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Multitasking in a plant–ant interaction: how does Acacia myrtifolia manage both ants and pollinators?

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Abstract

Plant associations with protective ants are widespread among angiosperms, but carry the risk that ants will deter pollinators as well as herbivores. Such conflict, and adaptations to ameliorate or prevent the conflict, have been documented in African and neotropical acacias. Ant–acacia associations occur in Australia, but little is known of their ecology. Moreover, recent phylogenetic evidence indicates that Australian acacias are only distantly related to African and American acacias, providing an intercontinental natural experiment in the management of ant–pollinator conflict. We examined four populations of Acacia myrtifolia over a 400-km environmental gradient in southeastern Australia using ant and pollinator exclusion as well as direct observation of ants and pollinators to assess the potential for ant–pollinator conflict to affect seed set. Native bees were the only group of floral visitors whose visitation rates were a significant predictor of fruiting success, although beetles and wasps may play an important role as “insurance” pollinators. We found no increase in pollinator visitation or fruiting success following ant exclusion, even with large sample sizes and effective exclusion. Because ants are facultative visitors to A. myrtifolia plants, their presence may be insufficient to interfere greatly with floral visitors. It is also likely that the morphological location of extrafloral nectaries tends to draw ants away from reproductive parts, although we commonly observed ants on inflorescences, so the spatial separation is not strict. A. myrtifolia appears to maintain a generalized mutualism over a wide geographic range without the need for elaborate adaptations to resolve ant–pollinator conflict.

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References

  • Andersen AN (1991) The ants of southern Australia: a guide to the Bassian fauna. CSIRO Publishing, Melbourne

    Google Scholar 

  • Andersen A (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. J Biogeogr 22:15–29. doi:10.2307/2846070

  • Australia’s Virtual Herbarium (2011) Australia’s Virtual Herbarium. http://avh.ala.org.au/search. Accessed 1 Sept 2011

  • Bernhardt P, Walker K (1984) Bee foraging on three sympatric species of Australian Acacia. Int J Entomol 26:322–330

    Google Scholar 

  • Bernhardt P, Walker K (1985) Insect foraging on Acacia retinodes var retinodes in Victoria, Australia. Int J Entomol 27:97–101

    Google Scholar 

  • Bernhardt P, Kenrick J, Knox RB (1984) Pollination biology and the breeding system of Acacia retinodes (Leguminosae, Mimosoideae). Ann Mo Bot Gard 71:17–29. doi:10.2307/2399054

    Article  Google Scholar 

  • Bleil R, Bluethgen N, 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 65:291–300. doi:10.2984/65.3.291

    Article  Google Scholar 

  • Bolton B (2013) An online catalog of the ants of the world. http://antcat.org. Accessed 10 Feb 2013

  • Boughton V (1981) Extrafloral nectaries of some australian phyllodineous acacias. Aust J Bot 29:653–664

    Article  Google Scholar 

  • Brown G, Murphy D, Miller J, Ladiges P (2008) Acacia s.s. and its relationship among tropical Legumes, tribe Ingeae (Leguminosae: Mimosoideae). Syst Bot 33:739–751

  • Buckley RC (1982) Ant–plant interactions: a world review. In: Buckley RC (ed) Ant–plant interactions in Australia. Dr. W. Junk, The Hague

  • Chamberlain SA, Holland JN (2008) Density-mediated, context-dependent consumer-resource interactions between ants and extrafloral nectar plants. Ecology 89:1364–1374

    Article  PubMed  Google Scholar 

  • Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant–plant protection mutualisms. Ecology 90:2384–2392. doi:10.1890/08-1490.1

    Article  PubMed  Google Scholar 

  • Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant–plant relationships. J Hymenopt Res 2:13–83

    Google Scholar 

  • Fisher BL (2010) Biogeography. In: Lach L, Parr CL, Abbott K (eds) Ant ecology. Oxford University Press, New York, pp 18–37

    Google Scholar 

  • Flora of Australia Online (2011) Flora of Australia Online. http://www.environment.gov.au/biodiversity/abrs/online-resources/flora/main/. Accessed 19 Aug 2011

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

  • González-Teuber M, Heil M (2009) The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists. J Chem Ecol 35:459–468. doi:10.1007/s10886-009-9617-4

    Article  PubMed  Google Scholar 

  • González-Teuber M, Eilmus S, Muck A, Svatos A, Heil M (2009) Pathogenesis-related proteins protect extrafloral nectar from microbial infestation. Plant J 58:464–473. doi:10.1111/j.1365-313X.2009.03790.x

    Article  PubMed  Google Scholar 

  • González-Teuber M, Silva Bueno JC, Heil M, Boland W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLoS One 7:e46598. doi:10.1371/journal.pone.0046598

    Article  PubMed Central  PubMed  Google Scholar 

  • Heil M, McKey D (2003) Protective ant–plant interactions as model systems in ecological and evolutionary research. Ann Rev Ecol Evol Syst 34:425–453

  • Heil M, Greiner S, Meimberg H, Krüger R, Noyer J-L, Heubl G, Linsenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Gonzalez-Teuber M, Clement LW, Kautz S, Verhaaghd M, Silva Bueno JC (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096. doi:10.1073/pnas.0904304106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275. doi:10.2307/2406628

    Article  Google Scholar 

  • Kautz S, Lumbsch HT, Ward PS, Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63:839–853

    Article  CAS  PubMed  Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biology. University Press of Colorado, Boulder

    Google Scholar 

  • Kenrick J (1994) Some aspects of the reproductive biology of Acacia. Ph.D. dissertation. Department of Botany, University of Melbourne, Melbourne

  • Knox RB, Kenrick J, Bernhardt P, Marginson R, Beresford G, Baker I, Baker HG (1985) Extrafloral nectaries as adaptations for bird pollination in Acacia terminalis. Am J Bot 72:1185–1196

    Article  Google Scholar 

  • Knox RB, Marginson R, Kenrick J, Beattie AJ (1986) The role of extrafloral nectaries in Acacia. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold, London, pp 293–307

    Google Scholar 

  • Lach L, Hobbs RJ, Majer JD (2009) Herbivory-induced extrafloral nectar increases native and invasive ant worker survival. Popul Ecol 51:237–243. doi:10.1007/s10144-008-0132-2

    Article  Google Scholar 

  • Luckow M, Miller JT, Murphy DJ, Livshultz T (2003) A phylogenetic analysis of the Mimosoideae (Leguminosae) based on chloroplast DNA sequence data. In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics, part 10: Higher level systematics. Royal Botanic Gardens, Kew, pp 197–220

  • Malé P-JG, Leroy C, Dejean A, Quilichini A, Orivel J (2012) An ant symbiont directly and indirectly limits its host plant’s reproductive success. Evol Ecol 26:55–63. doi:10.1007/s10682-011-9485-7

    Article  Google Scholar 

  • Marginson R, Sedgley M, Douglas TJ, Knox RB (1985) Structure and secretion of the extrafloral nectaries of Australian acacias. Isr J Bot 34:91–102

  • Martínez-Bauer AE (2014) The ecology of mutualism in Acacia myrtifolia. Ph.D. thesis. School of Biological Sciences, Monash University, Melbourne

  • Maslin BR, Miller JT, Seigler DS (2003) Overview of the generic status of Acacia (Leguminosae: Mimosoideae). Aust Syst Bot 16:1–18

  • Miller JT, Burd M (2014) Australia’s Acacia: unrecognized convergent evolution. In: Prins HHT, Gordon IJ (eds) Invasion biology and ecosystem theory: insights from a continent in transition. Cambridge University Press, Cambridge

    Google Scholar 

  • Moya-Raygoza G, Larsen KJ (2001) Temporal resource switching by ants between honeydew produced by the fivespotted gama grass leafhopper (Dalbulus quinquenotatus) and nectar produced by plants with extrafloral nectaries. Am Midl Nat 146:311–320

  • Murphy DJ (2008) A review of the classification of Acacia (Leguminosae, Mimosoideae). Muelleria 26:10–26

    Google Scholar 

  • Murphy DJ, Brown GK, Miller JT, Ladiges PY (2010) Molecular phylogeny of Acacia Mill. (Mimosoideae: Leguminosae): evidence for major clades and informal classification. Taxon 59:7–19

  • Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–551. doi:10.1111/j.2006.0030-1299.14143.x

    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

  • Prescott MN (2005) The pollination ecology of a south-eastern Australia Acacia community. Ph.D. dissertation. Department of Zoology, University of Oxford, Oxford

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Raine NE, Willmer P, Stone GN (2002) Spatial structuring and floral avoidance behavior prevent ant–pollinator conflict in a Mexican ant-Acacia. Ecology 83:3086–3096

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

    Book  Google Scholar 

  • Romero GQ, Antiqueira PAP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS One 6:e20689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shattuck S (1999) Australian ants: their biology and identification. CSIRO, Collingwood

  • Stiehl Alves EM, Marins-Corder MP (2009) Reproductive biology of Acacia mearnsii de Wild. (Fabaceae) IV: flower visitors. Rev Arvore 33:443–450

    Google Scholar 

  • Stone GN, Raine NE, Prescott M, Willmer PG (2003) Pollination ecology of acacias (Fabaceae, Mimosoideae). Aust Syst Bot 16:103–118. doi:10.1071/sb02024

    Article  Google Scholar 

  • Tandon R, Shivanna KR, Ram HYM (2001) Pollination biology and breeding system of Acacia senegal. Bot J Linn Soc 135:251–262. doi:10.1111/j.1095-8339.2001.tb01094.x

    Article  Google Scholar 

  • The Legume Phylogeny Working Group (2013) Legume phylogeny and classification in the 21st century: progress, prospects and lessons for other species-rich clades. Taxon 62:217–248. doi:10.12705/622.8

    Article  Google Scholar 

  • Thorp RW, Sugden EA (1990) Extrafloral nectaries producing rewards for pollinator attraction in Acacia longifolia (Andr.) Willd. Isr J Bot 39:177–186

    Google Scholar 

  • Tybirk K (1993) Pollination, breeding system and seed abortion in some African acacias. Bot J Linn Soc 112:107–137. doi:10.1111/j.1095-8339.1993.tb00312.x

    Article  Google Scholar 

  • Wagner D, Kay A (2002) Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evol Ecol Res 4:293–305

    Google Scholar 

  • Weber MG, Keeler KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 111:1251–1261

    Article  PubMed Central  PubMed  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 

  • Yu DW, Pierce NE (1998) A castration parasite of an ant–plant mutualism. Proc R Soc B 265:375–382

    Article  PubMed Central  Google Scholar 

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Acknowledgments

We thank the Department of Sustainability and Environment of Victoria for permission to conduct the research (permit#10005111), and Parks Victoria, especially the rangers, for their kind support at the individual parks. We also thank Ken Walker for the identification of flower visitors, Simon Hinkley for ant identification corroboration, Alejandra Morán Ordóñez for the sites map, and the anonymous reviewers and the handling editor, Martin Heil, for their valuable comments and suggestions. AMB was supported by a Postgraduate Scholarship from CONACyT (Consejo Nacional de Ciencia y Tecnología, México), SEP (Secretaría de Educación Pública, México) and a Dean’s Scholarship from the Monash University Faculty of Science. MB was supported by the National Evolutionary Synthesis Center, Durham, North Carolina, during the preparation of the manuscript.

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Correspondence to Angélica E. Martínez-Bauer.

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Communicated by Martin Heil.

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Martínez-Bauer, A.E., Martínez, G.C., Murphy, D.J. et al. Multitasking in a plant–ant interaction: how does Acacia myrtifolia manage both ants and pollinators?. Oecologia 178, 461–471 (2015). https://doi.org/10.1007/s00442-014-3215-0

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