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Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis

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Abstract

The antibiotic hypothesis proposes that ant pollination is rare at least in part because the cuticular antimicrobial secretions of ants are toxic to pollen grains. We tested this hypothesis by comparing the effects of ants and bees on pollen in two regions: a tropical rainforest in Amazonian Peru and temperate forests and old fields in Canada. We found support for three predictions that follow from the antibiotic hypothesis. (1) For all 10 ant and 11 plant species in our study, contact with ants significantly reduced pollen germination, confirming the generality of this effect. (2) Contact with two bee species did not have similar effects; pollen exposed to bees germinated as well as control pollen. (3) Consistent with the presumed greater abundance of entomopathogens in the tropics, which may have selected for stronger antibiotic secretions in tropical ants, tropical ants had more negative effects on pollen than temperate ants. We speculate that the antibiotic hypothesis contributes not only to the rarity but also to the biogeography of ant pollination, and we discuss whether the negative effects of ants on pollen have resulted in selection for floral defenses against ants.

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References

  • Adler L (2000) The ecological significance of toxic nectar. Oikos 91:409–420

    Article  Google Scholar 

  • 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 71:421–426

    Article  Google Scholar 

  • Beattie AJ, Turnbull CT, Hough T, Jobson S, Knox RB (1985) The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. Am J Bot 72:606–614

    Article  Google Scholar 

  • Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Fla Entomol 53:229–232

    Article  Google Scholar 

  • Bot ANM, Ortius-Lechner D, Finster K, Maile R, Boomsma JJ (2002) Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc 49:363–370

    Article  Google Scholar 

  • Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865

    Article  CAS  Google Scholar 

  • de Vega C, Arista M, Ortiz PL, Herrera CM, Talavera S (2009) The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite. Ann Bot 103:1065–1075

    Article  PubMed  Google Scholar 

  • Feinsinger P, Swarm LA (1978) How common are ant-repellent nectars? Biotropica 10:238–239

    Article  Google Scholar 

  • Fernández-Marín H, Zimmerman JK, Rehner SA, Wcislo WT (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc B 273:1689–1695

    Article  PubMed  Google Scholar 

  • Galen C, Butchart B (2003) Ants in your plants: effects of nectar-thieves on pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosum. Oikos 101:521–528

    Article  Google Scholar 

  • Garcia MB, Antor RJ, Espadaler X (1995) Ant pollination of the palaeoendemic dioecious Borderea pyrenaica (Dioscoreaceae). Plant Syst Evol 198:17–27

    Article  Google Scholar 

  • Ghazoul J (2001) Can floral repellents pre-empt potential ant-plant conflicts? Ecol Lett 4:295–299

    Article  Google Scholar 

  • Gomez JM, Zamora R (1992) Pollination by ants: consequences of the quantitative effects on a mutualistic system. Oecologia 91:410–418

    Article  Google Scholar 

  • Graystock P, Hughes WOH (2011) Disease resistance in a weaver ant, Polyrhachis dives, and the role of antibiotic-producing glands. Behav Ecol Sociobiol 65:2319–2327

    Article  Google Scholar 

  • Guernier V, Hochberg ME, Guégan J-F (2004) Ecology drives the worldwide distribution of human diseases. PLoS Biol 2:0740–0746

    Article  CAS  Google Scholar 

  • Guerrant EO, Fiedler PL (1981) Flower defenses against nectar-pilferage by ants. Biotropica 13:25–33

    Article  Google Scholar 

  • Haber WA, Frankie GW, Baker HG, Baker I, Koptur S (1981) Ants like floral nectar. Biotropica 13:211–214

    Article  Google Scholar 

  • Harris FLC, Beattie AJ (1991) Viability of pollen carried by Apis mellifera L., Trigona carbonaria Smith and Vespula germanica (F.) (Hymenoptera: Apidae, Vespidae). J Aust Entomol Soc 30:45–47

    Article  Google Scholar 

  • Herrera CM (1987) Components of pollinator ‘quality’: comparative analysis of a diverse insect assemblage. Oikos 50:79–90

    Article  Google Scholar 

  • Hickman JC (1974) Pollination by ants: a low-energy system. Science 184:1290–1292

    Article  PubMed  CAS  Google Scholar 

  • Hoffman AA, Clancy DJ, Merton E (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136:993–999

    Google Scholar 

  • Hoggard SJ, Wilson PD, Beattie AJ, Stow AJ (2011) Social complexity and nesting habits are factors in the evolution of antimicrobial defences in wasps. PLoS ONE 6:e21763

    Article  PubMed  CAS  Google Scholar 

  • Hölldobler B, Engel-Siegel H (1984) On the metapleural gland of ants. Psyche 91:201–224

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Hull DA, Beattie AJ (1988) Adverse effects on pollen exposed to Atta texana and other North American ants: implications for ant pollination. Oecologia 75:153–155

    Article  Google Scholar 

  • Janzen DH (1977) Why don’t ants visit flowers? Biotropica 9:252

    Article  Google Scholar 

  • Junker RR, Blüthgen N (2008) Floral scents repel potentially nectar-thieving ants. Evol Ecol Res 10:295–308

    Google Scholar 

  • Junker RR, Daehler CC, Dötterl S, Keller A, Blüthgen N (2011) Hawaiian ant-flower networks: nectar-thieving ants prefer undefended native over introduced plants with floral defenses. Ecol Monogr 81:295–311

    Article  Google Scholar 

  • Lach L (2005) Interference and exploitation competition of three nectar-thieving ant species. Insectes Soc 52:257–262

    Article  Google Scholar 

  • Ness JH, Morin DF, Giladi I (2009) Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists? Oikos 118:1793–1804

    Article  Google Scholar 

  • Nicklen EF, Wagner D (2006) Conflict resolution in an ant-plant interaction: Acacia constricta traits reduce ant costs to reproduction. Oecologia 148:81–87

    Article  PubMed  Google Scholar 

  • Nunn CL, Altizer SM, Sechrest W, Cunningham AA (2005) Latitudinal gradients of parasite species richness in primates. Divers Distrib 11:249–256

    Article  Google Scholar 

  • Peakall R, Beattie AJ (1989) Pollination of the orchid Microtis parviflora R. Br. by flightless worker ants. Funct Ecol 3:515–522

    Article  Google Scholar 

  • Peakall R, Angus CJ, Beattie AJ (1990) The significance of ant and plant traits for ant pollination in Leporella fimbriata. Oecologia 84:457–460

    Google Scholar 

  • Pitman NCA (2008) An overview of the Los Amigos watershed, Madre de Dios, southeastern Peru. http://cicra.acca.org.pe/espanol/paisaje_biodiversidad/los-amigos-overview9.pdf

  • Poulsen M, Bot ANM, Nielsen MG, Boomsma JJ (2002) Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behav Ecol Sociobiol 52:151–157

    Article  Google Scholar 

  • Proctor M, Yeo P (1972) The Pollination of Flowers. Taplinger Publishing Company, New York

    Google Scholar 

  • Puterbaugh M (1998) The role of ants as flower visitors: experimental analysis in three alpine plant species. Oikos 83:36–46

    Article  Google Scholar 

  • Rader R, Edwards W, Westcott DA, Cunningham SA, Howlett BG (2011) Pollen transport differs among bees and flies in a human-modified landscape. Divers Distrib 17:519–529

    Article  Google Scholar 

  • Raine NE, Willmer P, Stone GN (2002) Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in a Mexican ant-acacia. Ecology 83:3086–3098

    Google Scholar 

  • Ramsey M (1995) Ant pollination of the perennial herb Blandfordia grandiflora (Liliaceae). Oikos 74:265–272

    Article  Google Scholar 

  • Richards JS, Stanley JN, Gregg PC (2005) Viability of cotton and canola pollen on the proboscis of Helicoverpa armigera: implications for spread of transgenes and pollination ecology. Ecol Entomol 30:327–333

    Article  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago

    Google Scholar 

  • Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269

    Article  Google Scholar 

  • Stow AJ, Beattie A (2008) Chemical and genetic defenses against disease in insect societies. Brain Behav Immun 22:1009–1013

    Article  PubMed  CAS  Google Scholar 

  • Stow A, Briscoe D, Gillings M, Holley M, Smith S, Leys R, Silberbauer T, Turnbull C, Beattie A (2007) Antimicrobial defences increase with sociality in bees. Biol Lett 3:422–424

    Article  PubMed  Google Scholar 

  • Stow A, Turnbull C, Gillings M, Smith S, Holley M, Silberbauer L, Wilson PD, Briscoe D, Beattie A (2010) Differential antimicrobial activity in response to the entomopathogenic fungus Cordyceps in six Australian bee species. Aust J Entomol 49:145–149

    Article  Google Scholar 

  • Thomson J (2003) When is it mutualism? Am Nat 162:S1–S9

    Article  PubMed  Google Scholar 

  • Thorp RW (2000) The collection of pollen by bees. Plant Syst Evol 222:211–223

    Article  Google Scholar 

  • Turillazzi S, Mastrobuoni G, Dani FR, Moneti G, Pieraccini G, la Marca G (2006) Dominulin A and B: two new antibacterial peptides identified on the cuticle and in the venom of the social paper wasp Polistes dominulus using MALDI-TOF, MALDI-TOF/TOF, and ESI-Ion trap. J Am Soc Mass Spectrom 17:376–383

    Article  PubMed  CAS  Google Scholar 

  • Veal DA, Trimble JE, Beattie AJ (1992) Antimicrobial properties of secretions from the metapleural glands of Myrmecia gulosa (the Australian bull ant). J Appl Bacteriol 72:188–194

    Article  PubMed  CAS  Google Scholar 

  • Wagner D (2000) Pollen viability reduction as a potential cost of ant association for Acacia constricta (Fabaceae). Am J Bot 87:711–715

    Article  PubMed  CAS  Google Scholar 

  • Walker TN, Hughes WOH (2011) Arboreality and the evolution of disease resistance in ants. Ecol Entomol 36:588–595

    Article  Google Scholar 

  • Weir TL, Newbold S, Vivanco JM, van Haren M, Fritchman C, Dossey AT, Bartram S, Boland W, Cosio EG, Kofer W (2011) Plant-inhabiting ant uses chemical cues for host discrimination. Biotropica. doi:10.1111/j.1744-7429.2011.00786.x

    Google Scholar 

  • Willmer PG, Stone GN (1997) How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388:165–167

    Article  CAS  Google Scholar 

  • Willmer PG, Nuttman CV, Raine NE, Stone GN, Pattrick JG, Henson K, Stillman P, McIlroy L, Potts SG, Knudsen JT (2009) Floral volatiles controlling ant behaviour. Funct Ecol 23:888–900

    Article  Google Scholar 

  • Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507

    Article  Google Scholar 

  • Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev 86:774–791

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Lina Arcila Hernández, Adam Cembrowski, Antonio Coral, Eddie Ho, Gabriel Miller, and Jon Sanders for field/laboratory assistance; Frank Azorsa Salazar, Laurence Packer, and Claus Rasmussen for identifying our Peruvian ants and bee; Takashi Makino, Alison Parker, and James Thomson for their comments and for supplying the B. impatiens; the residents of Port Whitby for allowing us to collect flowers; the directors and staff at CICRA/the Amazon Conservation Association and the Koffler Scientific Reserve at Jokers Hill for logistics and permission to work at these sites; and the Peruvian Ministry of Agriculture for issuing a research permit (No. 299-2011-AG-DGFFS-DGEFFS). We are also grateful to the AE and two anonymous reviewers for their comments on an earlier draft. A Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to MEF funded this research; EMD was also supported by an NSERC Undergraduate Student Research Award.

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  1. University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Emily M. Dutton

  2. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord Street, Toronto, ON, M5S 3G5, Canada

    Megan E. Frederickson

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  1. Emily M. Dutton
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Correspondence to Megan E. Frederickson.

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Dutton, E.M., Frederickson, M.E. Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis. Arthropod-Plant Interactions 6, 561–569 (2012). https://doi.org/10.1007/s11829-012-9201-8

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  • DOI: https://doi.org/10.1007/s11829-012-9201-8

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