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Mutualism in a community context: the positive feedback between an ant–aphid mutualism and a gall-making midge

  • Community Ecology
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Abstract

Although mutualisms are widespread and often described in natural history accounts, their ecological influences on other community members remain largely unexplored. Many of these influences are likely a result of indirect effects. In this field study, we investigated the indirect effects of an ant–aphid mutualism on the abundance, survival rates and parasitism rates of a co-occurring herbivore. Rabdophaga salicisbrassicoides (Diptera: Cecidomyiidae) induces rosette galls on the developing shoots of Salix exigua trees, and populations can reach outbreak densities (up to 1,000 galls/stem) in central Washington State (USA). Ant-tended aphids feed on these same stems and often feed on gall tissue. In this study we used a combination of manipulative experiments and observational surveys to test the hypothesis that the abundances of aphids, ants, and galls have positive and reciprocal effects on one another, in a manner that would create a positive feedback loop in population growth. In addition, we examined whether the combined presence of ants and aphids reduces parasitism rates for the gallers. In support of the positive feedback loop hypothesis, aphids enjoyed higher population growth rates in the presence of ants and galls, the presence of ants and aphids resulted in increased abundance of galls, and the abundances of ants, aphids and galls were all positively correlated with one another. However, the mechanism underlying the positive effect of ants and aphids on galler density remains unknown, as the mutualism did not affect parasitism rates. More broadly, this study demonstrates that mutualisms can have significant and complex indirect effects on community and population ecology.

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References

  • Abrams PA (2003) Effects of altered resource consumption rates by one consumer species on a competitor. Ecol Lett 6:550–555

    Article  Google Scholar 

  • Analytical Software (2003) Statistix, version 8.0 for Windows. Tallahassee, Fla.

  • Banks CJ (1962) Effects of the ant Lasius niger (L.) on insects preying on small populations of Aphis fabae Scop. on bean plants. Ann Appl Biol 50:669–679

    Article  Google Scholar 

  • Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146

    Google Scholar 

  • Bluthgen N, Fiedler K (2002) Interactions between weaver ants Oecophylla smaragdina, homopterans, trees and lianas in an Australian rain forest canopy. J Anim Ecol 71:793–801

    Article  Google Scholar 

  • Bonsall MB, Hassell MP (1999) Parasitoid-mediated effects: apparent competition and persistence of host-parasitoid assemblages. Popul Ecol 41:59–68

    Article  Google Scholar 

  • Briggs CJ, Latto J (2000) The effect of dispersal on the population dynamics of a gall-forming midge and its parasitoids. J Anim Ecol 69:96–105

    Article  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 

  • Buckley RC (1987) Interactions involving ants, homoptera, and plants. Annu Rev Ecol Syst 18:111–135

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071

    Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    Article  PubMed  CAS  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  PubMed  CAS  Google Scholar 

  • Clancy KM, Price PW (1986) Temporal variation in three-trophic-level interactions among willows, sawflies, and parasites. Ecology 67:1601–1607

    Article  Google Scholar 

  • Compton SG, Robertson HG (1988) Complex interactions between mutualisms: ants tending homopterans protect fig seeds and pollinators. Ecology 69:1302–1305

    Article  Google Scholar 

  • Compton, SG, and Robertson HG (1991) Effects of ant-homopteran systems on fig–fig wasp interactions. In: Huxley C R, Cutler D F (eds) Ant–plant interactions. Oxford University Press, London, pp 120–130

  • Cushman JH, Compton SG, Zachariades C, Ware AB, Nefdt RJC, Rashbrook VK (1998) Geographic and taxonomic distribution of a positive interaction: ant-tended homopterans indirectly benefit figs across Southern Africa. Oecologia 116:373–380

    Article  Google Scholar 

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

    Article  Google Scholar 

  • DeClerck-Floate R, Price PW (1994) Impact of bud-galling midge on bud populations of Salix exigua. Oikos 70:253–260

    Article  Google Scholar 

  • Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331

    Article  CAS  Google Scholar 

  • Diaz BM, Fereres A (2004) Life table and population parameters of Nasonovia ribisnigri (Homoptera: Aphididae) at different constant temperatures. Environ Entomol 34:527–534

    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 

  • Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81:3522–3529

    Article  Google Scholar 

  • Fox JW, Olsen E (2000) Food web structure and the strength of transient indirect effects. Oikos 90:219–226

    Article  Google Scholar 

  • Fowler SV, Macgarvin M (1985) The impact of hairy wood ants, Formica lugubris, on the guild structure of herbivorous insects on birch, Betula pubescens. J Anim Ecol 54:847–855

    Article  Google Scholar 

  • Francoeur A (1973) Revision taxonomique des especes nearctiques du groupe fusca, genre Formica (Formicidae: Hymenoptera). Mem Soc Entomol Que 3:1–316

    Google Scholar 

  • Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE (2002) Oviposition tests of ant preference in a myrmecophilous butterfly. J Evol Biol 15:861–870

    Article  Google Scholar 

  • Girousse C, Faucher M, Kleinpeter C, Bonnemain JL (2003) Dissection of the effects of the aphid Acrythosiphon pisum feeding on assimilate partitioning in Medicago sativa. New Phytol 157:83–92

    Article  Google Scholar 

  • Girousse C, Moulia B, Silk W, Bonnemain JL (2005) Aphid infestation causes different changes in carbon and nitrogen allocation in alfalfa stems as well as different inhibitions of longitudinal and radial expansion. Plant Physiol 137:1474–1484

    Article  PubMed  CAS  Google Scholar 

  • Harris P, Shorthouse JD (1996) Effectiveness of gall inducers in weed biological control. Can Entomol 128:1021–1055

    Google Scholar 

  • Hay ME, Parker JD, Burkepile DE, Caudill CC, Wilson AE, Hallinan ZP, Chequer AD (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 

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

    Article  Google Scholar 

  • Hentz M, Nuessly G (2004) Development, longevity, and fecundity of Sipha flava (Homoptera: Aphididae) feeding on Sorghum bicolor. Environ Entomol 33:546–553

    Google Scholar 

  • Huxley CR, Cutler DF (eds) (1991) Ant–plant interactions. Oxford University Press, New York

    Google Scholar 

  • Inouye BD, Agrawal AA (2004) Ant mutualists alter the composition and functional response of parasitoids attacking the gall wasp Disholcaspis eldoradensis (Cynipidae). Ecol Entomol 29:692–696

    Article  Google Scholar 

  • Katayama N. Suzuki N (2003) Bodyguard effects of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae). Appl Entomol Zool 38:427–433

    Article  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kersting U, Satar S, Uygun N (1999) Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Hom., Aphididae) reared on Gossypium hirsutum L. J Appl Entomol 123: 23–27

    Google Scholar 

  • Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84:2302–2312

    Google Scholar 

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink–source interactions. Oecologia 88:1432–1439

    Article  Google Scholar 

  • Larsen KJ, Stahle LM, Dotseth EJ (2001) Tending ants (Hymenoptera: Formicidae) regulate Dalbulus quinquenotatus (Homoptera: Cicadellidae) population dynamics. Environ Entomol 30:757–762

    Google Scholar 

  • Letourneau DK, Dyer LA (1998) Experimental test in lowland tropical forest shows top–down effects through four trophic levels. Ecology 79:1678–1687

    Article  Google Scholar 

  • Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186

    Article  Google Scholar 

  • Martinez del Rio C, Silva A, Medel R, Hourdequin M (1996) Seed dispersers as disease vectors: bird transmission of mistletoe seeds to plant hosts. Ecology 77:912–921

    Article  Google Scholar 

  • McCornack BP, Ragsdale DW, Venette RC (2004) Demography of soybean aphid (Homoptera: Aphididae) at summer temperatures. J Econ Entomol 97:854–861

    Article  PubMed  CAS  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 

  • Morales MA (2002) Ant-dependent oviposition in the membracid Publilia concave. Ecol Entomol 27:247–250

    Article  Google Scholar 

  • Moran MD, Rooney TP, Hurd LE (1996) Top–down cascade from a bitrophic predator in an old-field community. Ecology 77:2219–2227

    Article  Google Scholar 

  • Nakamura M, Miyamoto Y, Ohgushi T (2003) Gall initiation enhances the availability of food resources for herbivorous insects. Funct Ecol 17:851–857

    Article  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA 97:13184–13187

    Article  PubMed  CAS  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Article  Google Scholar 

  • Peacor SD., Werner EE (2001) The contribution of indirect effects to the net effects of a predator. Proc Natl Acad Sci USA 98:3904–3908

    Article  PubMed  CAS  Google Scholar 

  • Pearson DE, Callaway KM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18: 456–461

    Article  Google Scholar 

  • Pemberton RW (1998) The occurrence and abundance of plants with extrafloral nectaries, the basis for antiherbivore defensive mutualisms along a latitudinal gradient in East Asia. J Biogeogr 25:661–668

    Article  Google Scholar 

  • Pierce NE, Elgar MA (1985) The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid butterfly. Behav Ecol Sociobiol 16:209–222

    Article  Google Scholar 

  • Price PW (1989) Clonal development of coyote willow, Salix exigua (Salicaceae), and attack by the shoot-galling sawfly Euura exiguae (Hymenoptera: Tenthredinidae). Ann Entomol Soc Am 18:61–68

    Google Scholar 

  • Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN, Mobley K (1986) Parasite mediation in ecological interactions. Annu Rev Ecol Syst 17:487–505

    Article  Google Scholar 

  • Raman A, Madhavan S, Florentine SK, Dhileepan K (2006) Metabolite mobilization in the stem galls of Parthenium hysterophorus induced by Epiblema strenuana inferred from the signatures of isotopic carbon and nitrogen and concentrations of total non-structural carbohydrates. Entomol Exp Appl 119:101–107

    Article  CAS  Google Scholar 

  • Richards WR (1972) Chaitophorinae of Canada (Homoptera: Aphididae). Entomological Society of Canada, Ottawa

  • SAS (2004) SAS statistical software version 9.3.1. SAS Institute, Cary, N.C.

  • Schmitt RJ, Holbrook SJ (2003) Mutualism can mediate competition and promote coexistence. Ecol Lett 6:898–902

    Article  Google Scholar 

  • Schmitz OJ, Hambalk PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153

    Article  PubMed  Google Scholar 

  • Shingleton AW, Stern DL (2003) Molecular phylogenetic evidence for multiple gains or losses of ant mutualism within the aphid genus Chaitophorus. Mol Phylogenet Evol 26:26–35

    Article  PubMed  CAS  Google Scholar 

  • Sih A, Crowley P, McPeek M, Petranka J, Strohmeiev K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York

    Google Scholar 

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

    Article  Google Scholar 

  • Stadler B, Dixon AFG (2005) Ecology and evolution of aphid–ant interactions. Annu Rev Ecol Evol Syst 36:345–372

    Article  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Syst 35:435–466

    Article  Google Scholar 

  • Sullivan DJ, Völkl W (1999) Hyperparasitism: multitrophic ecology and behavior. Annu Rev Entomol 44:291–315

    Article  PubMed  CAS  Google Scholar 

  • Tscharntke T (1992) Cascade effects among four trophic levels: bird predation on galls affects density-dependent parasitism. Ecology 73:1689–1698

    Article  Google Scholar 

  • Van Hezewijk BH, Roland J (2003) Gall size determines the structure of the Rabdophaga salicisbrassicoides host-parasitoid community. Ecol Entomol 28:593–603

    Article  Google Scholar 

  • Völkl W (1992) Aphids or their parasitoids: who actually benefits from ant attendance? J Anim Ecol 61:273–281

    Article  Google Scholar 

  • Völkl W, Kroupa AS (1997) Effects of adult mortality risks on parasitoid foraging tactics. Anim Behav 54:349–359

    Article  Google Scholar 

  • Walsh BD, Riley CV (1869) Galls and their architects. Am Entom 1:101–110

    Google Scholar 

  • Webster MS, Almany GR (2002) Positive indirect effects in a coral reef fish community. Ecol Lett 5:549–557

    Article  Google Scholar 

  • Weis AE (1984) Apical dominance asserted over lateral buds by the gall of Rhabdophaga strobiloides (Diptera: Cecidomyiidae). Can Entomol 116:1277–1279

    Article  Google Scholar 

  • Weis AE, Kapelinski A (1984) Manipulation of host plant development by the gall-midge Rhabdophaga strobiloides. Ecol Entomol 9:457–465

    Google Scholar 

  • Wilson LF (1968) Life history and habits of the pine cone willow midge, Rhabdophaga strobiloides (Diptera: Cecdomyiidae), in Michigan. Can Entomol 100:430–433

    Google Scholar 

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

    Article  Google Scholar 

  • Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466

    Article  Google Scholar 

  • Yao I, Shibao H, Akimoto SI (2000) Costs and benefits of ant attendance to the drapanosiphid aphid Tuberculatus quercicola. Oikos 89:3–10

    Article  Google Scholar 

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Acknowledgements

We thank K. Monsen, M. Brassil, H. Pedersen, E. Rose, S. Schwartz, K. Helm, S. Locke, K. Buckingham, E. Larson and D. Juarez for critical field assistance and stimulating discussions. Many thanks to R. Gagne for identifying Rabdophaga salicisbrassicoides (Diptera: Cecidomyiidae), K. Pike for identifying Chaitophorus utahensis (Homoptera: Aphididae), and J. Longino for identifying Formica neoclara (Hymenoptera: Formicidae). We also thank J. MacLaughlin, D. Hooper, G. Wimp, J. Rudgers, J. N. Holland and two anonymous reviewers for comments on previous drafts. These comments greatly improved the quality of this manuscript. The Biology Department at Western Washington University provided financial assistance for this study.

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  1. Department of Biology, Western Washington University, Bellingham, WA, USA

    Amy M. Savage & Merrill A. Peterson

  2. Department of Ecology and Evolution, Rice University, Houston, TX, USA

    Amy M. Savage

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  1. Amy M. Savage
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  2. Merrill A. Peterson
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Correspondence to Amy M. Savage.

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Communicated by Jay Rosenheim.

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Savage, A.M., Peterson, M.A. Mutualism in a community context: the positive feedback between an ant–aphid mutualism and a gall-making midge. Oecologia 151, 280–291 (2007). https://doi.org/10.1007/s00442-006-0582-1

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