, Volume 174, Issue 1, pp 163–171 | Cite as

Floral visitation by the Argentine ant reduces pollinator visitation and seed set in the coast barrel cactus, Ferocactus viridescens

  • Katherine E. LeVanEmail author
  • Keng-Lou James Hung
  • Kyle R. McCann
  • John T. Ludka
  • David A. Holway
Plant-microbe-animal interactions - Original research


Mounting evidence indicates that trade-offs between plant defense and reproduction arise not only from resource allocation but also from interactions among mutualists. Indirect costs of plant defense by ants, for example, can outweigh benefits if ants deter pollinators. Plants can dissuade ants from occupying flowers, but such arrangements may break down when novel ant partners infiltrate mutualisms. Here, we examine how floral visitation by ants affects pollination services when the invasive Argentine ant (Linepithema humile) replaces a native ant species in a food-for-protection mutualism with the coast barrel cactus (Ferocactus viridescens), which, like certain other barrel cacti, produces extrafloral nectar. We compared the effects of floral visitation by the Argentine ant with those of the most prevalent native ant species (Crematogaster californica). Compared to C. californica, the Argentine ant was present in higher numbers in flowers. Cactus bees (Diadasia spp.), the key pollinators in this system, spent less time in flowers when cacti were occupied by the Argentine ant compared to when cacti were occupied by C. californica. Presumably as a consequence of decreased duration of floral visits by Diadasia, cacti occupied by L. humile set fewer seeds per fruit and produced fewer seeds overall compared to cacti occupied by C. californica. These data illustrate the importance of mutualist identity in cases where plants balance multiple mutualisms. Moreover, as habitats become increasingly infiltrated by introduced species, the loss of native mutualists and their replacement by non-native species may alter the shape of trade-offs between plant defense and reproduction.


Extrafloral nectar Invasion Diadasia Mutualism Crematogaster 



Experiments conducted comply with the current US law and was performed in part at the University of California Natural Reserve System Scripps Coastal Reserve. For access to field sites, we thank D. Smith (Torrey Pines State Reserve) and I. Kay (University of California Natural Reserve System). We gratefully acknowledge field assistance by C. Johnson. Helpful comments on the manuscript were provided by A. Noto, E. Cleland, J. Nieh, J. Shurin and two anonymous reviewers. Financial support provided in part by an NSF graduate research fellowship (K.E.L.), National Geographic Young Explorers grant (K.J.H.), Sigma Xi Grant in Aid of Research (K.J.H.), David Marc Belkin Memorial Research Scholarship (K.R.M.), Cactus and Succulent Society of America Award (K.R.M.), NSF DEB 07-16966 (D.A.H.), and an Academic Senate Bridge Grant (D.A.H.).

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  1. Adler LS (2001) The ecological significance of toxic nectar. Oikos 91:409–420CrossRefGoogle Scholar
  2. Agarwal VM, Rastogi N (2008) Role of floral repellents in the regulation of flower visits of extrafloral nectary-visiting ants in an Indian crop plant. Ecol Entomol 33:59–65CrossRefGoogle Scholar
  3. Ballantyne G, Willmer P (2012) Nectar theft and floral ant-repellence: a link between nectar volume and ant-repellent traits? PLoS ONE 7:e43869PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bentley BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annu Rev Ecol Syst 8:407–427CrossRefGoogle Scholar
  5. Blair AW, Williamson PS (2008) Effectiveness and importance of pollinators to the star cactus (Astrophytum asterias). Southwest Nat 53:423–430CrossRefGoogle Scholar
  6. Blancafort X, Gomez C (2005) Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Acta Oecol 28:49–55CrossRefGoogle Scholar
  7. Chamberlain SA, Holland JN (2008) Density-mediated, context-dependent consumer-resource interactions between ants and extrafloral nectar plants. Ecology 89:1364–1374PubMedCrossRefGoogle Scholar
  8. Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant–plant protection mutualisms. Ecology 90:2384–2392PubMedCrossRefGoogle Scholar
  9. Chamberlain SA, Rudgers JA (2012) How do plants balance multiple mutualists? Correlations among traits for attracting protective bodyguards and pollinators in cotton (Gossypium). Evol Ecol 26:65–77CrossRefGoogle Scholar
  10. Galen C (1999) Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. Bioscience 49:631–640CrossRefGoogle Scholar
  11. Gomez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am Nat 162:242–256PubMedCrossRefGoogle Scholar
  12. Goss K, Moger TM, Nielson A, Carmona-Galindo VD (2011) Investigation of castor bean investment in extra-floral nectary glands and reproduction. Bios 82:43–45CrossRefGoogle Scholar
  13. 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 Lond B 274:2951–2957CrossRefGoogle Scholar
  14. Holland JN, Chamberlain SA, Miller TEX (2011) Consequences of ants and extrafloral nectar for pollinating seed-consuming mutualism: ant satiation, floral distraction, or plant defense? Oikos 120:381–388CrossRefGoogle Scholar
  15. Holway DA (1998) Factors governing rate of invasion: a natural experiment using Argentine ants. Oecologia 115:206–212CrossRefGoogle Scholar
  16. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  17. Ingram S (2008) Cacti, agaves, and yuccas of California and Nevada. Cachuma, Los OlivosGoogle Scholar
  18. Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743CrossRefGoogle Scholar
  19. Junker R, Chung AYC, Bluthgen N (2007) Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecol Res 22:665–670CrossRefGoogle Scholar
  20. Junker RR, Daehler CC, Doetterl S, Keller A, Bluethgen N (2011) Hawaiian ant-flower networks: nectar-thieving ants prefer undefended native over introduced plants with floral defenses. Ecol Monogr 81:295–311CrossRefGoogle Scholar
  21. Kay AD, Zumbusch T, Heinen JL, Marsh TC, Holway DA (2010) Nutrition and interference competition have interactive effects on the behavior and performance of Argentine ants. Ecology 91:57–64PubMedCrossRefGoogle Scholar
  22. Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474CrossRefGoogle Scholar
  23. Lach L (2003) Invasive ants: unwanted partners in ant–plant interactions? Ann Mo Bot Gard 90:91–108CrossRefGoogle Scholar
  24. Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994–2004PubMedCrossRefGoogle Scholar
  25. Lach L (2008a) Argentine ants displace floral arthropods in a biodiversity hotspot. Divers Distrib 14:281–290CrossRefGoogle Scholar
  26. Lach L (2008b) Floral visitation patterns of two invasive ant species and their effects on other hymenopteran visitors. Ecol Entomol 33:155–160CrossRefGoogle Scholar
  27. Lach L, Hoffmann BD (2011) Are invasive ants better plant-defense mutualists? A comparison of foliage patrolling and herbivory in sites with invasive yellow crazy ants and native weaver ants. Oikos 120:9–16CrossRefGoogle Scholar
  28. Ludka JT (2009) Protection and reliability: an examination of the quality and quantity of ant protection in the food-for-protection mutualism between Ferocactus viridescens, Crematogaster californica and the invasive Linepithema humile. Masters thesis, Division of Biology, University of California, San Diego, Ann Arbor, USAGoogle Scholar
  29. Messina FJ (1981) Plant-protection as a consequence of an ant–membracid mutualism—interactions on goldenrod (Solidago sp.). Ecology 62:1433–1440CrossRefGoogle Scholar
  30. Morris WF, Wilson WG, Bronstein JL, Ness JH (2005) Environmental forcing and the competitive dynamics of a guild of cactus-tending ant mutualists. Ecology 86:3190–3199CrossRefGoogle Scholar
  31. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514CrossRefGoogle Scholar
  32. Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Invasions 6:445–461CrossRefGoogle Scholar
  33. Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87:912–921PubMedCrossRefGoogle Scholar
  34. Newell W, Barber TC (1913) The Argentine ant. USDA Bur Entomol Bull 122:98Google Scholar
  35. Oliveira PS, Rico-Gray V, Diaz-Castelazo C, Castillo-Guevara C (1999) Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in opuntia stricta (Cactaceae). Funct Ecol 13:623–631CrossRefGoogle Scholar
  36. Palmer TM et al (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci USA 107:17234–17239PubMedCrossRefGoogle Scholar
  37. Romero GQ, Antiqueira PAP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS ONE 6:e20689PubMedCentralPubMedCrossRefGoogle Scholar
  38. Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant–plant mutualism. Ecology 85:192–205CrossRefGoogle Scholar
  39. Sipes SD, Tepedino VJ (2005) Pollen-host specificity and evolutionary patterns of host switching in a clade of specialist bees (Apoidea: Diadasia). Biol J Linn Soc 86:487–505CrossRefGoogle Scholar
  40. Sipura M (2002) Contrasting effects of ants on the herbivory and growth of two willow species. Ecology 83:2680–2690CrossRefGoogle Scholar
  41. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol S 35:435–466Google Scholar
  42. Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J Ecol 92:132–141CrossRefGoogle Scholar
  43. Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199CrossRefGoogle Scholar
  44. Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46:68–74CrossRefGoogle Scholar
  45. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216PubMedCrossRefGoogle Scholar
  46. Visser D, Wright MG, Giliomee JH (1996) The effect of the Argentine ant, Linepithema humile (Mayr) (Hymenoptera, Formicidae) on flower-visiting insects of Protea nitida mill (Proteaceae). Afr Entomol 4:285–287Google Scholar
  47. Wagner D, Kay A (2002) Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evol Ecol Res 4:293–305Google Scholar
  48. Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  49. Willmer PG et al (2009) Floral volatiles controlling ant behaviour. Funct Ecol 23:888–900CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Katherine E. LeVan
    • 1
    Email author
  • Keng-Lou James Hung
    • 1
  • Kyle R. McCann
    • 1
  • John T. Ludka
    • 1
  • David A. Holway
    • 1
  1. 1.Section of Ecology, Behavior, and Evolution, Division of Biological SciencesUniversity of California, San DiegoLa JollaUSA

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