Kolja Siebert were involved in the raiding experiments and Valerie Finke in the evacuation experiments. We would like to thank Tobias Pamminger and Barbara Feldmeyer for feedback on the study design and manuscript. This study was funded by the Deutsche Forschungsgemeinschaft (Fo 298/9-2).

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

265_2015_2018_MOESM1_ESM.docx (233 kb)
ESM 1 (DOCX 232 kb)
265_2015_2018_Fig5_ESM.jpg (153 kb)
Fig. S1

Host colony aggression, measured as the aggression index according to Errard and Hefetz (1979), towards different opponent species. (left figure) Colony aggression of T. ambiguus and T. longispinosus hosts from Michigan towards the sympatric slavemaker T. pilagens, a non-nestmate conspecific ant and the allopatric slavemakers T. duloticus from Ohio and P. americanus from either New York or Ohio. (right figure) Colony aggression of T. ambiguus and T. longispinosus from Michigan, T. longispinosus from New York and T. curvispinosus from Ohio towards their respective sympatric slavemaking species and towards a non-nestmate conspecific ant. Solid symbols represent aggression towards slavemaking species and hollow symbols towards non-nestmate conspecifics. Different symbols represent different opponent species. Symbols moreover represent the back-transformed logit-mean ± s.e. Significance levels: * < 0.05; ** < 0.01; *** < 0.001.(JPEG 79 kb)

265_2015_2018_MOESM2_ESM.eps (676 kb)
High Resolution Image (EPS 675 kb)

References

  1. Alloway TM (1979) Raiding behaviour of two species of slavemaking ants, Harpagoxenus americanus (Emery) and Leptothorax duloticus Wesson (Hymenoptera: Formicidae). Anim Behav 27:202–210CrossRefGoogle Scholar
  2. Alloway TM (1990) Slave-species ant colonies recognize slavemakers as enemies. Anim Behav 39:1218–1220CrossRefGoogle Scholar
  3. Aureli F, Cords M, Van Schaik CP (2002) Conflict resolution following aggression in gregarious animals: a predictive framework. Anim Behav 64:325–343CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-6 http://cran.R-project.org/package=lme4.
  5. Bauer S, Witte V, Böhm M, Foitzik S (2009) Fight or flight? a geographic mosaic in host reaction and potency of a chemical weapon in the social parasite Harpagoxenus sublaevis. Behav Ecol Sociobiol 64:45–56CrossRefGoogle Scholar
  6. Beibl J, Stuart RJ, Heinze J, Foitzik S (2005) Six origins of slavery in formicoxenine ants. Insect Soc 52:291–297CrossRefGoogle Scholar
  7. Brandt M, Heinze J, Schmitt T, Foitzik S (2005) A chemical level in the co-evolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18:176–586CrossRefGoogle Scholar
  8. Brandt M, Heinze J, Schmitt T, Foitzik S (2006) Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus. Insect Soc 53:291–299CrossRefGoogle Scholar
  9. Buschinger A, Ehrhardt W, Winter U (1980) The organization of slave raids in dulotic ants: a comparative study (Hymenoptera; Formicidae). Ethology 53:245–264Google Scholar
  10. Buschinger A (1989) Evolution, speciation, and inbreeding in the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). J Evol Biol 2:265–283CrossRefGoogle Scholar
  11. Errard C, Hefetz A (1997) Label familiarity and discriminatory ability of ants reared in mixed groups. Insect Soc 44:189–198CrossRefGoogle Scholar
  12. D’Ettorre P, Errard C (1998) Chemical disguise during colony founding in the dulotic ant Polyergus rufescens Latr. (Hymenoptera, Formicidae). Insect Soc Life 2:71–77Google Scholar
  13. D’Ettorre P, Heinze J (2001) Sociobiology of slavemaking ants. Acta Etholog 3:67–82CrossRefGoogle Scholar
  14. D'Ettorre P, Mondy N, Lenoir A, Errard C (2002) Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature. Proc R Soc Lond B Biol Sci 269:1911–1918CrossRefGoogle Scholar
  15. Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154CrossRefGoogle Scholar
  16. Foitzik S, DeHeer CJ, Hunjan DN, Herbers JM (2001) Coevolution in host parasite systems: behavioral strategies of slavemaking ants and their hosts. Proc R Soc Lond B Biol Sci 268:1139–1146CrossRefGoogle Scholar
  17. Foitzik S, Herbers J (2001) Colony structure of a slavemaking ant. II. Frequency of slave raids and impact on the host population. Evolution 55:316–323PubMedCrossRefGoogle Scholar
  18. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78PubMedCrossRefGoogle Scholar
  19. 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. doi: 10.1098/rspb.2011.0581 Google Scholar
  20. Gibbs AG, Rajpurohit S (2010) Cuticular and water balance. Insect hydrocarbons: biology, biochemistry, and chemical ecology 6:100–121CrossRefGoogle Scholar
  21. Gladstone DE (1981) Why there are no ant slave rebellions. Am Nat 117:779–781CrossRefGoogle Scholar
  22. Herbers J, Foitzik S (2002) The ecology of slavemaking ants and their hosts in north temperate forests. Ecology 83:148–163CrossRefGoogle Scholar
  23. Hick K, Reddon AR, O’Connor CM, Balshine S (2014) Strategic and tactical fighting decisions in cichlid fishes with divergent social systems. Behaviour 151:47–71CrossRefGoogle Scholar
  24. Hölldobler B, Lumsden CJ (1980) Territorial strategies in ants. Science 210:732–739PubMedCrossRefGoogle Scholar
  25. Hölldobler B (1976) Tournaments and slavery in a desert ant. Science 192:912–914PubMedCrossRefGoogle Scholar
  26. Jackson BD, Morgan ED (1993) Insect chemical communication: pheromones and exocrine glands of ants. Chemoecology 4:125–144CrossRefGoogle Scholar
  27. Jongepier E, Kleeberg I, Job S, Foitzik S (2014) Collective defence portfolios of ant hosts shift with social parasite pressure. Proc R Soc Lond B Biol Sci 281. doi: 10.1098/rspb.2014.0225
  28. Jongepier E, Kleeberg I, Foitzik S (2015) The ecological success of a social parasite increases with manipulation of collective host behaviour. J Evol Biol. doi: 10.1111/jeb.12738
  29. Kleeberg I, Pamminger T, Jongepier E, Papenhagen M, Foitzik S (2014) Forewarned is Forearmed: aggression and information use determine fitness costs of slave raids. Behav Ecol 25:1058–1063CrossRefGoogle Scholar
  30. Kleeberg I, Jongepier E, Job S, Foitzik S (2015) Geographic variation in social parasite pressure predicts intraspecific but not interspecific aggressive responses in hosts of a slavemaking ant. Ethology 121:694–702CrossRefGoogle Scholar
  31. Kronauer DJC, Schöning C, D’Ettorre P, Boomsma JJ (2010) Colony fusion and worker reproduction after queen loss in army ants. Proc R Soc Lond B Biol Sci 277:755–763CrossRefGoogle Scholar
  32. Kutter H (1957) Zur Kenntnis schweizerischer Coptoformica Arten. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 30:1–24Google Scholar
  33. Lenoir A, Malosse C, Yamaoka R (1997) Chemical mimicry between parasitic ants of the genus Formicoxenus and their host Myrmica (Hymenoptera, Formicidae). Biochem Syst Ecol 25:379–389CrossRefGoogle Scholar
  34. Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599PubMedCrossRefGoogle Scholar
  35. Mori A, Grasso DA, Visicchio R, Le Moli F (2000) Colony founding in Polyergus rufescens: the role of the Dufour’s gland. Insect Soc 47:7–10CrossRefGoogle Scholar
  36. Mori A, Grasso DA, Visicchio R, Le Moli F (2001) Comparison of reproductive strategies and raiding behavior in facultative and obligatory slave-making ants: the case of Formica sanguinea and Polyergus rufescens. Insect Soc 48:302–314CrossRefGoogle Scholar
  37. Neat FC, Taylor AC, Huntingford FA (1998) Proximate costs of fighting in male cichlid fish: the role of injuries and energy metabolism. Anim Behav 55:875–882PubMedCrossRefGoogle Scholar
  38. Pamminger T, Scharf I, Pennings PS, Foitzik S (2011) Increased host aggression as an induced defense against slave-making ants. Behav Ecol 23:255–260CrossRefGoogle Scholar
  39. Pamminger T, Modlmeier AP, Suette S, Pennings PS, Foitzik S (2012) Raiders from the sky: slavemaker founding queens select for aggressive host colonies. Biol Lett 8:748–750PubMedPubMedCentralCrossRefGoogle Scholar
  40. Preuschoft S, van Schaik CP (2000) „Dominance and communication” in Conflict management in various social settings: 77 – 105Google Scholar
  41. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608PubMedCrossRefGoogle Scholar
  42. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  43. Sanetra M, Guesten R (2001) The socially parasitic ant genus Strongylognathus Mayr in North Africa (Insecta: Hymenoptera: Formicidae). Zootaxa 20:4–18Google Scholar
  44. Seifert B, Kleeberg I, Feldmeyer B, Pamminger T, Jongepier E, Foitzik S (2014) Temnothorax pilagens sp. n. – a new slave-making species of the tribe Formicoxenini from North America (Hymenoptera, Formicidae). ZooKeys 368:65PubMedCrossRefGoogle Scholar
  45. Schneirla T C (1971) Army ants. A study in social organization. San Francisco, CA: W. H. Freeman and CompanyGoogle Scholar
  46. Schumann RD (1992) Raiding behavior of the dulotic ant Chalepoxenus muellerianus (Finzi) in the field (Hymenoptera: Formicidae, Myrmicinae). Insect Soc 39:325–333CrossRefGoogle Scholar
  47. Thomas JA, Schönrogge K, Elmes GW, Fellowes MDE, Holloway GJ, Rolff J (2005) Specializations and host associations of social parasites of ants. Insect evolutionary ecology: Proceedings of the Royal Entomological Society's 22nd Symposium, Reading, UK, 2003. CABI PublishingGoogle Scholar
  48. Tsuneoka Y, Akino T (2012) Chemical camouflage of the slave-making ant Polyergus samurai queen in the process of the host colony usurpation (Hymenoptera: Formicidae). Chemoecology 22:89–99CrossRefGoogle Scholar
  49. Van Zweden HS, D’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. Insect hydrocarbons: biology, biochemistry and chemical ecology 11:222–243CrossRefGoogle Scholar
  50. Vander Meer RK, Alonso LE (2002) Queen primer pheromone affects conspecific fire ant (Sonlenopsis invicta) aggression. Behav Ecol Sociobiol 51:122–130CrossRefGoogle Scholar
  51. Van Wilgenburg E, van Lieshout E, Elgar MA (2005) Conflict resolution strategies in meat ants (Iridomyrmex purpureus): ritualized displays versus lethal fighting. Behaviour 142:701–716CrossRefGoogle Scholar
  52. Wiens JA (1976) Population responses to patchy environments. Annu Rev Ecol Syst 7:81–120CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Institute of ZoologyJohannes Gutenberg UniversityMainzGermany

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