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
Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nat 397(6715):151–154
Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Annu Rev Entomol 53:19–37
Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Fla Entomol 53(4):229–232
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
Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1(6):155–160
Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235
Bush AO (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge
Cervo R (2006) Polistes wasps and their social parasites: an overview. Ann Zool Fennici 43:531–549
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
Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol Ecol 5(4):599–601
Chernenko A, Helanterä H, Sundström L (2011) Egg recognition and social parasitism in Formica ants. Ethol 117(12):1081–1092
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
Collingwood CA (1979) The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomologica Scnadinavica. Scandinavian Science Press Ltd., Klampenborg
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
Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Oxford University Press, Oxford
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
Czechowski W, Vepsäläinen K (1999) Plesiobiosis between Formica fusca L. and Formica aquilonia Yarr. (Hymenoptera, Formicidae). Ann Zool Wars 49:125–127
Czechowski W, Radchenko A, Czechowska W (2002) The ants of Poland. Museum & Institute of Zoology, Warsaw
Davies NB (2000) Cuckoos, cowbirds and other cheats. T. & A. D. Poyser, London
Davies NB, Welbergen JA (2008) Cuckoo–hawk mimicry? An experimental test. Proc R Soc B 275(1644):1817–1822
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
Dlusskij GM (1967) Murav'i roda Formika. Nauka, Moscow
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
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
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
Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2(1):67–69
Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35(2):282–290
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
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
Helanterä H, Sundström L (2007) Worker policing and nest mate recognition in the ant Formica fusca. Behav Ecol Sociobiol 61:1143–1149
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Massachusetts
Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evol 58(6):1251–1260
Hughes WOH, Boomsma JJ (2006) Does genetic diversity hinder parasite evolution in social insect colonies? J Evol Biol 19(1):132–143
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
Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86(4):836–852
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
Lenoir A, D'Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599
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
Lorenzi MC (2006) The result of an arms race: the chemical strategies of Polistes social parasites. Ann Zool Fennici 43:550–563
Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39(1):343–363
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
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
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
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
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
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
Payne RB (1977) The ecology of brood parasitism in birds. Annu Rev Ecol Syst 8(1):1–28
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evol 43(2):258–275
Raczkowski JM, Luque GM (2011) Colony founding and social parasitism in Lasius (acanthomyops). Insect Soc 58(2):237–244
Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133(3):407–435
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
Rothstein SI (1982) Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11(4):229–239
Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21(1):481–508
Santschi F (1906) A propos de moeurs parasitiques temporaires des fourmis du genre Bothriomyrmex. Ann Soc Entomol Fr 75:363–392
Savolainen R (1990) Colony success of the submissive ant Formica fusca within territories of the dominant Formica polyctena. Ecol Entomol 15(1):79–85
Savolainen R, Vepsäläinen K (1989) Niche differentiation of ant species within territories of the wood ant Formica polyctena. Oikos 56(1):3–16
Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton
Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, Görlitz/Tauer
Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Wiley–Blackwell, Oxford
Snedecor GW, Cochran WG (1980) Statistical methods, 8th edn. Iowa State University Press, Iowa
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
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
Thomas F, Renaud F, Guégan J-F (2005) Parasitism and ecosystems. Oxford University Press, Oxford
Thompson JN (2005) Coevolution: the geographic mosaic of coevolutionary arms races. Curr Biol 15(24):992–994
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
Welbergen JA, Davies NB (2009) Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol 19(3):235–240
Wilson EO (1971) Insect societies. The Belknap press of Harvard University Press, Cambridge
Wojcik DP (1989) Behavioral interactions between ants and their parasites. Fla Entomol 72(1):43–51
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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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