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Oecologia

, Volume 172, Issue 3, pp 779–790 | Cite as

An ant’s-eye view of an ant-plant protection mutualism

  • M. C. LananEmail author
  • J. L. Bronstein
Plant-animal interactions - Original research

Abstract

Ant protection of extrafloral nectar (EFN)-secreting plants is a common form of mutualism found in most habitats around the world. However, very few studies have considered these mutualisms from the ant, rather than the plant, perspective. In particular, a whole-colony perspective that takes into account the spatial structure and nest arrangement of the ant colonies that visit these plants has been lacking, obscuring when and how colony-level foraging decisions might affect tending rates on individual plants. Here, we experimentally demonstrate that recruitment of Crematogaster opuntiae (Buren) ant workers to the EFN-secreting cactus Ferocactus wislizeni (Englem) is not independent between plants up to 5 m apart. Colony territories of C. opuntiae are large, covering areas of up to 5,000 m2, and workers visit between five and 34 EFN-secreting barrel cacti within the territories. These ants are highly polydomous, with up to 20 nest entrances dispersed throughout the territory and interconnected by trail networks. Our study demonstrates that worker recruitment is not independent within large polydomous ant colonies, highlighting the importance of considering colonies rather than individual workers as the relevant study unit within ant/plant protection mutualisms.

Keywords

Extrafloral nectar Mutualism Polydomy Social insects Foraging 

Notes

Acknowledgments

We would like to thank Joshua Ness and Bill Morris for their input throughout the design and conduct of these experiments. We also wish to thank David Holway, and all the members of the Bronstein lab group for their advice and comments on this manuscript. Carolyn Camp, Rebecca Ruppel, and Andrew Waser provided assistance in the field. This work was funded by an International Arid Lands Consortium (no. 03R-25) grant to Judith Bronstein, Ido Izhaki, and Ran Nathan, a University of Arizona Center for Insect Science grant to Michele Lanan, and a NIH Postdoctoral Excellence in Research and Teaching (PERT) fellowship to Michele Lanan. All experiments described herein comply with the laws of the country in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Anderson C, McShea DW (2001) Intermediate-level parts in insect societies: adaptive structures that ants build away from the nest. Insect Soc 48:291–301CrossRefGoogle Scholar
  2. Benson L (1982) The cacti of the United States and Canada. StanfordUniversity Press, StanfordGoogle Scholar
  3. Bluthgen N, Fiedler K (2004a) Competition for composition: lessons from nectar-feeding ant communities. Ecology 85:1479–1485CrossRefGoogle Scholar
  4. Bluthgen N, Fiedler K (2004b) Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. J Anim Ecol 73:155–166CrossRefGoogle Scholar
  5. Bluthgen N, Gottsberger G, Fiedler K (2004) Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecol 29:418–429CrossRefGoogle Scholar
  6. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51CrossRefGoogle Scholar
  7. Bronstein JL (1998) The contribution of ant plant protection studies to our understanding of mutualism. Biotropica 30:150–161CrossRefGoogle Scholar
  8. Byk J, Del-Claro F (2011) Ant-plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Popul Ecol 53:327–332CrossRefGoogle Scholar
  9. Chamberlain SA, Holland JN (2009a) Body size predicts degree in ant-plant mutualistic networks. Funct Ecol 23:196–202CrossRefGoogle Scholar
  10. Chamberlain SA, Holland JN (2009b) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384–2392PubMedCrossRefGoogle Scholar
  11. Cogni R, Freitas AVL, Oliveira PS (2003) Interhabitat differences in ant activity on plant foliage: ants at extrafloral nectaries of Hibiscus pernambucensis in sandy and mangrove forests. Entomol Exp Appl 107:125–131CrossRefGoogle Scholar
  12. Cuautle M, Rico-Gray V (2003) The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Funct Ecol 17:417–423CrossRefGoogle Scholar
  13. Cushman JH, Whitham TG (1991) Competition mediating the outcome of a mutualism: protective services of ants as a limiting resource for membracids. Am Nat 138:851–865Google Scholar
  14. Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153–181CrossRefGoogle Scholar
  15. Debout G, Schatz B, Elias M, McKey D (2007) Polydomy in ants: what we know, what we think we know, and what remains to be done. Biol J Linn Soc 90:319–348CrossRefGoogle Scholar
  16. Dejean A et al (2010) Spatial distribution of dominant arboreal ants in a malagasy coastal rainforest: gaps and presence of an invasive species. Plos One 5:e9319Google Scholar
  17. Diaz-Castelazo C, Guimaraes PR, Jordano P, Thompson JN, Marquis RJ, Rico-Gray V (2010) Changes of a mutualistic network over time: reanalysis over a 10-year period. Ecology 91:793–801PubMedCrossRefGoogle Scholar
  18. Dreisig H (2000) Defense by exploitation in the Florida carpenter ant, Camponotus floridanus, at an extrafloral nectar resource. Behav Ecol Sociobiol 47:274–279CrossRefGoogle Scholar
  19. Dutra HP, Freitas AVL, Oliveira PS (2006) Dual ant attraction in the neotropical shrub Urera baccifera (Urticaceae): the role of ant visitation to pearl bodies and fruits in herbivore deterrence and leaf longevity. Funct Ecol 20:252–260CrossRefGoogle Scholar
  20. Guimaraes PR, Rico-Gray V, dos Reis SF, Thompson JN (2006) Asymmetries in specialization in ant-plant mutualistic networks. Proc R Soc B Biol Sci 273:2041–2047CrossRefGoogle Scholar
  21. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453CrossRefGoogle Scholar
  22. Holland JN, Chamberlain SA, Horn KC (2009) Optimal defence theory predicts investment in extrafloral nectar resources in an ant-plant mutualism. J Ecol 97:89–96CrossRefGoogle Scholar
  23. Holldobler B, Lumsden CJ (1980) Territorial strategies in ants. Science 210:732–739PubMedCrossRefGoogle Scholar
  24. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  25. Holway DA, Case TJ (2000) Mechanisms of dispersed central-place foraging in polydomous colonies of the Argentine ant. Anim Behav 59:433–441PubMedCrossRefGoogle Scholar
  26. Inouye DW, Taylor OR Jr (1979) A temperate region plant-ant-seed predator system: consequences of extra floral nectar secretion by Helianthella quinquenervis. Ecology 60:1–7CrossRefGoogle Scholar
  27. Keeler KH (2008) World list of angiosperms with extrafloral nectaries. University of Nebraska, LincolnGoogle Scholar
  28. Lanan MC (2010) Collective decision-making and foraging in a community of desert ants. PhD dissertation, University of Arizona, TucsonGoogle Scholar
  29. Lenoir L (2003) Response of the foraging behaviour of red wood ants (Formica rufa group) to exclusion from trees. Agric For Entomol 5:183–189CrossRefGoogle Scholar
  30. Mathews CR, Bottrell DG, Brown JH (2011) Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on Peach (Rosales: Rosaceae). Environ Entomol 40:42–51PubMedCrossRefGoogle Scholar
  31. McIver JD (1991) Dispersed central place foraging in Australian meat ants. Insect Soc 38:129–137CrossRefGoogle Scholar
  32. Miller TEX (2007) Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116:500–512CrossRefGoogle Scholar
  33. Morales MA (2000) Survivorship of an ant-tended membracid as a function of ant recruitment. Oikos 90:469–476CrossRefGoogle Scholar
  34. 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
  35. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514CrossRefGoogle Scholar
  36. 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
  37. Ness JH, Morris WF, Bronstein JL (2009) For ant-protected plants, the best defense is a hungry offense. Ecology 90:2823–2831PubMedCrossRefGoogle Scholar
  38. 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
  39. Pfeiffer M, Linsenmair KE (1998) Polydomy and the organization of foraging in a colony of the Malaysian giant ant Camponotus gigas (Hym./Form.). Oecologia 117:579–590CrossRefGoogle Scholar
  40. Portha S, Deneubourg JL, Detrain C (2002) Self-organized asymmetries in ant foraging: a functional response to food type and colony needs. Behav Ecol 13:776–781CrossRefGoogle Scholar
  41. Prasad S, Sukumar R (2010) Context-dependency of a complex fruit-frugivore mutualism: temporal variation in crop size and neighborhood effects. Oikos 119:514–523CrossRefGoogle Scholar
  42. Quinet Y, Hamidi R, Ruiz-Gonzalez MX, de Biseau J-C, Longino JT (2009) Crematogaster pygmaea (Hymenoptera: Formicidae: Myrmicinae), a highly polygynous and polydomous Crematogaster from northeastern Brazil. Zootaxa 2075:45–54Google Scholar
  43. Rico-Gray V, Oliveira AT (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  44. Rosumek FB et al (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549PubMedCrossRefGoogle Scholar
  45. Rudgers JA, Gardener MC (2004) Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85:1495–1502CrossRefGoogle Scholar
  46. Saracco JF, Collazo JA, Groom MJ, Carlo TA (2005) Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37:81–87CrossRefGoogle Scholar
  47. Somanathan H, Borges RM, Chakravarthy VS (2004) Does neighborhood floral display matter? Fruit set in carpenter bee-pollinated Heterophragma quadriloculare and beetle-pollinated Lasiosiphon eriocephalus. Biotropica 36:139–147Google Scholar
  48. Steiner FM et al (2007) Abandoning aggression but maintaining self-nonself discrimination as a first stage in ant supercolony formation. Curr Biol 17:1903–1907PubMedCrossRefGoogle Scholar
  49. Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199CrossRefGoogle Scholar
  50. Tillberg CV, Breed MD (2004) Placing an omnivore in a complex food web: dietary contributions to adult biomass of an ant. Biotropica 36:266–272Google Scholar
  51. Trager MD et al (2010) Benefits for plants in ant-plant protective mutualisms: a meta-analysis. Plos One 5:e14308Google Scholar
  52. Wagner D, Nicklen EF (2010) Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: does extrafloral nectar attract ant nests and thereby enhance plant nutrition? J Ecol 98:614–624CrossRefGoogle Scholar
  53. Wilder SM, Holway D, Suarez AV, Eubanks MD (2011) Macronutrient content of plant-based food affects growth of a carnivorous arthropod. Ecology 92:325–332PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Arizona Research LabsUniversity of ArizonaTucsonUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

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