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

Oecologia

Volumn 151, Issue 2, 2007, Pages 280-291

  Savage, Amy M ^a,b   Peterson, Merrill A ^a  

^a WESTERN WASHINGTON UNIVERSITY   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

Ant aphid mutualism; Community ecology; Direct and indirect effects; Galls; Positive feedback

Indexed keywords

ABUNDANCE; ANT; APHID; COMMUNITY ECOLOGY; COMMUNITY ORGANIZATION; DECIDUOUS TREE; FEEDBACK MECHANISM; GALL; HYPOTHESIS TESTING; MUTUALISM; PARASITISM; POPULATION ECOLOGY; POPULATION GROWTH; POPULATION OUTBREAK; SURVIVAL;

ANALYSIS OF VARIANCE; ANIMAL; ANT; APHID; ARTICLE; COMPARATIVE STUDY; FLY; PARASITOLOGY; PHYSIOLOGY; POPULATION DYNAMICS; SYMBIOSIS; UNITED STATES; WILLOW;

ANALYSIS OF VARIANCE; ANIMALS; ANTS; APHIDS; DIPTERA; POPULATION DYNAMICS; SALIX; SYMBIOSIS; WASHINGTON;

NORTH AMERICA; UNITED STATES; WASHINGTON [UNITED STATES];

APHIDIDAE; CECIDOMYIIDAE; CHIRONOMIDAE; DIPTERA; FORMICIDAE; RABDOPHAGA SALICISBRASSICOIDES; SALIX; SALIX EXIGUA;

EID: 33847337030     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-006-0582-1     Document Type: Article

References (81)

1. Abrams PA (2003) Effects of altered resource consumption rates by one consumer species on a competitor. Ecol Lett 6:550-555
2. Analytical Software (2003) Statistix, version 8.0 for Windows. Tallahassee, Fla.
3. 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
4. Bernot RJ, Turner AM (2001) Predator identity and trait-mediatedindirect effects in a littoral food web. Oecologia 129:139-146
5. 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
6. Bonsall MB, Hassell MP (1999) Parasitoid-mediated effects: apparent competition and persistence of host-parasitoid assemblages. Popul Ecol 41:59-68
7. 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
8. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31-51
9. Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150-161
10. Buckley RC (1987) Interactions involving ants, homoptera, and plants. Annu Rev Ecol Syst 18:111-135
11. 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
12. Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635-639
13. Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742-1744
14. Clancy KM, Price PW (1986) Temporal variation in three-trophic-level interactions among willows, sawflies, and parasites. Ecology 67:1601-1607
15. Compton SG, Robertson HG (1988) Complex interactions between mutualisms: ants tending homopterans protect fig seeds and pollinators. Ecology 69:1302-1305
16. 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
17. 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
18. Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153-181
19. DeClerck-Floate R, Price PW (1994) Impact of bud-galling midge on bud populations of Salix exigua. Oikos 70:253-260
20. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297-331
21. Diaz BM, Fereres A (2004) Life table and population parameters of Nasonovia ribisnigri (Homoptera: Aphididae) at different constant temperatures. Environ Entomol 34:527-534
22. 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
23. Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81:3522-3529
24. Fox JW, Olsen E (2000) Food web structure and the strength of transient indirect effects. Oikos 90:219-226
25. 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
26. Francoeur A (1973) Revision taxonomique des especes nearctiques du groupe fusca, genre Formica (Formicidae: Hymenoptera). Mem Soc Entomol Que 3:1-316
27. 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
28. 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
29. 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 diVerent inhibitions of longitudinal and radial expansion. Plant Physiol 137:1474-1484
30. Harris P, Shorthouse JD (1996) Effectiveness of gall inducers in weed biological control. Can Entomol 128:1021-1055
31. 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
32. 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
33. Hentz M, Nuessly G (2004) Development, longevity, and fecundity of Sipha flava (Homoptera: Aphididae) feeding on Sorghum bicolor. Environ Entomol 33:546-553
34. Huxley CR, Cutler DF (eds) (1991) Ant-plant interactions. Oxford University Press, New York
35. 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
36. 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
37. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83-112
38. 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
39. Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84:2302-2312
40. Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:1432-1439
41. Larsen KJ, Stahle LM, Dotseth EJ (2001) Tending ants (Hymenoptera: Formicidae) regulate Dalbulus quinquenotatus (Homoptera: Cicadellidae) population dynamics. Environ Entomol 30:757-762
42. Letourneau DK, Dyer LA (1998) Experimental test in lowland tropical forest shows top-down effects through four trophic levels. Ecology 79:1678-1687
43. Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180-1186
44. 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
45. McCornack BP, Ragsdale DW, Venette RC (2004) Demography of soybean aphid (Homoptera: Aphididae) at summer temperatures. J Econ Entomol 97:854-861
46. Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217-225
47. Morales MA (2002) Ant-dependent oviposition in the membracid Publilia concave. Ecol Entomol 27:247-250
48. Moran MD, Rooney TP, Hurd LE (1996) Top-down cascade from a bitrophic predator in an old-field community. Ecology 77:2219-2227
49. Nakamura M, Miyamoto Y, Ohgushi T (2003) Gall initiation enhances the availability of food resources for herbivorous insects. Funct Ecol 17:851-857
50. 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
51. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81-105
52. 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
53. Pearson DE, Callaway KM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18: 456-461
54. 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
55. 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
56. 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
57. 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
58. 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
59. Richards WR (1972) Chaitophorinae of Canada (Homoptera: Aphididae). Entomological Society of Canada, Ottawa
60. SAS (2004) SAS statistical software version 9.3.1. SAS Institute, Cary, N.C.
61. Schmitt RJ, Holbrook SJ (2003) Mutualism can mediate competition and promote coexistence. Ecol Lett 6:898-902
62. 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
63. 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
64. Sih A, Crowley P, McPeek M, Petranka J, Strohmeiev K (1985) Predation, competition, and prey communities: a review of Weld experiments. Annu Rev Ecol Syst 16:269-311
65. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York
66. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235-246
67. Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345-372
68. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Syst 35:435-466
69. Sullivan DJ, Völkl W (1999) Hyperparasitism: multitrophic ecology and behavior. Annu Rev Entomol 44:291-315
70. Tscharntke T (1992) Cascade effects among four trophic levels: bird predation on galls affects density-dependent parasitism. Ecology 73:1689-1698
71. Van Hezewijk BH, Roland J (2003) Gall size determines the structure of the Rabdophaga salicisbrassicoides host-parasitoid community. Ecol Entomol 28:593-603
72. Völkl W (1992) Aphids or their parasitoids: who actually benefits from ant attendance? J Anim Ecol 61:273-281
73. Völkl W, Kroupa AS (1997) Effects of adult mortality risks on parasitoid foraging tactics. Anim Behav 54:349-359
74. Walsh BD, Riley CV (1869) Galls and their architects. Am Entom 1:101-110
75. Webster MS, Almany GR (2002) Positive indirect effects in a coral reef fish community. Ecol Lett 5:549-557
76. Weis AE (1984) Apical dominance asserted over lateral buds by the gall of Rhabdophaga strobiloides (Diptera: Cecidomyiidae). Can Entomol 116:1277-1279
77. Weis AE, Kapelinski A (1984) Manipulation of host plant development by the gall-midge Rhabdophaga strobiloides. Ecol Entomol 9:457-465
78. Wilson LF (1968) Life history and habits of the pine cone willow midge, Rhabdophaga strobiloides (Diptera: Cecdomyiidae), in Michigan. Can Entomol 100:430-433
79. Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82:440-452
80. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443-466
81. Yao I, Shibao H, Akimoto SI (2000) Costs and beneWts of ant attendance to the drapanosiphid aphid Tuberculatus quercicola. Oikos 89:3-10