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Ant-Hemipteran Mutualisms: Keystone Interactions that Alter Food Web Dynamics and Influence Plant Fitness

Consequences of Ant-Hemipteran Mutualisms for Biocontrol

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Book cover Trophic and Guild in Biological Interactions Control

Part of the book series: Progress in Biological Control ((PIBC,volume 3))

Abstract

Predicting the direct and indirect effects of natural enemies on herbivorous insects in species-rich, highly connected arthropod food webs can be extremely difficult. Community ecologists developed the keystone species concept to help simplify this task. Keystone species are species that have disproportionately large effects on the abundance of many interacting species in a community. Keystone species, however, can be difficult to identify in some communities and the effect of species that seem to play key roles in community dynamics often vary dramatically in both space and time. In some communities, pairwise interactions among species may alter the community-wide effect of a species such that it functions as a keystone species. In this chapter, we term this a ‘keystone interaction’ and explore the possibility that mutualisms involving ants and honeydew-producing Hemipterans may alter the abundance and distribution of many species in a predictable manner via increased ant predation in the presence of Hemipterans. Mutualisms involving ants and honeydew-producing insects are incredibly widespread in terrestrial ecosystems and may alter the structure of entire arthropod communities. We review cases where these mutualisms result in interference of biological control via intraguild predation of important biological control agents as well as cases where ant mutualisms result in enhanced biological control via intensified ant predation of important plant-damaging herbivores. In addition, we report the results of our own work involving the ecological consequences of fire ant-aphid mutualisms. We conclude that ant-Hemiptera mutualisms rarely disrupt biological, but instead these mutualisms often increase the effectiveness of ants as biological control agents via the removal of insect herbivores that are more important pests than the Hemipterans that benefit from ant mutualisms.

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References

  • Anonymous, 1999, New fire ant endangers California agriculture. Calif Grow. 23(8): 18.

    Google Scholar 

  • Bach, C.E., 1991, Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87: 233-239.

    Article  Google Scholar 

  • Banks, C. J., and Macaulay, E. D. M., 1967, Effects of Aphis fabae Scop. and its attendant ants and insect predators on yields of field beans (Vicia faba L.). Ann Appl Biol. 60: 445-453.

    Article  Google Scholar 

  • Bertness, M. D., and G. H. Leonard, 1997, The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78: 1976-1989.

    Article  Google Scholar 

  • Boucher, D. H., James, and K. H. Keeler, 1982, The ecology of mutualism. Ann Rev Ecol Syst. 13: 315-347.

    Article  Google Scholar 

  • Bronstein, J. L., 1994a, Conditional outcomes in mutualistic interactions. Trends Ecol Evol. 9: 214-217.

    Article  Google Scholar 

  • Bronstein, J. L., 1994b, Our current understanding of mutualism. Quart Rev Biol. 69: 31-51.

    Article  Google Scholar 

  • Bruno, J.F., 2000, Facilitation of cobble beach plant communities through habitat modification by Spartina alterniflora. Ecology 81: 1179-1192.

    Article  Google Scholar 

  • Bruno J.F., Stachowicz J.J., Bertness M.D., 2003, Inclusion of facilitation into ecological theory. Trends Ecol Evol. 18: 119–25.

    Article  Google Scholar 

  • Buckley, R., 1983, Interaction between ants and membracid bugs decreases growth and seed set of host plant bearing extrafloral nectaries. Oecologia 58: 132-136.

    Article  Google Scholar 

  • Buckley, R., 1987, Interactions involving plants, Homoptera, and ants. Ann Rev Ecol Syst. 18: 111-135.

    Article  Google Scholar 

  • Buckley, R., 1990, Ants protect tropical Homoptera against nocturnal spider predation. Biotropica 22: 207-209.

    Article  Google Scholar 

  • Chang, G. C., 1996, Comparison of single versus multiple species of generalist predators for biological control. Environ Entomol. 25: 207-213.

    Google Scholar 

  • Clements, F. E., 1916, Plant succession: an analysis of the development of vegetation. Carnegie Inst Wash Pub. 242: 1-512.

    Google Scholar 

  • Coll, M. and M. Guershon, 2002, Omnivory in terrestrial arthropods: Mixing plant and prey diets. Ann Rev Entomol 47: 267-297.

    Article  CAS  Google Scholar 

  • Chase, J. M., P. A. Abrams, J. P. Grover, S. Diehl, P. Chesson, R. D. Holt, S. A. Richards, R. M. Nisbet, and T. J. Case, 2002, The interaction between predation and competition: A review and synthesis. Ecology Letters 5: 302-315.

    Article  Google Scholar 

  • DeJean, A., T. Bourgoin, and M. Gibernau, 1997, Ant species that protect figs against other ants: result of territoriality induced by a mutualistic homopteran. Ecoscience 4: 446-453.

    Google Scholar 

  • Denno, R. F.,M. S. McClure, and J. R. Ott, 1995, Interspecific interactions in phytophagous insects: competition revisited and resurrected. Ann Rev Entomol. 40: 297-331.

    Article  CAS  Google Scholar 

  • Douglas, A. E., 1993, The nutritional quality of phloem sap utilized by natural aphid populations. Ecol Entomol. 18: 31-38.

    Google Scholar 

  • Elton, C. S., 1958, The ecology of invasion by animals and plants. Methuen, London.

    Google Scholar 

  • Eubanks, M. D., 2001, Estimates of the direct and indirect effects of red imported fire ants on biological control. Biol Control 21: 35-43.

    Article  Google Scholar 

  • Eubanks, M.D., S.A. Blackwell, C.J. Parrish, Z.D. DeLamar, and H. Hull-Sanders, 2002, Intraguild predation of beneficial arthropods by red imported fire ants in cotton. Environ Entomol. 31: 1168-1174.

    Google Scholar 

  • Eubanks, M.D. and J.D. Styrsky, 2005, Effects of plant feeding on the performance of omnivorous ‘predators’, in: Plant-Provided Food and Herbivore-Carnivore Interactions, F. Wäckers, P. van Rijn and J. Bruin, eds. Cambridge University Press, London, pp. 148-177.

    Google Scholar 

  • Eubanks, M.D., 2005, Predaceous herbivores and herbivorous predators: The biology of omnivores and the ecology of omnivore – prey interactions, in: Ecology of Predator – Prey Interactions, P. Barbosa and I. Castellanos, eds. Oxford University Press, Oxford, pp. 3-17.

    Google Scholar 

  • Floate, K. D., and T. G. Whitham, 1994, Aphid-ant interaction reduces chrysomelid herbivory in a cottonwood hybrid zone. Oecologia 97: 215-221.

    Article  Google Scholar 

  • Fritz, R. S., 1983, Ant protection of a host plant’s defoliator: consequence of an ant-membracid mutualism. Ecology 64: 789-797.

    Article  Google Scholar 

  • Hairston, N. G., F. E. Smith, and L. B. Slobodkin, 1960, Community structure, population control and competition. Am Nat. 94: 421–425.

    Article  Google Scholar 

  • Harmon, J.P. and D.A. Andow, 2004, Indirect effects between shared prey: Predictions for biological control. Biocontrol 49: 605-626.

    Article  Google Scholar 

  • Helms, K. R., and S. B. Vinson, 2002, Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83: 2425-2438.

    Article  Google Scholar 

  • Hölldobler, B., and E. O. Wilson, 1990, The Ants. Harvard University Press, Cambridge.

    Google Scholar 

  • Holway, D. A., L. Lach, A. V. Suarez, N. D. Tsutsui, and T. J. Case, 2002, The causes and consequences of ant invasions. Ann Rev Ecol Syst. 33: 181-233.

    Article  Google Scholar 

  • Huang, H.T. and P. Yang, 1987, The ancient cultured citrus ant. BioScience 37: 665-671.

    Article  Google Scholar 

  • Ito, F. and S. Higashi, 1991, An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol. 60: 463-470.

    Article  Google Scholar 

  • Jutsum, A.R., J.M. Cherrett, M. Fisher, 1981, Interactions between the fauna of citrus trees in Trinidad and the ants Atta cephalotes and Azteca sp. J. App Ecol. 18: 187-195.

    Article  Google Scholar 

  • Kaplan, I. and M.D. Eubanks, 2002, Disruption of cotton aphid (Hompoptera: Aphididae)-natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ Entomol. 31: 1175-1183.

    Google Scholar 

  • Kaplan, I. and M.D. Eubanks, 2005, Aphids alter the community-wide impact of fire ants. Ecology 86: 1640-1649.

    Google Scholar 

  • Karhu, K.J., 1998, Effects of ant exclusion during outbreaks of a defoliator and a sap-sucker on birch. Ecol Entomol. 23: 185-194.

    Article  Google Scholar 

  • Kay, A.D., S.E. Scott, J.D. Schade, and S.E. Hobbie, 2004, Stoichiometric relations in an ant-treehopper mutualism. Ecol Letters 7: 1024-1028.

    Article  Google Scholar 

  • Khoo, K. C. and C.T. Ho, 1992, The influence of Dolichoderus thoracicus (Hymenoptera: Formicidae) on losses due to Helopeltis heivora (Heteroptera: Miridae), black pod disease, and mammalian pests in cocoa in Malaysia. Bull Entomol Res. 82: 485-491.

    Google Scholar 

  • Koss, A.M. and W.E. Snyder, 2005, Alternative prey disrupt biocontrol by a guild of generalist predators. Biol Control 32: 243-251.

    Article  Google Scholar 

  • Laine K.J. and P. Niemela, 1980, The influence of ants on the survival of mountain birches during an Oporinia autumnata (Lep., Geometridae) outbreak. Oecologia 47: 39-42.

    Article  Google Scholar 

  • Lawton, J. H., and D. R. Strong, 1981, Community patterns and competition in folivorous insects. Am Nat. 118: 317-338.

    Article  Google Scholar 

  • Löhr, B., 1992, The pugnacious ant, Anopeplis custodiens (Hymenoptera: Formicidae), and its beneficial effect on coconut production in Tanzania. Bull Entomol Res. 82: 213-218.

    Article  Google Scholar 

  • MacArthur, R. H., 1955, Fluctuations of animal populations and a measure of community stability. Ecology 36: 533-536.

    Article  Google Scholar 

  • MacKay, W.P. and R. Fagerlund, 1997, Range expansion of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), into New Mexico and extreme western Texas. Proc Entomol Soc Wash. 99: 757-758.

    Google Scholar 

  • Mahdi, T., and J. B. Whittaker, 1993, Do birch trees (Betula pendula) grow better if foraged by wood ants? J Anim Ecol. 62: 101-116.

    Article  Google Scholar 

  • Menalled, F.D., A.C. Costamagna, P.C. Marino, and D.A. Landis, 2003, Temporal variation in the response of parasitoids to agricultural landscape structure. Agric Ecosyst Environ. 96: 29-35.

    Google Scholar 

  • Messina, F. J, 1981, Plant protection as a consequence of an ant membracid mutualism: interactions on goldenrod (Solidago sp.). Ecology 62: 1433-1440.

    Article  Google Scholar 

  • Mills, L. S., M. E. Soule, and D. F. Doak, 1993, The keystone-species concept in ecology and conservation. BioScience 43: 219-224.

    Article  Google Scholar 

  • Mittler, T. E, 1958, Studies on the feeding and nutrition of Tuberolachnus salignus. II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. J Exp Biol. 35: 74-84.

    CAS  Google Scholar 

  • Moya-Raygoza, G. and R. Nault, 2000, Obligatory mutualism between Dalbulus quinquenotatus(Homoptera: Cicadellidae) and attendant ants. Ann Entomol Soc Am. 93: 929-940.

    Article  Google Scholar 

  • Murdoch, W. W., J. Chesson, and P. L. Chesson, 1985, Biological control in theory and practice. Am Nat. 125: 344-366.

    Article  Google Scholar 

  • Nickerson, J. C., C. A. Rolph Kay, L. L. Buschman, and W. H. Whitcomb, 1977, The presence of Spissistilus festinus as a factor affecting egg predation by ants in soybeans. Flor Entomol. 60: 193-199.

    Article  Google Scholar 

  • Oliveira, P.S. and K. Del-Claro, 2005, Multitrophic interactions in a neotropical savannah: ant-hemipteran systems, associated insect herbivores and a host plant, in: Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity, D. Burslem, M. Pinard, and S. Hartley, eds. Cambridge University Press, Cambridge, pp. 414-438.

    Google Scholar 

  • Paine, R. T. 1969, A note on trophic complexity and community stability. Am Nat. 103: 91-93.

    Article  Google Scholar 

  • Pedigo, L. P., 2002, Entomology and Pest Management, 4th ed., Prentice Hall, Upper Saddle River.

    Google Scholar 

  • Polis, G. A., 1991, Complex trophic interactions in deserts: an empirical critique of food-web theory. Am Nat. 138: 123-155.

    Article  Google Scholar 

  • Polis, G. A., Myers, C. A., and Holt, R. D., 1989, The ecology and evolution of intraguild predation: potential competitors that eat each other. Ann Rev Ecol Syst. 20: 297-330.

    Article  Google Scholar 

  • Polis, G. A., and Strong, D. R., 1996, Food web complexity and community dynamics. Am Nat. 147: 813-846.

    Article  Google Scholar 

  • Porter, S. D., and D. A. Savignano, 1990, Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71: 2095-2106.

    Article  Google Scholar 

  • Power, M. E., and D. Tilman, 1996, Challenges in the quest for keystones. Bioscience 46: 609-621.

    Article  Google Scholar 

  • Queiroz, J. M., and P. S. Oliveira, 2001, Tending ants protect honeydew-producing whiteflies (Homoptera: Aleyrodidae). Environ Entomol. 30: 295-297.

    Article  Google Scholar 

  • Reilly, J.J. and Sterling, W.L., 1983a, Interspecific association between the red imported fire ant (Hymenoptera: Formicidae), aphids, and some predaceous insects in a cotton agroecosystem. Environ Entomol. 12: 541-545.

    Google Scholar 

  • Reilly, J.J. and Sterling, W.L., 1983b, Dispersion patterns of the red imported fire ant (Hymenoptera: Formicidae), aphids, and some predaceous insects in east Texas cotton fields. Environ Entomol. 12: 380-385.

    Google Scholar 

  • Renault, C.K., L.M. Buffa, and M.A. Delfino, 2005, An aphid-ant interaction: effects on different trophic levels. Ecol Res. 20: 71-74.

    Article  Google Scholar 

  • Rico-Gray, V. and G. Castro, 1996, Effect of an ant-aphid interaction on the reproductive fitness of Paullinia fuscecens (Sapindaceae). Southwest Nat. 41: 434-440.

    Google Scholar 

  • Rico-Gray, V. and L.B. Thein, 1989, Ant-mealybug interaction decreases reproductive fitness of Schomburgkia tibicinis (Orchidaceae) in Mexico. J Trop Ecol. 5: 109-112.

    Article  Google Scholar 

  • Romeis, A., D. Babendreier, F.L. Wackers, and T.G. Shanower, Habitat and plant specificity of Trichogramma egg parasitoids – underlying mechanisms and implications. Bas App Ecol 6: 215-236.

    Google Scholar 

  • Room, P.M., 1972, The fauna of the mistletoe Tapinanthus bangwensis (Engl. and K. Krause) growing on cocoa in Ghana: relationships between fauna and mistletoe. J Anim Ecol. 41: 611-621.

    Article  Google Scholar 

  • Rosenheim, J. A., 1998, Higher order predators and the regulation of insect herbivore populations. Annu Rev Entomol. 43: 421-447.

    Article  PubMed  CAS  Google Scholar 

  • Rosenheim, J. A., 2001, Source-sink dynamics for a generalist insect predator in habitats with strong higher-order predation. Ecol Monogr 71: 93-116.

    Article  Google Scholar 

  • Rosenheim, J. A., Wilhoit, L. R., and Armer, C. A., 1993, Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96: 439-449.

    Article  Google Scholar 

  • Rosenheim, J. A., Kaya, H. K., Ehler, L. E., Marois, J. J., and Jaffee, B. A., 1995, Intraguild predation among biological-control agents: Theory and evidence. Biol Control 5: 303-335.

    Article  Google Scholar 

  • Sanford, E., 1999, Regulation of keystone predation by small changes in ocean temperature. Science 283: 2095-2097.

    Article  PubMed  CAS  Google Scholar 

  • Sipura, M., 2002, Contrasting effects of ants on the herbivory and growth of two willow species. Ecology 83: 2680-2690.

    Article  Google Scholar 

  • Stachowicz, J. J., 2001, Mutualisms, positive interactions, and the structure of ecological communities. BioScience 51: 235-246.

    Article  Google Scholar 

  • Stechman, D. H., W. Volkl, and P. Stary, 1996, Ant attendance as a critical factor in the biological control of the banana aphid, Pentalonia nigronervossa Coq. (Hom. Aphididae) in Oceania. J App Entomol. 120: 119-123.

    Article  Google Scholar 

  • Strong, D. R., Jr., J. H. Lawton, and T. R. E. Southwood, 1984, Insects on plants: community patterns and mechanisms. Harvard University Press, Cambridge.

    Google Scholar 

  • Symondson, W.O.C., K.D. Sunderland, and M.H. Greenstone, 2002, Can generalist predators be effective biocontrol agents. Ann Rev Entomol. 47: 561-594.

    Article  CAS  Google Scholar 

  • Suzuki, N., K. Ogura and N. Katayama, 2004, The efficiency of herbivore exclusion by ants attracted to aphids on the vetch Vicia angustifolia L. (Leguminosae). Ecol Res. 19: 275-282.

    Article  Google Scholar 

  • Teder, T., M. Tanhuanpaa, K. Ruohomaki, P. Kaitaniemi, and J. Henriksson, 2000, Temporal and spatial variation of larval parasitism in non-outbreaking poupulations of a folivorous moth. Oecologia 123: 516-524.

    Article  Google Scholar 

  • Van Driesche, R. G. and T.S. Bellows, 1996, Biological control. Chapman and Hall, New York.

    Google Scholar 

  • Van Mele, P. and N.T.T. Cuc, 2001, Farmers’ perceptions and practices in use of Dolichoderus thoracicus (Smith) (Hymenoptera: Formicidae) for biological control of pests of Sapodilla. Biol Control 20: 23-29.

    Article  Google Scholar 

  • Vinson, S. B., 1997, Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biology, and impact. Am Entomol. 43: 23-39.

    Google Scholar 

  • Vinson, S.B. and Scarborough, T.A., 1989, Impact of the imported fire ant on laboratory populations of cotton aphid (Aphis gossypii) predators. Flor Entomol. 72: 107-111.

    Article  Google Scholar 

  • Way, M. J., 1963, Mutualism between ants and honeydew-producing Homoptera. Ann Rev Entomol. 8: 307-344.

    Article  Google Scholar 

  • Way, M. J. and K. C. Khoo, 1992, Role of ants in pest management. Ann Rev Entomol. 37: 479-503.

    Google Scholar 

  • Whittaker, J.B. and S. Warrington, 1985, An experimental field study of different levels of insect herbivory induced by Formica rufa predation on sycamore (Acer pseudoplatanus). III. Effects on tree growth. J App Ecol. 22: 797-811.

    Article  Google Scholar 

  • Williams, D.F., 1994, Exotic ants: Biology, Impact, and Control of Introduced Species. Westview Press, Boulder.

    Google Scholar 

  • Wimp, G. M. and T. G. Whitham, 2001, Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82: 440-452.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Entomology and Plant Pathology, Auburn University, Auburn

    Micky D. Eubanks & John D. Styrsky

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  1. Micky D. Eubanks
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  1. Institut de Recherche en Biologie Végétale, Université de Montréal, Montréal, Canada

    Jacques Brodeur

  2. CRDH, Agriculture, Agri-Food Canada, Saint-Jean-sur-Richelieu, Québec, Canada

    Guy Boivin

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Eubanks, M.D., Styrsky, J.D. (2006). Ant-Hemipteran Mutualisms: Keystone Interactions that Alter Food Web Dynamics and Influence Plant Fitness. In: Brodeur, J., Boivin, G. (eds) Trophic and Guild in Biological Interactions Control. Progress in Biological Control, vol 3. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4767-3_8

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