, Volume 186, Issue 3, pp 691–701 | Cite as

Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub

  • Javier Ibarra-Isassi
  • Paulo S. OliveiraEmail author
Plant-microbe-animal interactions - original research


Animal-pollinated plants can be susceptible to changes in pollinator availability. Honeydew-producing treehoppers frequently occur on inflorescences, potentially enhancing ant-mediated negative effects on pollination services. However, the effect of ant-attended, honeydew-producing insects on plant reproduction remains uncertain. We recorded the abundance of treehoppers and ants on Byrsonima intermedia (Malpighiaceae), and monitored floral visitors in a Brazilian cerrado savanna. We manipulated the presence of ants and ant–treehopper associations on inflorescences to assess their effect on pollination and fruit formation. We used dried ants pinned to inflorescences to evaluate the effect of ant presence and ant identity on potential pollinators. Results show that the presence of treehoppers increases ant abundance on flowers and disrupts pollination by oil-collecting bees, decreasing the frequency and duration of floral visits and reducing fruit and seed set. Treehopper herbivory has no direct effect on fruit or seed production, which are independent of treehopper density. Pinned ants promote avoidance by floral visitors, reducing the number of visits. Ant identity mediates visitation decisions, with Ectatomma brunneum causing greater avoidance by floral visitors than Camponotus rufipes. Field videos show that pollinating bees are harassed by ants near flowers, prompting avoidance behavior by the bees. This is the first demonstration of indirect effects by honeydew-gathering ants, via disrupted pollination, on plant reproduction in tropical cerrado savanna. Our results highlight the importance of studying other interactions near flowers, in addition to just observing pollinators, for a proper understanding of plant reproduction.


Ant–plant–herbivore interaction Byrsonima Cerrado savanna Oil-collecting bees Flower avoidance behavior 



We thank A. Freitas, S. Sendoya, R. Cogni, M. Vidal, A. Nogueira, C. Vieira, and M. Azevedo-Silva for reading early drafts of the manuscript. The final version was considerably improved by comments from S. Koptur, L. Lach, S. Murphy, and M. Pareja. Constructive criticisms from the handling editor, S. Whitehead, and two anonymous reviewers greatly enhanced the revised manuscript. A. Tacioli helped in the field, and S. Sendoya assisted with the statistical analyses. We also thank M. Azevedo-Silva for help with the figures, and H. Soares Jr for editing the videos and for the flower photo. JI-I was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and the São Paulo Research Foundation (2014/12486-8); PSO was supported by the São Paulo Research Foundation (2014/23141-1), and the Brazilian Research Council (306115/2013-1).

Author contribution statement

JI-I and PSO conceived and designed the experiments. JI-I performed the experiments and analyzed the data. JI-I and PSO wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (MPEG 34182 kb)
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Supplementary material 2 (DOCX 233 kb)
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Supplementary material 3 (DOCX 18 kb)
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Supplementary material 4 (DOCX 18 kb)


  1. Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant–pollinator interaction network. Oikos 117:1796–1807CrossRefGoogle Scholar
  2. Altshuler D (1999) Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest. Oecologia 119:600–606CrossRefPubMedGoogle Scholar
  3. Alves-Silva E (2011) Post-fire resprouting of Banisteriopsis malifolia (Malpighiaceae) and the role of extrafloral nectaries on the associated ant fauna in a Brazilian savanna. Sociobiology 58:327–339Google Scholar
  4. Ballantyne G, Willmer P (2012) Nectar theft and floral ant-repellence: a link between nectar volume and ant-repellent traits? PLoS ONE 7:e43869CrossRefPubMedPubMedCentralGoogle Scholar
  5. Barton K (2016) MuMIn: Multi-model inference. R package version 1.15.6. Accessed 21 Nov 2017
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Beattie AJ (2007) The evolution of ant pollination systems. Botanische Jahrbücher Systematik 127:43–55CrossRefGoogle Scholar
  8. Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. Am J Bot 71:421–426CrossRefGoogle Scholar
  9. Bleil R, Blüthgen B, Junker RR (2011) Ant–plant mutualism in Hawai‘i? Invasive ants reduce flower parasitism but also exploit floral nectar of the endemic shrub Vaccinium reticulatum (Ericaceae). Pac Sci 65:291–300CrossRefGoogle Scholar
  10. Boas JCV, Fava WS, Laroca S, Sigrist MR (2013) Two sympatric Byrsonima species (Malpighiaceae) differ in phenological and reproductive patterns. Flora 208:360–369CrossRefGoogle Scholar
  11. Canedo-Júnior EO, Santiago GS, Ribas CR, Zurlo LF, Cuissi RG, Souza B, Faria LD, Rabello AM, Braga DD, Silva E (2017) The effect size of aphid-tending ants in an agricultural tri-trophic system. J Appl Entomol 00:1–10. Google Scholar
  12. Cembrowski AR, Tan MG, Thomson JD, Frederickson ME (2014) Ants and ant scent reduce bumblebee pollination of artificial flowers. Am Nat 183:133–139CrossRefPubMedGoogle Scholar
  13. de Vega C, Gómez JM (2014) Polinización por hormigas: conceptos, evidencias y futuras direcciones. Ecosistemas 23:48–57CrossRefGoogle Scholar
  14. de Vega C, Herrera CM (2013) Microorganisms transported by ants in duce changes in floral nectar composition of an ant-pollinated plant. Am J Bot 100:792–800CrossRefPubMedGoogle Scholar
  15. Del-Claro K, Oliveira PS (1996) Honeydew flicking by treehoppers provides cues to potential tending ants. Anim Behav 51:1071–1075CrossRefGoogle Scholar
  16. Del-Claro K, Oliveira PS (2000) Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124:156–165CrossRefPubMedGoogle Scholar
  17. Dutton EM, Frederickson ME (2012) Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis. Arthropod-Plant Interact 6:561–569CrossRefGoogle Scholar
  18. Gonzálvez FG, Santamaría L, Corlett RT, Rodríguez-Gironés MA (2013) Flowers attract weaver ants that deter less effective pollinators. J Ecol 101:78–85CrossRefGoogle Scholar
  19. Hanna C, Naughton I, Boser C, Alarcón R, Hung KLJ, Holway D (2015) Floral visitation by the Argentine ant reduces bee visitation and plant seed set. Ecology 96:222–230CrossRefPubMedGoogle Scholar
  20. Horvitz CC, Schemske DW (1984) Effects of ants and an ant-tended herbivore on seed production of a neotropical herb. Ecology 65:1369–1378CrossRefGoogle Scholar
  21. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  22. Ibarra-Isassi J, Sendoya SF (2016) Ants as floral visitors of Blutaparon portulacoides (A. St-Hil.) Mears (Amaranthaceae): an ant pollination system in the Atlantic Rainforest. Arthropod-Plant Interact 10:221–227CrossRefGoogle Scholar
  23. Junker RR, Chung AYC, Blüthgen N (2007) Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecology 22:665–670CrossRefGoogle Scholar
  24. Kaminski LA, Freitas AVL, Oliveira PS (2010) Interaction between mutualisms: ant–tended butterflies exploit enemy-free space provided by ant–treehopper associations. Am Nat 176:322–334CrossRefPubMedGoogle Scholar
  25. Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649CrossRefGoogle Scholar
  26. Keeler KH (1977) The extrafloral nectaries of Ipomoea carnea (Convolvulaceae). Am J Bot 64:1182–1188CrossRefGoogle Scholar
  27. Lach L (2003) Invasive ants: unwanted partners in ant–plant interactions? Ann Mo Bot Gard 90:91–108CrossRefGoogle Scholar
  28. Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by argentine ants. Ecology 88:1994–2004CrossRefPubMedGoogle Scholar
  29. Lach L (2008) Floral visitation patterns of two invasive ant species and their effects on other hymenopteran visitors. Ecol Entomol 33:155–160CrossRefGoogle Scholar
  30. Lau JA, Galloway LF (2004) Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae). Oecologia 141:577–583CrossRefPubMedGoogle Scholar
  31. LeVan KE, Holway DA (2015) Ant–aphid interactions increase ant floral visitation and reduce plant reproduction via decreased pollinator visitation. Ecology 96:1620–1630CrossRefGoogle Scholar
  32. Li J, Wang Z, Tan K, Qu Y, Nieh JC (2014) Giant Asian honeybees use olfactory eavesdropping to detect and avoid ant predators. Anim Behav 97:69–76CrossRefGoogle Scholar
  33. Lopes BC (1995) Treehoppers (Homoptera, Membracidae) in southeastern Brazil: use of host plants. Revista Brasileira de Zoologia 12:595–608CrossRefGoogle Scholar
  34. Messina FJ (1981) Plant protection as a consequence of ant–membracid mutualism: interactions on Goldenrod (Solidago sp.). Ecology 62:1433–1440CrossRefGoogle Scholar
  35. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  36. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514CrossRefGoogle Scholar
  37. Ness JH, Morris WF, Bronstein JL (2009) For ant-protected plants, the best defense is a hungry offense. Ecology 90:2823–2831CrossRefPubMedGoogle Scholar
  38. Ohm JR, Miller TEX (2014) Balancing anti-herbivore benefits and anti-pollinator costs of defensive mutualists. Ecology 95:2924–2935CrossRefGoogle Scholar
  39. Oliveira PS (1997) The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct Ecol 11:323–330CrossRefGoogle Scholar
  40. Oliveira PS, Del-Claro K (2005) Multitrophic interactions in a neotropical savanna: ant–hemipteran systems, associated insect herbivores and a host plant. In: Burslem DFRP, Pinard MA, Hartley SE (eds) Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge University Press, Cambridge, pp 414–438CrossRefGoogle Scholar
  41. Oliveira MIB, Polido CA, Costa LC, Fava WS (2007) Sistema reprodutivo e polinização de Byrsonima intermedia A. Juss. (Malpighiaceae) em Mato Grosso do Sul, Brasil. Revista Brasileira de Biociências 5:756–758Google Scholar
  42. Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira PS, Marquis RJ (eds) The cerrado of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120CrossRefGoogle Scholar
  43. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  44. Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TPJ, Goheen R, Pringle RM (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci USA 107:17234–17239CrossRefPubMedPubMedCentralGoogle Scholar
  45. Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect ecology: behavior, populations and communities. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  46. Pringle EG, Dirzo R, Gordon DM (2011) Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree. Ecology 92:37–46CrossRefPubMedGoogle Scholar
  47. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  48. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Rico-Gray V, Castro G (1996) Effect of an ant–aphid interaction on the reproductive fitness of Paullinia fuscecens (Sapindaceae). Southwest Nat 41:434–440Google Scholar
  50. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  51. Rico-Gray V, Thien LB (1989) Ant–mealybug interaction decreases reproductive fitness of Schomburgkia tibicinis (Orchidaceae) in Mexico. J Trop Ecol 5:109–112CrossRefGoogle Scholar
  52. Romero GQ, Antiqueira PP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behavior. PLoS ONE 6:e20689CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rosenheim JA, Wilhoit LR, Goodell PB, Grafton-Cardwell EE, Leigh TF (1997) Plant compensation, natural biological control, and herbivory by Aphis gossypii on pre-reproductive cotton: the anatomy of a non-pest. Entomol Exp Appl 85:45–63CrossRefGoogle Scholar
  54. Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New YorkCrossRefGoogle Scholar
  55. Sendoya SF, Freitas AVL, Oliveira PS (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am Nat 174:134–140CrossRefPubMedGoogle Scholar
  56. Sidhu CS, Wilson-Rankin EE (2016) Honey bees avoiding ant harassment at flowers using scent cues. Environ Entomol 45:420–426CrossRefGoogle Scholar
  57. Sigrist MR, Sazima M (2004) Pollination and reproductive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Ann Bot 94:33–41CrossRefPubMedPubMedCentralGoogle Scholar
  58. Souto LS, Oliveira DMT (2005) Morphology, anatomy, and development of Byrsonima intermedia A. Juss. (Malpighiaceae) fruit and seed. Braz J Bot 28:697–712CrossRefGoogle Scholar
  59. Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274:151–164CrossRefPubMedGoogle Scholar
  60. Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199CrossRefGoogle Scholar
  61. Tsuji K, Hasyim A, Nakamura K (2004) Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators. Ecol Res 19:669–673CrossRefGoogle Scholar
  62. Vidal MC, Sendoya SF, Oliveira PS (2016) Mutualism exploitation: predatory drosophilid larvae sugar-trap ants and jeopardize facultative ant–plant mutualism. Ecology 97:1650–1657CrossRefPubMedGoogle Scholar
  63. Wang Y, Wang S (2015) Persistence of pollination mutualisms in the presence of ants. Bull Math Biol 77:202–229CrossRefPubMedGoogle Scholar
  64. Wang Y, Wu H (2015) Stability of plant–pollinator–ant co-mutualism. Appl Math Comput 261:231–241Google Scholar
  65. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060CrossRefGoogle Scholar
  66. 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 B 281:20132144CrossRefPubMedPubMedCentralGoogle Scholar
  67. Zanchetta D, Reis CM, Delgado JM, Silva CEF, de Luca EF, Fernandes FD, Lutgens HD, Tannus JLS, Pinheiro LD, Martins MRC, Sawaya R (2006) Plano de Manejo Integrado. Estações Ecológica e Experimental de Itirapina-SP. Primeira Revisão. Instituto Florestal, São PauloGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Departamento de Biologia AnimalUniversidade Estadual de CampinasCampinasBrazil
  2. 2.Department of BiologyConcordia UniversityMontrealCanada

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