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The function of ant repellence by flowers: testing the “nectar protection” and “pollinator protection” hypotheses

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Abstract

According to the “nectar protection” and “pollinator protection” hypotheses, ant repellents in flowers have evolved to prevent ants from exploiting floral nectar and chasing away pollinators, respectively. We used weaver ants, Oecophylla smaragdina, to determine the strength of ant repellence in 32 bee-pollinated plant species and used the comparative method to test whether nectar production, size of pollinating bees and plant growth form were related to floral repellence. Flowers were more likely to repel ants if they offered nectar as a reward and were pollinated by small bees than if they were nectarless and pollinated by large bees. Furthermore, tree flowers were more likely than shrub or vine flowers to repel ants. Our results validate the pollinator protection hypothesis and the nectar protection hypothesis. Depending on the ecological context, therefore, ant repellents can function as direct or indirect exploitation barriers: they can prevent ants from removing nectar without effecting pollination (direct barriers) and, when flowers are pollinated by large bees, the absence of ant repellents—or even the presence of ant attractants—can result in ants chasing small ineffective pollinators away (indirect barriers).

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References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) 2nd international symposium on information theory. Budapest, Akademia Kiado, pp 267–281

    Google Scholar 

  • Ballantyne G, Willmer P (2012) Nectar theft and floral ant-repellence: a link between nectar volume and ant-repellent traits? PLoS ONE 7(8):10

    Article  Google Scholar 

  • Baroni Urbani C, de Andrade ML (1997) Pollen eating, storing, and spitting by ants. Naturwissenschaften 84(6):256–258

    Article  CAS  Google Scholar 

  • Bista S, Shivakoti K (2011) Honeybee flora at Kabre, Dolakha District. Nepal Agric Res J 4–5:18–25

  • Bluthgen N, Fiedler K (2004) Competition for composition: lessons from nectar-feeding ant communities. Ecology 85(6):1479–1485

    Article  Google Scholar 

  • Bremer B, Bremer K, Chase MW et al (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141(4):399–436

    Article  Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65(1):23–35

    Article  Google Scholar 

  • Corbet SA, Willmer PG (1980) Pollination of the yellow passionfruit—nectar, pollen and carpenter bees. J Agric Sci 95:655–666

    Article  Google Scholar 

  • Crozier RH, Newey PS, Schluns EA, Robson SKA (2010) A masterpiece of evolution—Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecol News 13:57–71

    Google Scholar 

  • Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61(2):153–181

    Article  Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300(5621):969–972

    Article  CAS  PubMed  Google Scholar 

  • Dejean A, Corbara B, Orivel J, Leponce M (2007) Rainforest Canopy Ants: the implications of territoriality and predatory behavior. Funct Ecosyst Commun 1(2):105–120

    Google Scholar 

  • Devall MS, Thien LB (1989) Factors influencing the reproductive success of Ipomoea pes-caprae (Convolvulaceae) around the Gulf of Mexico. Am J Bot 76(12):1821–1831

    Article  Google Scholar 

  • Devy MS, Davidar P (2003) Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. Am J Bot 90(4):650–657

    Article  PubMed  Google Scholar 

  • Dulberger R (1981) The floral biology of Cassia didymobotrya and Cassia auriculata (Caesalpiniaceae). Am J Bot 68(10):1350–1360

    Article  Google Scholar 

  • Efloras (2008) Missouri Botanical Garden, St. Louis, MO and Harvard University Herbaria, Cambridge, MA. http://www.efloras.org. Accessed February 2014

  • Endress PK (1996) Diversity and evolutinary biology of tropical flowers. Cambridge University Press, Cambridge

    Google Scholar 

  • Fiala B, Krebs SA, Barlow HS, Maschwitz U (1996) Interactions between the climber Thunbergia grandiflora, its pollinator Xylocopa latipes and the ant Dolichoderus thoracicus: the “nectar-thief hypothesis” refuted? Malay Nat J 50(1):1–14

    Google Scholar 

  • Galen C (1999) Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85(3):426–434

    Article  Google Scholar 

  • Galen C, Cuba J (2001) Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55(10):1963–1971

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Gómez JM, Zamora R (1992) Pollination by ants—consequences of the quantitative effects on a mutualistic system. Oecologia 91(3):410–418

    Article  Google Scholar 

  • Gómez JM, Zamora R, Hodar JA et al (1996) Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105(2):236–242

    Article  Google Scholar 

  • Gonzálvez FG, Rodríguez-Gironés MA (2013) Seeing is believing: information content and behavioural response to visual and chemical cues. Proc Biol Sci R Soc 280(1763):20130886

    Article  Google Scholar 

  • Gonzálvez FG, Santamaría L, Corlett RT et al (2013) Flowers attract weaver ants that deter less effective pollinators. J Ecol 101:78–85

    Article  Google Scholar 

  • Harley R (1991) The greasy pole syndrome. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 430–433

    Google Scholar 

  • Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206

    Article  CAS  PubMed  Google Scholar 

  • Inc StatSoft (2011) Electronic statistics textbook. StatSoft, Tulsa

    Google Scholar 

  • Janzen DH (1966) Coevolution of mutualism between ants and Acacias in Central America. Evolution 20(3):249–275

    Article  Google Scholar 

  • Junker RR, Bluthgen N (2008) Floral scents repel potentially nectar-thieving ants. Evol Ecol Res 10(2):295–308

    Google Scholar 

  • Junker RR, Chung YC, Bluthgen N (2007) Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecol Res 22(4):665–670

    Article  Google Scholar 

  • Junker RR, Daehler CC, Dotterl S et al (2011) Hawaiian ant-flower networks: nectar-thieving ants prefer undefended native over introduced plants with floral defenses. Ecol Monogr 81(2):295–311

    Article  Google Scholar 

  • Kato M (2000) Anthophilous insect community and plant–pollinator interactions on Amami Islands in the Ryukyu Archipelago, Japan. Contrib Biol Lab Kyoto Univ 29(2):157–254

    Google Scholar 

  • Kato M, Kosaka Y, Kawakita A et al (2008) Plant–pollinator interactions in tropical monsoon forests in Southeast Asia. Am J Bot 95(11):1375–1394

    Article  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149(4):646–667

    Article  Google Scholar 

  • McDade LA, Daniel TF, Kiel CA (2008) Toward a comprehensive understanding of phylogenetic relationships among lineages of Acanthaceae s.l. (Lamiales). Am J Bot 95(9):1136–1152

    Article  PubMed  Google Scholar 

  • Momose K, Yumoto T, Nagamitsu T et al (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant–pollinator community in a lowland dipterocarp forest. Am J Bot 85(10):1477–1501

    Article  CAS  PubMed  Google Scholar 

  • Murali KS (1993) Differential reproductive success in Cassia fistula in different habitats—a case of pollinator limitation. Curr Sci 65(3):270–272

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Offenberg J, Havanon S, MacIntosh D et al (2004a) Observations on the ecology of weaver ants (Oecophylla smaragdina Fabricius) in a Thai mangrove ecosystem and their effect on herbivory of Rhizophora mucronata Lam. Biotropica 36:344–351

    Google Scholar 

  • Offenberg J, Nielsen MG, MacIntosh DJ et al (2004b) Evidence that insect herbivores are deterred by ant pheromones. Proc R Soc Lond B 271:S433–S435

    Article  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401(6756):877–884

    Article  CAS  PubMed  Google Scholar 

  • Parker IM, Lopez I, Petersen JJ et al (2010) Domestication syndrome in Caimito (Chrysophyllum cainito L.): fruit and seed characteristics. Econ Bot 64(2):161–175

    Article  PubMed Central  PubMed  Google Scholar 

  • Pascarella JB (1997) Breeding systems of Ardisia Sw (Myrsinaceae). Brittonia 49(1):45–53

    Article  Google Scholar 

  • Punekar SA, Kumaran NKP, Bhat HR (2010) Observations on an unusual behaviour in the carpenter bee Xylocopa aestuans (Latreille, 1802) (Hymenoptera: Apidae) of the Wetern Ghats, India. J Threat Taxa 2(10):1232–1233

    Article  Google Scholar 

  • R Development Core Team (2010) R: a language and evironment for statistical computing. R Foundation for Statistical Computing, Vienna

    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(11):3086–3096

    Google Scholar 

  • Raju AJS, Rao SP (2006) Nesting habits, floral resources and foraging ecology of large carpenter bees (Xylocopa latipes and Xylocopa pubescens) in India. Curr Sci 90(9):1210–1217

    Google Scholar 

  • Reddi CS, Das RK, Aluri RJS, Aluri JB (1996) Sexual system and pollination ecology of Gmelina asiatica L. (Vervenaceae). J Palynol 32:41–50

    Google Scholar 

  • Rodriguez-Girones MA, Santamaria L (2005) Resource partitioning among flower visitors and evolution of nectar concealment in multi-species communities. Proc R Soc B Biol Sci 272(1559):187–192

    Article  Google Scholar 

  • Rodríguez-Gironés MA, Gonzálvez FG, Llandres AL et al (2013) Possible role of weaver ants, Oecophylla smaragdina, in shaping plant–pollinator interactions in South-East Asia. J Ecol 101(4):1000–1006

  • Romero GQ, Antiqueira PAP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS ONE 6(6):9

    Article  Google Scholar 

  • Schaeferhoff B, Fleischmann A, Fischer E et al (2010) Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evol Biol 10:352

  • Singh G (2004) Plant systematics: an integrated approach. Science Publishers Inc, New York

    Google Scholar 

  • Siqueira de Castro M (2002) Bee fauna of some tropical and exotic fruits: potencial pollinators and their conservation. In: Kevan P, Fonseca VI (eds) Pollinating bees—the consevation link between agriculture and nature. Ministry of Envirinment, Brasilia

    Google Scholar 

  • Thomas SG, Rehel SM, Varghese A et al (2009) Social bees and food plant associations in the Nilgiri Biosphere Reserve, India. Trop Ecol 50(1):79–88

    Google Scholar 

  • Thompson JN (1982) Interaction and coevolution. Wiley, New York

    Book  Google Scholar 

  • Tsuji K, Hasyim A, Harlion, Nakamura K (2004) Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators. Ecol Res 19(6):669–673

  • Van Mele P, Vayssieres JF, Abandonon A et al (2009) Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa. Physiol Entomol 34:256–261

    Article  Google Scholar 

  • Willmer PG, Stone GN (1997) How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388(6638):165–167

    Article  CAS  Google Scholar 

  • Willmer PG, Nuttman CV, Raine NE et al (2009) Floral volatiles controlling ant behaviour. Funct Ecol 23(5):888–900

    Article  Google Scholar 

  • Wojciechowski MF (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perpective. In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics. Royal Botanic Gardens, Kew, pp 5–35

    Google Scholar 

  • Wurdack KJ, Davis CC (2009) Malpiguiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 96(8):1551–1570

    Article  PubMed  Google Scholar 

  • Yamasaki E, Sakai S (2013) Wind and insect pollination (ambophily) of Mallotus spp. (Euphorbiaceae) in tropical and temperate forests. Aust J Bot 61(1):60–66

    Article  Google Scholar 

  • Yanoviak SP, Kaspari M (2000) Community structure and the habitat templet: ants in the tropical forest canopy and litter. Oikos 89(2):259–266

    Article  Google Scholar 

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Acknowledgments

We thank Oriol Verdeny for assistance with the statistical analysis. Three anonymous reviewers made useful comments on an earlier version of this manuscript. This work was supported by the Ministerio de Ciencia e Innovación/FEDER (projects CGL2007-63223/BOS and CGL2010-16795 to MARG) and CSIC (studentship JAE-Pre_08_01008 to FGG).

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  1. Estación Experimental de Zonas Áridas, EEZA-CSIC, Ctra. de Sacramento S/N, La Cañada de San Urbano, 04120, Almeria, Spain

    Francisco G. Gonzálvez & Miguel A. Rodríguez-Gironés

  2. Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, 666303, Yunnan, China

    J. Chen

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  1. Francisco G. Gonzálvez
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Correspondence to Francisco G. Gonzálvez.

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Gonzálvez, F.G., Chen, J. & Rodríguez-Gironés, M.A. The function of ant repellence by flowers: testing the “nectar protection” and “pollinator protection” hypotheses. Evol Ecol 29, 391–403 (2015). https://doi.org/10.1007/s10682-014-9742-7

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