, Volume 186, Issue 3, pp 601–610 | Cite as

Keystone mutualism strengthens top–down effects by recruiting large-bodied ants

  • Robert E. ClarkEmail author
  • Michael S. Singer
Highlighted Student Research


Determining the impacts of mutualistic interactions and predator diversity on food webs are two important goals in community ecology. In this study, we examined how predator community variation mediates the strength of top–down effects in the presence and absence of mutualistic interactions. We examined the impacts of predatory ant species that simultaneously prey on leaf-chewing herbivores (Lepidoptera) and engage in food-for-protection mutualisms with sap-feeding herbivores (Hemiptera) in the lower canopy of Connecticut forests. In this 2-year study, we examined three hypothetical mechanisms by which mutualisms can alter the top–down effects of ants: (1) sap feeders increase ant abundance, thus strengthening predatory effects; (2) sap feeders increase the relative abundance of a species that has stronger predatory effects; and (3) changes to predator diversity (species richness) are caused by sap feeders mediating top–down effects of the ant community. Experiments revealed that host plants occupied by sap feeders favored large-bodied ant species in the genus Camponotus, but there were no changes to community-wide ant abundance or ant species richness. Fitting predictions of predation strength based on the functional trait of body size, large-bodied Camponotus suppressed caterpillars and reduced leaf herbivory. This work shows that the ant–hemipteran mutualism, which has been characterized as a keystone interaction, can generate strong top–down effects on leaf-chewing herbivores and herbivory via increasing the relative abundance of species with functional traits relevant to predation, such as body size. Therefore, the emergence of specific ants as keystone predators in a community can be contingent upon their mutualism with sap-feeding Hemiptera.


Predator–prey interactions Mutualism Food webs Ants Caterpillars 



This work was supported by an NSF Doctoral Dissertation Improvement Grant DEB-1404177. We thank Jacob Feder, Erin Smith, Henok Alemu, Mattheau Comerford, Taiga Araki, Max Atkinson, Pierre Gerard, and Delaine Winn for assistance in fieldwork, curation of specimens, and collection of data in spring and summers of 2013–2015. Sonia E. Sultan, Frederick M. Cohan, and Manuel A. Morales provided helpful feedback on design and analysis of experiments. Matthew S. Wallace and Mark J. Rothschild aided in identification of Membracidae and Coccidae specimens. We thank Carmen Blubaugh and three anonymous reviewers for helpful feedback on the previous versions of this manuscript.

Author contribution statement

REC ran field experiments and performed statistical analyses. Both REC and MSS designed experiments, participated in fieldwork, evaluated experimental results, and wrote and revised manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2017_4047_MOESM1_ESM.docx (922 kb)
Supplementary material 1 (DOCX 922 kb)


  1. Atlegrim O (2005) Indirect effects of ant predation (Hymenoptera: Formicidae) on bilberry Vaccinium myrtillus. Eur J Entomol 102:175–180CrossRefGoogle Scholar
  2. Barber NA, Marquis RJ (2009) Spatial variation in top-down direct and indirect effects on white oak (Quercus alba L.). Am Midl Nat 162:169–179CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, et al (2015) lme4: linear mixed-effects models using “Eigen” and S4Google Scholar
  4. Beckerman AP, Uriarte M, Schmitz OJ (1997) Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proc Natl Acad Sci USA 94:10735–10738CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146CrossRefPubMedGoogle Scholar
  6. Blüthgen N, Verhaagh M, Goitía W et al (2000) How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229–240. CrossRefPubMedGoogle Scholar
  7. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. CrossRefPubMedGoogle Scholar
  8. Clark RE, Farkas TE, Lichter-Marck I, Johnson ER, Singer MS (2016) Multiple interaction types determine the impact of ant predation of caterpillars in a forest community. Ecology 97:3379–3388CrossRefPubMedGoogle Scholar
  9. Crider KK (2011) Predator interference with the cinnabar moth (tyria jacobaeae) for the biological control of tansy ragwort (senecio jacobaea). Invasive Plant Sci Manag 4:332–340. CrossRefGoogle Scholar
  10. Davenport JM, Chalcraft DR (2013) Nonconsumptive effects in a multiple predator system reduce the foraging efficiency of a keystone predator. Ecol Evol 3:3063–3072CrossRefPubMedPubMedCentralGoogle Scholar
  11. Davidson DW (1998) Resource discovery versus resource domination in ants: a functional mechanism for breaking the trade-off. Ecol Entomol 23:484–490CrossRefGoogle Scholar
  12. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538CrossRefPubMedGoogle Scholar
  13. Ellison AM, Gotelli NJ, Farnsworth EJ, Alpert GD (2012) A field guide to the ants of New England. Yale University Press, New HavenGoogle Scholar
  14. Emmerson MC, Raffaelli D (2004) Predator–prey body size, interaction strength, and the stability of a real food web. J Anim Ecol 73:399–409CrossRefGoogle Scholar
  15. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soule ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–306CrossRefPubMedGoogle Scholar
  16. Fox J, Weisberg S, Adler D, et al (2015) Car: companion to applied regressionGoogle Scholar
  17. Griffin JN, De la Haye KL, Hawkins SJ, Thompson RC, Jenkins SR (2008) Predator diversity and ecosystem functioning: density modifies the effect of resource partitioning. Ecology 89:298–305CrossRefPubMedGoogle Scholar
  18. Griffin JN, Toscano BJ, Griffen BD, Silliman BR (2015) Does relative abundance modify multiple predator effects? Basic Appl Ecol 16:641–651. CrossRefGoogle Scholar
  19. Grover CD, Dayton KC, Menke SB, Holway DA (2008) Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods. Ecol Entomol 33:101–106Google Scholar
  20. Heck KL, Pennock JR, Valentine JF, Coen LD, Sklenar SA (2000) Effects of nutrient enrichment and small predatory density on seagrass ecosystems: an experimental assessment. Limnol Oceanogr 45:1041–1057CrossRefGoogle Scholar
  21. Helms KR, Hayden CP, Vinson SB (2011) Plant-based food resources, trophic interactions among alien species, and the abundance of an invasive ant. Biol Invasions 13:67–79CrossRefGoogle Scholar
  22. Hӧlldobler B, Wilson EO (1990) The ants. Belknap Press, CambridgeCrossRefGoogle Scholar
  23. Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. CrossRefGoogle Scholar
  24. Lenth RV (2016) Least-Squares Means: The R Package lsmeans. J Stat Soft 69(1):1–33CrossRefGoogle Scholar
  25. Ito F, Higashi S (1991) An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol 60:463–470. CrossRefGoogle Scholar
  26. Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116CrossRefGoogle Scholar
  27. Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649CrossRefGoogle Scholar
  28. Karhu KJ, Neuvonen S (1998) wood ants and a geometrid defoliator of birch: predation outweighs beneficial effects through the host plant. Oecologia 113:509–516CrossRefPubMedGoogle Scholar
  29. Kotze DJ, O’Hara RB, Lehvävirta S (2012) Dealing with varying detection probability, unequal sample sizes and clumped distributions in count data. PLoS One 7:e40923CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015) Global patterns in background losses of woody plant foliage to insects. Glob Ecol Biogeogr 24:1126–1135CrossRefGoogle Scholar
  31. Lach L, Parr CL, Abbott KL (2010) Ant ecology. Oxford University Press, OxfordGoogle Scholar
  32. Langsrud Ø (2003) ANOVA for unbalanced data: use Type II instead of Type III sums of squares. Stat Comput 13:163–167CrossRefGoogle Scholar
  33. Lefcheck JS, Duffy JE (2015) Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. Ecology 96:2973–2983. CrossRefPubMedGoogle Scholar
  34. Lichtenberg JS, Lichtenberg DA (2003) Predation of caterpillars on understory saplings in an Ozark forest. Southeast Nat 2:423–432CrossRefGoogle Scholar
  35. Long EY, Finke DL (2014) Contribution of predator identity to the suppression of herbivores by a diverse predator assemblage. Environ Entomol 43:569–576. CrossRefPubMedGoogle Scholar
  36. Marquis RJ (2010) The role of herbivores in terrestrial trophic cascades. In: Terborgh J, Estes JA (eds). Trophic Cascades, Island Press, pp 109–124Google Scholar
  37. Marshall MR, Cooper RJ (2004) Territory size of a migratory songbird in response to caterpillar density and foliage structure. Ecology 85:432–445. CrossRefGoogle Scholar
  38. McCoy MW, Stier AC, Osenberg CW (2012) Emergent effects of multiple predators on prey survival: the importance of depletion and the functional response. Ecol Lett 15:1449–1456CrossRefPubMedGoogle Scholar
  39. Menge B, Berlow E, Blanchette C, Navarrete S, Yamada S (1994) The keystone species concept—variation in interaction strength in a rocky intertidal habitat. Ecol Monogr 64:249–286CrossRefGoogle Scholar
  40. Messina FJ (1981) Plant protection as a consequence of an Ant-Membracid Mutualism: Interactions on Goldenrod (Solidago Sp.). Ecology 62:1433–1440. CrossRefGoogle Scholar
  41. Mestre L, Bucher R, Entling MH (2014) Trait-mediated effects between predators: ant chemical cues induce spider dispersal. J Zool 293:119–125. CrossRefGoogle Scholar
  42. Montllor CB, Bernays EA (1992) Invertebrate predators: how they constrain caterpillar feeding strategies. In: Stamp NE, Casey TM (eds) Caterpillars: Ecological and evolutionary constraints on foraging. Chapman and Hall, NYGoogle Scholar
  43. Nahas L, Gonzaga MO, Del-Claro K (2012) Emergent impacts of ant and spider interactions: herbivory reduction in a tropical savanna tree. Biotropica 44:498–505CrossRefGoogle Scholar
  44. Ness JH, Morris WF, Bronstein JL (2006) Variation in mutualistic potential among ant species tending extrafloral nectaries of Ferocactus wislizeni. Ecology 87:912–921CrossRefPubMedGoogle Scholar
  45. Oksanen FJ, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E and Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-4.
  46. Pohlert T (2016) The pairwise multiple comparison of mean ranks package (PMCMR). R package, Accessed 6 Jan 2017
  47. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Google Scholar
  48. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  49. Rosumek FB, Silveira FAO, Neves FDS, Barbosa NPDU, Diniz L, Oki Y, Pezzini F, Fernandes GW, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549CrossRefPubMedGoogle Scholar
  50. Rouabah A, Lasserre-Joulin F, Amiaud B, Plantureux S (2014) Emergent effects of ground beetles size diversity on the strength of prey suppression. Ecol Entomol 39:47–57CrossRefGoogle Scholar
  51. Rudolf VW (2006) The influence of size-specific indirect interactions in predator–prey systems. Ecology 87:362–371CrossRefPubMedGoogle Scholar
  52. Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426CrossRefPubMedGoogle Scholar
  53. Schmitz OJ (2009) Effects of predator functional diversity on grassland ecosystem function. Ecology 90:2339–2345CrossRefPubMedGoogle Scholar
  54. Silliman BR, Bertness MD (2002) A trophic cascade regulates salt marsh primary production. Proc Natl Acad Sci 99(16):10500–10505CrossRefPubMedPubMedCentralGoogle Scholar
  55. Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Annu Rev Ecol Syst 22:115–143CrossRefGoogle Scholar
  56. Sinclair ARE, Mduma S, Brashares JS (2003) Patterns of predation in a diverse predator–prey system. Nature 425:288. CrossRefPubMedGoogle Scholar
  57. Singer MS, Farkas TE, Skorik Christian M, Mooney KA (2012) Tritrophic interactions at a community level: effects of host plant species quality on bird predation of caterpillars. Am Nat 179:363–374CrossRefPubMedGoogle Scholar
  58. Singer MS, Clark RE, Lichter-Marck IH, Johnson ER, Mooney KA (2017) Predatory birds and ants partition caterpillar prey by body size and diet breadth. J Anim Ecol. PubMedGoogle Scholar
  59. Skinner GJ, Whittaker JB (1981) An Experimental Investigation of Inter-Relationships Between the Wood Ant (Formica rufa) and Some Tree-Canopy Herbivores. Journal of Animal Ecology 50:313–326. CrossRefGoogle Scholar
  60. Snyder WE, Snyder GB, Finke DL, Straub CS (2006) Predator biodiversity strengthens herbivore suppression. Ecol Lett 9:789–796CrossRefPubMedGoogle Scholar
  61. Sokol-Hessner L, Schmitz OJ (2002) Aggregate effects of multiple predator species on a shared prey. Ecology 83:2367–2372CrossRefGoogle Scholar
  62. Soomdat NN, Griffin JN, McCoy M, Hensel MJS, Buhler S, Chejanovski Z, Silliman BR (2014) Independent and combined effects of multiple predators across ontogeny of a dominant grazer. Oikos 123:1081–1090CrossRefGoogle Scholar
  63. Stadler AB, Dixon FG (2008) Mutualism: ants and their insect partners. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  64. Steiner CF (2001) The effects of prey heterogeneity and consumer identity on the limitation of trophic-level biomass. Ecology 82:2495–2506CrossRefGoogle Scholar
  65. Straub CS, Snyder WE (2006) Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology 87:277–282CrossRefPubMedGoogle Scholar
  66. Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B Biol Sci 274:151–164CrossRefGoogle Scholar
  67. Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199CrossRefGoogle Scholar
  68. Terborgh J, Estes DJA (eds) (2010) Trophic cascades: predators, prey, and the changing dynamics of nature, 2nd edn. Island Press, Washington DCGoogle Scholar
  69. Weis JJ (2015) The role of species diversity in bottom-up and top-down interactions. In: Hanley TC, La Pierre KJ (eds) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial ecosystems. Cambridge University Press, Cambridge, pp 318–339CrossRefGoogle Scholar
  70. Wielgoss A, Tscharntke T, Rumede A, Fiala B, Seidel H, Shahabuddin S, Clough Y (2014) Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems. Proc R Soc Lond B Biol Sci 281:20132144CrossRefGoogle Scholar
  71. Wilder SM, Barnum TR, Holway DA, Suarez AV, Eubanks MD (2013) Introduced fire ants can exclude native ants from critical mutualist-provided resources. Oecologia 72:197–205CrossRefGoogle Scholar
  72. Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biology DepartmentWesleyan UniversityMiddletownUSA

Personalised recommendations