Skip to main content
SpringerLink
Log in

Towards a nutritional ecology of invasive establishment: aphid mutualists provide better fuel for incipient Argentine ant colonies than insect prey

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Many potential species invasions fail before establishment. This is likely especially true for invasive Argentine ants that must overcome a severe founding bottleneck and transition from propagules that rely on protein-rich prey to massive supercolonies that dominate by consuming carbohydrate-rich honeydew from hemipteran mutualists. While this dietary shift supports the classic idea that protein fuels early colony development and carbohydrates maintain adult workers, recent evidence suggests that carbohydrates can govern initial colony establishment. In this study, we use lab experiments to show that resources from aphid mutualists had greater benefits for Argentine ant propagule survival, maintenance, growth, and worker activity rates than did prey items. These effects persisted at low aphid densities, and when colonies were otherwise starved. Moreover, prey-starved colonies did not appear to consume aphids, suggesting that carbohydrate-rich honeydew is a mechanism that facilitates colony establishment. Combined, these results support a hypothesis that the dietary shift from prey to honeydew is driven more by increased access to hemipterans after establishment, than by specific benefits of prey early in colony development. The results highlight the important role of nutritional ecology for studying invasive establishment, linking propagule success not only to the supply of food resources, but also to their quality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbot KL, Green PT (2007) Collapse of an ant–scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246

    Google Scholar 

  • Aron S, Keller L, Passera L (2001) Role of resource availability on sex, caste, and reproductive allocation ratios in the Argentine ant Linepithema humile. J Anim Ecol 70:831–839

    Article  Google Scholar 

  • Bond W, Slingsby P (1984) Collapse of an ant-plant mutualism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 65:1031–1037

    Article  Google Scholar 

  • Brightwell RJ, Silverman J (2011) The Argentine ant persists through unfavourable winters via mutualism facilitated by a native tree. Environ Entomol 40:1019–1026

    Article  PubMed  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  PubMed  CAS  Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    Article  PubMed  CAS  Google Scholar 

  • Cushman JH, Whitham TG (1991) Competition mediating the outcome of a mutualism—protective services of ants as a limiting resource for membracids. Am Nat 138:851–865

    Article  Google Scholar 

  • Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744

    Article  PubMed  CAS  Google Scholar 

  • Frederickson ME (2006) The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites. Oecologia 149:418–427

    Article  PubMed  Google Scholar 

  • Gaigher R, Samways MJ, Henwood J, Jolliffe K (2011) Impact of a mutualism between an invasive ant and honeydew-producing insects on a functionally important tree on a tropical island. Biol Invasions 13:1717–1721

    Article  Google Scholar 

  • Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079

    Article  PubMed  CAS  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 R Soc B 274:2951–2957

    Article  PubMed  Google Scholar 

  • Hee J, Holway DA, Suarez AV, Case TJ (2000) Role of propagule size in the success of incipient colonies of the invasive Argentine ant. Cons Biol 14:559–563

    Article  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 honey-dew producing Hemiptera in carbohydrate transfer across trophic levels. Environ Entomol 37:487–493

    Article  PubMed  Google Scholar 

  • Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251

    Article  Google Scholar 

  • Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Johnson RA, Gibbs AG (2004) Effect of mating stage on water balance, cuticular hydrocarbons and metabolism in the desert harvester ant, Pogonomyrmex barbatus. J Ins Physiol 50:943–953

    Article  CAS  Google Scholar 

  • Kay AD, Scott SE, Schade JD, Hobbie SE (2004) Stoichiometric relations in an ant–treehopper mutualism. Ecol Lett 7:1024–1028

    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 

  • Le Breton J, Jourdan H, Chazeau J, Orivel J, Dejean A (2005) Niche opportunity and ant invasion: the case of Wasmannia auropunctata in a New Caledonian rain forest. J Trop Ecol 21:93–98

    Article  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 

  • Markin GP (1970) Foraging behavior of the Argentine ant in a California citrus grove. J Econ Entomol 63:740–744

    Google Scholar 

  • Mondor EB, Rosenheim JA, Addicott JF (2008) Mutualist-induced transgenerational polyphenisms in cotton aphid populations. Funct Ecol 22:157–162

    Google Scholar 

  • Newell W, Barber TC (1913) The Argentine ant. US Dept Agric Bur Entomol Bull 122:1–98

    Google Scholar 

  • O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817

    Article  Google Scholar 

  • Oliver TH, Leather SR, Cook JM (2008) Macroevolutionary patterns in the origin of mutualisms involving ants. J Evol Biol 21:1597–1608

    Article  PubMed  CAS  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton

    Google Scholar 

  • Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM (2010) Synergy of multiple partners, including freeloaders increases host fitness in a multispecies mutualism. Proc Natl Acad Sci 107:17234–17239

    Article  PubMed  CAS  Google Scholar 

  • Pontin AJ (1960) Field experiments on colony foundation by Lasius niger and L. flavus (F.) (Hym., Formicidae). Ins Soc 7:227–230

    Article  Google Scholar 

  • Powell BE, Silverman J (2010) Population growth of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) in the presence of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae). Environ Entomol 39:1492–1499

    Article  PubMed  Google Scholar 

  • Rodriguez-Cabal MA, Stubel KL, Nunez MA, Sanders NJ (2009) Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms. Biol Lett 5:499–502

    Article  PubMed  Google Scholar 

  • Rowles AD, Silverman J (2009) Carbohydrate supply limits invasion of natural communities by Argentine ants. Oecologia 161:161–171

    Article  PubMed  Google Scholar 

  • Sagata K, Lester PJ (2009) Behavioural plasticity associated with propagule size, resources, and the invasion success of the Argentine ant Linepithema humile. J Appl Ecol 46:19–27

    Article  Google Scholar 

  • Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003) Community disassembly by an invasive species. Proc Natl Acad Sci 100:2474–2477

    Article  PubMed  CAS  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102

    Article  Google Scholar 

  • Sorensen AA, Vinson SB (1981) Quantitative food distribution studies within laboratory colonies of the imported fire ant, Solenopsis invicta Buren. Ins Soc 28:129–160

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Suarez AV, Holway DA, Liang D, Tsutsui ND, Case TJ (2002) Spatiotemporal patterns in intraspecific aggression in the invasive Argentine ant. Anim Behav 64:697–708

    Article  Google Scholar 

  • Tillberg CV, Holway DA, LeBrun EG, Suarez AV (2007) Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proc Natl Acad Sci 104:20856–20861

    Article  PubMed  CAS  Google Scholar 

  • Toft S (1995) Value of the aphid Rhopalosiphum padi as food for cereal spiders. J Appl Ecol 32:552–560

    Article  Google Scholar 

  • Tschinkel WR (1992) Brood raiding and the population dynamics of founding and incipient colonies of the fire ant, Solenopsis invicta. Ecol Entomol 17:179–188

    Article  Google Scholar 

  • Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and cooperation in a widespread invasive species. Proc Natl Acad Sci 100:1078–1083

    Article  PubMed  CAS  Google Scholar 

  • Vogt JT, Appel AG, West MS (2000) Flight energetics and dispersal capability of the fire ant, Solenopsis Invicta Buren. J Ins Physiol 46:697–707

    Article  CAS  Google Scholar 

  • Walters AC, MacKay DA (2005) Importance of large colony size for successful invasion by Argentine ants (Hymenoptera: Formicidae): evidence for biotic resistance by native ants. Aust Ecol 30:395–406

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Yao I, Akimoto S (2002) Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola. Ecol Entomol 27:745–752

    Article  Google Scholar 

Download references

Acknowledgments

We thank A. D. Kay and B. Guenard for critical readings of this manuscript. Support for this research came from the Blanton J. Whitmire endowment at North Carolina State University. M Green assisted with monitoring this experiment. E Spicer-Rice assisted in the field. Experiments comply with all laws of the USA.

Author information

Authors and Affiliations

  1. Department of Entomology, North Carolina State University, Raleigh, NC, 27695, USA

    Jonathan Z. Shik & Jules Silverman

Authors
  1. Jonathan Z. Shik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jules Silverman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan Z. Shik.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 110 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shik, J.Z., Silverman, J. Towards a nutritional ecology of invasive establishment: aphid mutualists provide better fuel for incipient Argentine ant colonies than insect prey. Biol Invasions 15, 829–836 (2013). https://doi.org/10.1007/s10530-012-0330-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-012-0330-x

Keywords

Search

Navigation