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Colony take-over and brood survival in temporary social parasites of the ant genus Formica

Abstract

Parasites reduce host fitness, and so instigate counter adaptations by their hosts. In temporary social parasitism, usurpers must not only enter the colony unharmed, but also have their eggs reared by the host workers. We introduced parasitic Formica lugubris and Formica aquilonia queens into queen right and orphaned fragments of three host species, Formica cinerea, Formica picea and Formica fusca, and show that workers of all three host species kill over 40 % of the introduced queens within 10 days, regardless of the presence/absence of a resident queen, and parasite species. More parasite queens died in F. cinerea than in F. picea and F. fusca. There were no major differences in survival between the parasite species (except that F. lugubris survived longer than F. aquilonia in F. fusca colonies compared to F. picea colonies), but parasite queens survived longer in orphaned than in queen right fragments of F. fusca. Experimental introduction of parasite (F. aquilonia) eggs into orphaned colonies of F. fusca showed that none of the parasite eggs were reared until pupation; whereas on average, 12 % of the con-specific hetero-colonial eggs introduced in the same manner were reared until pupation. In all colonies that received parasite brood, all offspring consisted of worker-laid males, whereas the corresponding value was 50 % for colonies that received con-specific hetero-colonial brood. Thus, when the risks of entering host colonies and brood failure are combined, the rate of successful colony take-over is very low. Moreover, the host workers can to some extent alleviate the costs of parasitism by producing a final batch of own offspring.

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References

  • Achenbach A, Foitzik S (2009) First evidence for slave rebellion: enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus. Evol 63(4):1068–1075

    Article  Google Scholar 

  • Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nat 397(6715):151–154

    Article  CAS  Google Scholar 

  • Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Annu Rev Entomol 53:19–37

    PubMed  Article  CAS  Google Scholar 

  • Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Fla Entomol 53(4):229–232

    Article  Google Scholar 

  • Buczkowski G, Silverman J (2005) Context-dependent nestmate discrimination and the effect of action thresholds on exogenous cue recognition in the Argentine ant. Anim Behav 69(3):741–749

    Article  Google Scholar 

  • Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1(6):155–160

    PubMed  Article  CAS  Google Scholar 

  • Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235

    Google Scholar 

  • Bush AO (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge

    Google Scholar 

  • Cervo R (2006) Polistes wasps and their social parasites: an overview. Ann Zool Fennici 43:531–549

    Google Scholar 

  • Chapman NC, Nanork P, Gloag RS, Wattanachaiyingcharoen W, Beekman M, Oldroyd BP (2009) Queenless colonies of the Asian red dwarf honeybee Apis florea are infiltrated by workers from other queenless colonies. Behav Ecol 20(4):817–820

    Article  Google Scholar 

  • Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol Ecol 5(4):599–601

    PubMed  Article  CAS  Google Scholar 

  • Chernenko A, Helanterä H, Sundström L (2011) Egg recognition and social parasitism in Formica ants. Ethol 117(12):1081–1092

    Article  Google Scholar 

  • Chernenko A, Helanterä H, Sundström L (2012) Colony kin structure and queen recruitment in the ant Formica fusca (Hymenoptera: Formicidae). Myrmecol News 16:93–100

    Google Scholar 

  • Collingwood CA (1979) The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomologica Scnadinavica. Scandinavian Science Press Ltd., Klampenborg

    Google Scholar 

  • Crosland MWJ (1990) The influence of the queen, colony size and worker ovarian development on nestmate recognition in the ant Rhytidoponera confusa. Anim Behav 39(3):413–425

    Article  Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Oxford University Press, Oxford

    Google Scholar 

  • Czechowski W, Marko B (2005) Competition between Formica cinerea Mayr (Hymenoptera: Formicidae) and co-occurring ant species, with special reference to Formica rufa L.: direct and indirect interferences. Pol J Ecol 53(4):467–487

    Google Scholar 

  • Czechowski W, Vepsäläinen K (1999) Plesiobiosis between Formica fusca L. and Formica aquilonia Yarr. (Hymenoptera, Formicidae). Ann Zool Wars 49:125–127

    Google Scholar 

  • Czechowski W, Radchenko A, Czechowska W (2002) The ants of Poland. Museum & Institute of Zoology, Warsaw

    Google Scholar 

  • Davies NB (2000) Cuckoos, cowbirds and other cheats. T. & A. D. Poyser, London

    Google Scholar 

  • Davies NB, Welbergen JA (2008) Cuckoo–hawk mimicry? An experimental test. Proc R Soc B 275(1644):1817–1822

    PubMed  Article  CAS  Google Scholar 

  • Davies NB, Bourke AF, de L Brooke M (1989) Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends Ecol Evol 4(9):274–278

    PubMed  Article  CAS  Google Scholar 

  • Dlusskij GM (1967) Murav'i roda Formika. Nauka, Moscow

    Google Scholar 

  • Faber W (1967) Beiträge zur Kenntnis sozialparasitischer Ameisen, 1: Lasius (Austrolasius n. sg.) reginae n.sp., eine neue temporär sozialparasitische Erdameise aus Österreich (Hym. Formicidae). Pflanzenschutz-Ber 36:73–107

    Google Scholar 

  • Foitzik S, DeHeer CJ, Hunjan DN, Herbers JM (2001) Coevolution in host–parasite systems: behavioural strategies of slave-making ants and their hosts. Proc R Soc B 268(1472):1139–1146

    PubMed  Article  CAS  Google Scholar 

  • Fürst MA, Durey M, Nash DR (2012) Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc R Soc B 279(1728):516–522

    PubMed  Article  Google Scholar 

  • Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2(1):67–69

    Article  CAS  Google Scholar 

  • Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35(2):282–290

    Article  Google Scholar 

  • Härtel S, Neumann P, Kryger P, von der Heide C, Moltzer G-J, Crewe RM, van Praagh JP, Moritz RFA (2006) Infestation levels of Apis mellifera scutellata swarms by socially parasitic Cape honeybee workers (Apis mellifera capensis). Apidologie 37(4):462–470

    Article  Google Scholar 

  • Hasegawa E, Imai S (2004) Characterization of microsatellite loci in red wood ants Formica (s. str.) spp. and the related genus Polyergus. Mol Ecol Notes 4(2):200–203

    Article  CAS  Google Scholar 

  • Helanterä H, Sundström L (2007) Worker policing and nest mate recognition in the ant Formica fusca. Behav Ecol Sociobiol 61:1143–1149

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Massachusetts

    Google Scholar 

  • Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evol 58(6):1251–1260

    Google Scholar 

  • Hughes WOH, Boomsma JJ (2006) Does genetic diversity hinder parasite evolution in social insect colonies? J Evol Biol 19(1):132–143

    PubMed  Article  CAS  Google Scholar 

  • Johnson CA, Topoff H, Vander Meer RK, Lavine B (2005) Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae). Behav Ecol Sociobiol 57(3):245–255

    Article  Google Scholar 

  • Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86(4):836–852

    PubMed  Article  Google Scholar 

  • Lenoir A, Fresneau D, Errard C, Hefetz A (1999) The individuality and the colonial identity in ants: the emergence of the social representation concept. In: Detrain C, Deneubourg JL, Pasteels J (eds) Information processing in social insects. Birkhauser, Basel, pp 219–237

    Chapter  Google Scholar 

  • Lenoir A, D'Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    PubMed  Article  CAS  Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nat 430(6999):557–560

    Article  CAS  Google Scholar 

  • Lorenzi MC (2006) The result of an arms race: the chemical strategies of Polistes social parasites. Ann Zool Fennici 43:550–563

    Google Scholar 

  • Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39(1):343–363

    Article  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2008a) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol J Linn Soc 95(1):131–140

    Article  Google Scholar 

  • Martin SJ, Takahashi J, Ono M, Drijfhout FP (2008b) Is the social parasite Vespa dybowskii using chemical transparency to get her eggs accepted? J Insect Physiol 54(4):700–707

    PubMed  Article  CAS  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2011) Is parasite pressure a driver of chemical cue diversity in ants? Proc R Soc B 278(1705):496–503

    PubMed  Article  Google Scholar 

  • Mori A, Le Moli F (1998) Mating behavior and colony founding of the slave-making ant Formica sanguinea (Hymenoptera: Formicidae). J Insect Behav 11(2):235–245

    Article  Google Scholar 

  • Mori A, D'Ettorre P, Le Moli F (1995) Host nest usurpation and colony foundation in the European amazon ant; Polyergus rufescens Latr. (Hymenoptera: Formicidae). Insect Soc 42(3):279–286

    Article  Google Scholar 

  • Pamilo P, Chautems D, Cherix D (1992) Genetic differentiation of disjunct populations of the ants Formica aquilonia and Formica lugubris in Europe. Insect Soc 39(1):15–29

    Article  Google Scholar 

  • Payne RB (1977) The ecology of brood parasitism in birds. Annu Rev Ecol Syst 8(1):1–28

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evol 43(2):258–275

    Article  Google Scholar 

  • Raczkowski JM, Luque GM (2011) Colony founding and social parasitism in Lasius (acanthomyops). Insect Soc 58(2):237–244

    Google Scholar 

  • Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133(3):407–435

    Article  Google Scholar 

  • Rosengren R, Pamilo P, Cherix D (1986) Insular ecology of the red wood ant Formica truncorum Fabr. II. Distribution, reproductive strategy and competition. Ann Zool Fenn 59:63–94

    Google Scholar 

  • Rothstein SI (1982) Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11(4):229–239

    Article  Google Scholar 

  • Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21(1):481–508

    Article  Google Scholar 

  • Santschi F (1906) A propos de moeurs parasitiques temporaires des fourmis du genre Bothriomyrmex. Ann Soc Entomol Fr 75:363–392

    Google Scholar 

  • Savolainen R (1990) Colony success of the submissive ant Formica fusca within territories of the dominant Formica polyctena. Ecol Entomol 15(1):79–85

    Article  Google Scholar 

  • Savolainen R, Vepsäläinen K (1989) Niche differentiation of ant species within territories of the wood ant Formica polyctena. Oikos 56(1):3–16

    Article  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

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

    Google Scholar 

  • Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Wiley–Blackwell, Oxford

    Google Scholar 

  • Snedecor GW, Cochran WG (1980) Statistical methods, 8th edn. Iowa State University Press, Iowa

    Google Scholar 

  • Stuart RJ (1991) Nestmate recognition in leptothoracine ants: testing for effects of queen number, colony size and species of intruder. Anim Behav 42(2):277–284

    Article  Google Scholar 

  • Sundström L, Seppa P, Pamilo P (2005) Genetic population structure and dispersal patterns in Formica ants—a review. Ann Zool Fenn 42(3):163–177

    Google Scholar 

  • Thomas F, Renaud F, Guégan J-F (2005) Parasitism and ecosystems. Oxford University Press, Oxford

    Book  Google Scholar 

  • Thompson JN (2005) Coevolution: the geographic mosaic of coevolutionary arms races. Curr Biol 15(24):992–994

    Google Scholar 

  • Tschinkel WR, Adams ES, Macom T (1995) Territory area and colony size in the fire ant Solenopsis invicta. J Anim Ecol 64(4):473–480

    Article  Google Scholar 

  • Welbergen JA, Davies NB (2009) Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol 19(3):235–240

    PubMed  Article  CAS  Google Scholar 

  • Wilson EO (1971) Insect societies. The Belknap press of Harvard University Press, Cambridge

    Google Scholar 

  • Wojcik DP (1989) Behavioral interactions between ants and their parasites. Fla Entomol 72(1):43–51

    Article  Google Scholar 

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Acknowledgements

This study was supported by the Academy of Finland (project nos. 121216, 206505, 213821, 121078 and 135970). The authors wish to thank Hannele Luhtasela-El-Showk and Martina Ozan for help in the field, David R. Nash for discussions and valuable comments.

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Correspondence to Anton Chernenko.

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Communicated by S. Cremer

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Chernenko, A., Vidal-Garcia, M., Helanterä, H. et al. Colony take-over and brood survival in temporary social parasites of the ant genus Formica . Behav Ecol Sociobiol 67, 727–735 (2013). https://doi.org/10.1007/s00265-013-1496-7

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  • DOI: https://doi.org/10.1007/s00265-013-1496-7

Keywords

  • Social parasitism
  • Social
  • Ant
  • Brood
  • Recognition
  • Egg