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Introduced fire ants can exclude native ants from critical mutualist-provided resources

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Abstract

Animals frequently experience resource imbalances in nature. For ants, one resource that may be particularly valuable for both introduced and native species is high-carbohydrate honeydew from hemipteran mutualists. We conducted field and laboratory experiments: (1) to test if red imported fire ants (Solenopsis invicta) competed with native ants for access to mutualisms with aphids, and (2) to quantify the effects of aphid honeydew presence or absence on colony growth of native ants. We focused on native dolichoderine ants (Formicidae, Dolichoderinae) because they are abundant ants that have omnivorous diets that frequently include mutualist-provided carbohydrates. At two sites in the southeastern US, native dolichoderine ants were far less frequent, and fire ants more frequent, at carbohydrate baits than would be expected based on their frequency in pitfall traps. A field experiment confirmed that a native ant species, Dorymyrmex bureni, was only found tending aphids when populations of S. invicta were suppressed. In the laboratory, colonies of native dolichoderine ants with access to both honeydew and insect prey had twice as many workers and over twice as much brood compared to colonies fed only ad libitum insect prey. Our results provide the first experimental evidence that introduced ants compete for access to mutualist-provided carbohydrates with native ants and that these carbohydrates represent critical resources for both introduced and native ants. These results challenge traditional paradigms of arthropod and ant nutrition and contribute to growing evidence of the importance of nutrition in mediating ecological interactions.

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References

  • Andersen AN (1997) Functional groups and patterns of organization in North American ant communities: a comparison with Australia. J Biogeogr 24:433–460

    Article  Google Scholar 

  • Beggs J (2001) The ecological consequences of social wasps (Vespula spp.) invading an ecosystem that has abundant carbohydrate resource. Biol Conserv 99:17–28

    Article  Google Scholar 

  • Blüthgen N, Gebauer G, Fiedler K (2003) Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community. Oecologia 137:426–435

    Article  PubMed  Google Scholar 

  • Calixto AA, Harris MK, Knutson A, Barr CL (2007a) Native ant responses to Solenopsis invicta buren reduction using broadcast baits. Environ Entomol 36:1112–1123

    Article  PubMed  Google Scholar 

  • Calixto AA, Harris MK, Barr C (2007b) Resurgence and persistence of Dorymyrmex flavus after reduction of Solenopsis invcta buren with a broadcast bait. Environ Entomol 36:549–554

    Article  PubMed  Google Scholar 

  • Cook SC, Eubanks MD, Gold RE, Behmer ST (2010) Colony-level macronutrient regulation in ants: mechanisms, hoarding and associated costs. Anim Behav 79:429–437

    Article  Google Scholar 

  • Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153–181

    Article  Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972

    Article  PubMed  CAS  Google Scholar 

  • Dussutour A, Simpson SJ (2008) Carbohydrate regulation in relation to colony growth in ants. J Exp Biol 211:2224–2232

    Article  PubMed  CAS  Google Scholar 

  • Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:1–5

    Article  Google Scholar 

  • Dussutour A, Simpson SJ (2012) Ant workers die young and colonies collapse when fed a high-protein diet. Proc R Soc Lond B 279:2402–2408

    Article  PubMed  CAS  Google Scholar 

  • Eubanks MD (2001) Estimates of the direct and indirect effects of red imported fire ants on biological control in field crops. Biol Control 21:35–43

    Article  Google Scholar 

  • Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802

    Article  PubMed  Google Scholar 

  • Fanson BG, Yap S, Taylor PW (2012) Geometry of compensatory feeding and water consumption in Drosophila melanogaster. J Exp Biol 216:766–773

    Article  Google Scholar 

  • Grover CD, Kay AD, Monson JA, Marsh TC, Holway DA (2007) Linking nutrition and behavioural dominance: carbohydrate scarcity limits aggression and activity in Argentine ants. Proc Biol Sci 274:2951–2957

    Article  PubMed  Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci USA 107:15503–15507

    Article  PubMed  CAS  Google Scholar 

  • Helms KR, Vinson SB (2002) Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83:2425–2438

    Article  Google Scholar 

  • Helms KR, Vinson SB (2008) Plant resources and colony growth in an invasive ant: the importance of honeydew-producing hemiptera in carbohydrate transfer across trophic levels. Environ Entomol 37:487–493

    Article  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge

    Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Hook AW, Porter SD (1990) Destruction of harvester ant colonies by invading fire ants in south-central Texas (Hymenoptera: Formicidae). Southwest Nat 35:477–478

    Article  Google Scholar 

  • Kay AD, Zumbusch TB, Heinen JL, Marsh TC, Holway DA (2010) Nutrition and interference competition have interactive effects on the behavior and performance of Argentine ants. Ecology 91:57–64

    Article  PubMed  Google Scholar 

  • King JR, Tschinkel WR (2006) Experimental evidence that the introduced fire ant, Solenopsis invicta, does not competitively suppress co-occurring ants in a disturbed habitat. J Anim Ecol 75:1370–1378

    Article  PubMed  Google Scholar 

  • King JR, Tschinkel WR (2008) Experimental evidence that human impacts drive fire ant invasions and ecological change. Proc Natl Acad Sci USA 105:20339–20343

    Article  PubMed  CAS  Google Scholar 

  • Lach L, Parr CL, Abbott KL (2010) Ant ecology. Oxford University Press, Oxford

    Google Scholar 

  • LeBrun EG, Tillberg CV, Suarez AV, Folgarait PJ, Smith CR, Holway DA (2007) An experimental study of competition between fire ants and Argentine ants in their native range. Ecology 88:63–75

    Article  PubMed  CAS  Google Scholar 

  • LeBrun EG, Plowes RM, Gilbert LE (2012) Imported fire ants near the edge of their range: disturbance and moisture determine prevalence and impact of an invasive social insect. J Anim Ecol 81:884–895

    Article  PubMed  Google Scholar 

  • Macom TE, Porter SD (1995) Food and energy requirements of laboratory fire ant colonies (Hymenoptera: Formicidae). Environ Entomol 24:387–391

    Google Scholar 

  • Morrison LW (2002) Long-term impacts of an arthropod-community invasion by the imported fire ant, Solenopsis invicta. Ecology 83:2337–2345

    Article  Google Scholar 

  • Pontin AJ (1978) The numbers and distribution of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecol Entomol 3:203–207

    Article  Google Scholar 

  • Porter SD (1989) Effects of diet on the growth of laboratory fire ant colonies (Hymenoptera: Formicidae). J Kansas Entomol Soc 62:288–291

    Google Scholar 

  • Porter SD, Savignano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095–2106

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct Ecol 23:4–16

  • Savage AM, Rudgers JA, Whitney KD (2009) Elevated dominance of extrafloral nectary-bearing plants is associated with increased abundances of an invasive ant and reduced native ant richness. Divers Distrib 15:751–761

    Article  Google Scholar 

  • Savage AM, Johnson SD, Whitney KD, Rudgers JA (2011) Do invasive ants respond more strongly to carbohydrate availability than co-occurring non-invasive ants? A test along an active Anoplolepis gracilipes invasion front. Aust Ecol 36:310–319

    Article  Google Scholar 

  • Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton

    Google Scholar 

  • Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311

    Article  Google Scholar 

  • Slansky F, Rodriguez JG (1987) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, New York

    Google Scholar 

  • Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant-interactions. Annu Rev Ecol Evol Syst 36:345–372

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Tschinkel WR (2006) The fire ants. Belknap Press, Cambridge

    Google Scholar 

  • Vinson SB (1983) The physiology of the imported fire ant revisited. Fla Entomol 66:126–139

    Article  CAS  Google Scholar 

  • Vinson SB (1994) Impact of the invasion of Solenopsis invicta Buren on native food webs. In: Williams DF (ed) Exotic ants: biology, impact and control of introduced species. Westview Press, Boulder, Colorado, pp 240–258

    Google Scholar 

  • Wäckers F, van Rijn PCJ, Bruin J (2005) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Wilder SM, Eubanks MD (2010) Might nitrogen limitation promote omnivory among carnivorous arthropods? Comment. Ecology 91:3114–3117

    Article  PubMed  Google Scholar 

  • Wilder SM, Holway DA, Suarez AV, LeBrun EG, Eubanks MD (2011a) Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions. Proc Natl Acad Sci USA 108:20639–20644

    Article  PubMed  CAS  Google Scholar 

  • Wilder SM, Holway DA, Suarez AV, Eubanks MD (2011b) Macronutrient content of plant-based food affects growth of a carnivorous arthropod. Ecology 92:325–332

    Article  PubMed  Google Scholar 

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Acknowledgments

Funding was provided by National Science Foundation DEB 0716983 to M.D.E., DEB 0717054 to D.A.H. and DEB 0716966 to A.V.S. We thank M. Buckman for field assistance in Alabama and Michael Castro for assistance with laboratory work. We thank B. Stadler and two anonymous reviewers for helpful comments on a previous draft of this manuscript. All experiments complied with current US laws.

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The authors declare that they have no conflict of interest.

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Correspondence to Shawn M. Wilder.

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Communicated by Bernhard Stadler.

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Wilder, S.M., Barnum, T.R., Holway, D.A. et al. Introduced fire ants can exclude native ants from critical mutualist-provided resources. Oecologia 172, 197–205 (2013). https://doi.org/10.1007/s00442-012-2477-7

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