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Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity

  • Community ecology - Original Paper
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Abstract

Geographic variation in the outcome of interspecific interactions may influence not only the evolutionary trajectories of species but also the structure of local communities. We investigated this community consequence of geographic variation for a facultative mutualism between ants and wild cotton (Gossypium thurberi). Ants consume wild cotton extrafloral nectar and can protect plants from herbivores. We chose three sites that differed in interaction outcome, including a mutualism (ants provided the greatest benefits to plant fitness and responded to manipulations of extrafloral nectar), a potential commensalism (ants increased plant fitness but were unresponsive to extrafloral nectar), and a neutral interaction (ants neither affected plant fitness nor responded to extrafloral nectar). At all sites, we manipulated ants and extrafloral nectar in a factorial design and monitored the abundance, diversity, and composition of other arthropods occurring on wild cotton plants. We predicted that the effects of ants and extrafloral nectar on arthropods would be largest in the location with the mutualism and weakest where the interaction was neutral. A non-metric multidimensional scaling analysis revealed that the presence of ants altered arthropod composition, but only at the two sites in which ants increased plant fitness. At the site with the mutualism, ants also suppressed detritivore/scavenger abundance and increased aphids. The presence of extrafloral nectar increased arthropod abundance where mutual benefits were the strongest, whereas both arthropod abundance and morphospecies richness declined with extrafloral nectar availability at the site with the weakest ant–plant interaction. Some responses were geographically invariable: total arthropod richness and evenness declined by approximately 20% on plants with ants, and extrafloral nectar reduced carnivore abundance when ants were excluded from plants. These results demonstrate that a facultative ant–plant mutualism can alter the composition of arthropod assemblages on plants and that these community-level consequences vary across the landscape.

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References

  • Barton AM (1986) Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495–504

    Article  Google Scholar 

  • Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020

    Article  CAS  PubMed  Google Scholar 

  • Begon M, Townsend CR, Harper JL (2006) Ecology: individuals, populations, and communities, 4th edn. Blackwell, Malden

    Google Scholar 

  • Berenbaum MR, Zangerl AR (2006) Parsnip webworms and host plants at home and abroad: trophic complexity in a geographic mosaic. Ecology 12:3070–3081

    Article  Google Scholar 

  • Blüthgen N, Stork NE (2007) Ant mosaics in a tropical rainforest in Australia and elsewhere: a critical review. Austral Ecol 32:93–104

    Article  Google Scholar 

  • Brodie ED, Ridenhour BJ (2002) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082

    PubMed  Google Scholar 

  • Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Article  Google Scholar 

  • Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Article  Google Scholar 

  • Bronstein JL, Wilson WG, Morris WE (2003) Ecological dynamics of mutualist/antagonist communities. Am Nat 162:S24–S39

    Article  PubMed  Google Scholar 

  • Bronstein JL, Alarcon R, Geber M (2006) The evolution of plant-insect mutualisms. New Phytol 172:412–428

    Article  PubMed  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Cheney KL, Cote IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165

    Article  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2007) Primer, version 6.1.10: user manual and tutorial. Primer-E, Plymouth

    Google Scholar 

  • Clarke KR, Somerfield PJ, Airoldi LWRM (2006) Exploring interactions by second-stage community analyses. J Exp Mar Biol Ecol 338:179–192

    Article  Google Scholar 

  • Cuautle M, Rico-Gray V (2003) The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia. Funct Ecol 17:417–423

    Article  Google Scholar 

  • de la Fuente MAS, Marquis RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia (Berlin) 118:192–202

    Article  Google Scholar 

  • Despres L, Ibanez S, Hemborg AM, Godelle B (2007) Geographic and within-population variation in the globeflower-globeflower fly interaction: the costs and benefits of rearing pollinators’ larvae. Oecologia 151:240–250

    Article  PubMed  Google Scholar 

  • Di Giusto B, Anstett M, Dounias E, McKey DB (2001) Variation in the effectiveness of biotic defense: the case of an opportunistic ant-plant protection mutualism. Oecologia 129:367–375

    Google Scholar 

  • Edelaar P, Benkman CW (2006) Replicated population divergence caused by localized coevolution? A test of three hypotheses in the red crossbill-lodgepole pine system. J Evol Biol 19:1651–1659

    Article  CAS  PubMed  Google Scholar 

  • Elias M, Gompert Z, Jiggins C, Willmott K (2008) Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biology 6:2642–2649

    Article  CAS  PubMed  Google Scholar 

  • Fernandes GW, Fagundes M, Woodman RL, Price PW (1999) Ant effects on three-trophic level interactions: plant, galls, and parasitoids. Ecol Entomol 24:411–415

    Article  Google Scholar 

  • Fryxell PA (1979) The natural history of the cotton tribe. Texas A&M University Press, College Station

    Google Scholar 

  • Gaume L, McKey D, Terrin S (1998) Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host. Proc R Soc Lond B 265:569–575

    Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Gove AD, Rico-Gray V (2006) What determines conditionality in ant-Hemiptera interactions? Hemiptera habitat preference and the role of local ant activity. Ecol Entomol 31:568–574

    Article  Google Scholar 

  • Hanson HC (1923) Distribution of Arizona wild cotton. Arizona Exp Stn Tech Bull 3:48–59

    Google Scholar 

  • Hay ME et al (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu Rev Ecol Evol Syst 35:175–197

    Article  Google Scholar 

  • Horvitz CC, Schemske DW (1984) Effects of ants and an ant-tended herbivore on seed production of a neotropical herb. Ecology 65:1369–1378

    Article  Google Scholar 

  • Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649

    Article  Google Scholar 

  • Kersch MF, Fonseca CR (2005) Abiotic factors and the conditional outcome of an ant-plant mutualism. Ecology 86:2117–2126

    Article  Google Scholar 

  • Lach L (2008) Argentine ants displace floral arthropods in a biodiversity hotspot. Divers Distrib 14:281–290

    Article  Google Scholar 

  • Lukefahr MJ (1960) Effects of nectariless cottons on populations of three lepidopterous insects. J Econ Entomol 53:242–244

    Google Scholar 

  • Mathews CR, Bottrell DG, Brown MW (2009) Extrafloral nectaries alter arthropod community structure and mediate peach (Prunus persica) plant defense. Ecol Appl 19:722–730

    Article  PubMed  Google Scholar 

  • McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden Beach

    Google Scholar 

  • Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225

    Article  Google Scholar 

  • Mooney KA (2007) Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology 88:2005–2014

    Article  PubMed  Google Scholar 

  • Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514

    Article  Google Scholar 

  • Peterson MA (1995) Unpredictability in the facultative association between larvae of Euphilotes enoptes (Lepidoptera: Lycaenidae) and ants. Biol J Linn Soc 55:209–233

    Google Scholar 

  • Renault CK, Buffa LM, Delfino MA (2005) An aphid-ant interaction: effects on different trophic levels. Ecol Res 20:71–74

    Article  Google Scholar 

  • Rey PJ, Manzaneda AJ (2007) Geographical variation in the determinants of seed dispersal success of a myrmecochorous herb. J Ecol 95:1381–1393

    Article  Google Scholar 

  • Rico-Gray V, Palacios-Rios M, Garcia-Franco JG, Mackay WP (1998) Richness and seasonal variation of ant-plant associations mediated by plant-derived food resources in the semiarid Zapotitlan Valley, Mexico. Am Midl Nat 140:21–26

    Article  Google Scholar 

  • Rose USR, Lewis J, Tumlinson JH (2006) Extrafloral nectar from cotton (Gossypium hirsutum) as a food source for parasitic wasps. Funct Ecol 20:67–74

    Article  Google Scholar 

  • Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85:192–205

    Article  Google Scholar 

  • Rudgers JA, Clay K (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840

    Article  PubMed  Google Scholar 

  • Rudgers JA, Gardener MC (2004) Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85:1495–1502

    Article  Google Scholar 

  • Rudgers JA, Strauss SY (2004) A selection mosaic in the facultative mutualism between ants and wild cotton. Proc R Soc Lond B Biol Sci 271:2481–2488

    Google Scholar 

  • Rudgers JA, Hodgen JG, White JW (2003) Behavioral mechanisms underlie an ant-plant mutualism. Oecologia 135:51–59

    PubMed  Google Scholar 

  • Rudgers JA, Holah J, Orr SP, Clay K (2007) Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88:18–25

    Article  PubMed  Google Scholar 

  • SAS Institute (2004) SAS version 9.1.3. SAS Institute, Cary

    Google Scholar 

  • Savage AM, Peterson MA (2007) Mutualism in a community context: the positive feedback between an ant-aphid mutualism and a gall-making midge. Oecologia 151:280–291

    Article  PubMed  Google Scholar 

  • Schuster MF, Lukefahr MJ, Maxwell FG (1976) Impact of nectariless cotton on plant bugs and natural enemies. J Econ Entomol 69:400–402

    Google Scholar 

  • Smith RL, Flint HM (1977) A bibliography of the cotton leafperforator, Bucculatrix thurberiella, and a related species, Bucculatrix gossypiella, that also feeds on cotton (Lepidopteran: Lyonetiidae). Bull Entomol Soc Am 23:195–198

    Google Scholar 

  • Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246

    Article  Google Scholar 

  • Stapel JO (1997) Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Ann Entomol Soc Am 26:617–623

    Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc Lond B 274:151–164

    Google Scholar 

  • Taylor RM, Pfannenstiel RS (2008) Nectar feeding by wandering spiders on cotton plants. Environ Entomol 37:996–1002

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN, Fernandez CC (2006) Temporal dynamics of antagonism and mutualism in a geographically variable plant-insect interaction. Ecology 87:103–112

    Article  PubMed  Google Scholar 

  • Thrall PH, Slattery JF, Broadhurst LM, Bickford S (2007) Geographic patterns of symbiont abundance and adaptation in native Australian Acacia-rhizobia interactions. J Ecol 95:1110–1122

    Article  Google Scholar 

  • van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Google Scholar 

  • von Ende CN (2001) Repeated measures analysis: growth and other time dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 134–157

    Google Scholar 

  • Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82:440–452

    Google Scholar 

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Acknowledgments

We are indebted to R. Karban, who introduced us to the wild cotton system. Thanks are also extended to P. Ward (UC-Davis) and C. Olson, Associate Curator of the University of Arizona Insect Collection, for assistance with species identifications. J. Hodgen, W. White, C. Stephens, D. Hoyer, A. Stein, J. Howard, J. M. Rudgers, B. Bedard, and P. Murch provided invaluable field assistance. K. Whitney offered advice and help of many kinds. Thanks to S. Chamberlain, A. Dunham, J. Ness, M. Peterson, G. Wimp, and anonymous reviewers for improvements to this manuscript. This work was supported by an EPA S.T.A.R. fellowship and the Godwin Assistant Professorship to J.A.R. and a Wray-Todd fellowship to A.M.S. The research practices used for this study complied with all laws and regulations of the USA.

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  1. Megan A. Rúa

    Present address: Curriculum in Ecology, University of North Carolina-Chapel Hill, Chapel Hill, NC, 27599, USA

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  1. Department of Ecology and Evolutionary Biology, Rice University, 6100 Main Street, Houston, Texas, 77005, USA

    Jennifer A. Rudgers & Amy M. Savage

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  1. Jennifer A. Rudgers
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Correspondence to Jennifer A. Rudgers.

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Communicated by Volkmar Wolters.

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Rudgers, J.A., Savage, A.M. & Rúa, M.A. Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity. Oecologia 163, 985–996 (2010). https://doi.org/10.1007/s00442-010-1584-6

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