Protective Ant-plant Interactions as Model Systems in Ecological and Evolutionary Research

Annual Review of Ecology, Evolution, and Systematics

Volumn 34, Issue , 2003, Pages 425-453

  Heil, Martin ^a   McKey, Doyle ^b  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Antiherbivore defense; Coevolution; Myrmecophily; Myrmecophytism; Plant animal interaction

Indexed keywords

ANTIHERBIVORE DEFENSE; COEVOLUTION; MYRMECOPHILY; MYRMECOPHYTE; PLANT-INSECT INTERACTION;

ANIMALIA; FORMICIDAE; INSECTA;

EID: 0842322952     PISSN: 00664162     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ecolsys.34.011802.132410     Document Type: Review

References (214)

1. Agrawal AA. 1998. Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant. Ecology 79:2100-12
2. Agrawal AA, Dubin-Thaler BJ. 1999. Induced responses to herbivory in the Neotropical ant-plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues. Behav. Ecol. Sociobiol. 45:47-54
3. Alonso LE. 1998. Spatial and temporal variation in the ant occupants of a facultative ant-plant. Biotropica 30:201-13
4. Alvarez G, Armbrecht I, Jiménez E, Armbrecht H, Ulloa-Chacón P. 2001. Ant-plant association in two Tococa species from a primary rain forest of Colombian Choco (Hymenoptera: Formicidae). Sociobiology 38:585-602
5. Apple JL, Feener DH. 2001. Ant visitation of extrafloral nectaries of Passiflora: the effects of nectary attributes and ant behavior on patterns in facultative ant-plant mutualisms. Oecologia 127:409-16
6. Baker HG, Opler PA, Baker I. 1978. A comparison of the amino acid complements of floral and extrafloral nectars. Bot. Gaz. 139:322-32
7. Barton AM. 1986. Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495-504
8. Beattie AJ. 1985. The Evolutionary Ecology of Ant-Plant Mutualisms. Cambridge, UK: Cambridge Univ. Press
9. Belin-Depoux M, Bastien D. 2002. Glances on the myrmecophily in French Guiana. The devices of Maieta guianensis absorption and the triple Philodendron-ants-Aleyrodiciae association. Acta Bot. Gall. 149:299-318
10. Belin-Depoux M, Solano P-J, Lubrano C, Robin JR, Chteau P, Touzet M-C. 1997. La fonction myrmécophile de Cecropia obtusa Trecul (Cecropiaceae) en Guyane française. Acta Bot. Gall. 144:289-313
11. Belt T. 1874. The Naturalist in Nicaragua. London: Dent
12. Bentley BL. 1976. Plants bearing extrafloral nectaries and the associated ant community: interhabitat differences in the reduction of herbivore damage. Ecology 57:815-20
13. Bentley BL. 1977. Extrafloral nectaries and protection by pugnacious bodyguards. Annu. Rev. Ecol. Syst. 8:407-27
14. Bentley BL. 1981. Ants, extrafloral nectaries, and the vine life-form: an interaction. Trop. Ecol. 22:127-33
15. Bergstrom CT, Lachmann M. 2003. The Red King effect: when the slowest runner wins the coevolutionary race. Proc. Natl. Acad. Sci. USA 100:593-98
16. Bizerril MXA, Vieira EM. 2002. Azteca ants as antiherbivore agents of Tococa formicaria (Melastomataceae) in Brazilian Cerrado. Stud. Neotrop. Fauna Environ. 37:145-49
17. Blattner FR, Weising K, Bänfer G, Maschwitz U, Fiala B. 2001. Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Mol. Phylogenet. Evol. 19:331-44
18. Blüthgen N, Verhaagh M, Goitía W, Jaffé K, Morawetz W, Barthlott W. 2000. How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229-40
19. Blüthgen N, Wesenberg J. 2001. Ants induce domatia in a rain forest tree (Vochysia vismiaefolia). Biotropica 33:637-42
20. Bourke AF, Franks NR. 1995. Social Evolution in Ants. Princeton, NJ: Princeton Univ. Press. 529 pp.
21. Bronstein JL. 1998. The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150-61
22. Brouat C, Garcia N, Andary C, McKey D. 2001a. Plant lock and ant key: pairwise co-evolution of an exclusion filter in an ant-plant mutualism. Proc. R. Soc. London Ser. B 268:2131-41
23. Brouat C, Gielly L, McKey D. 2001b. Phylogenetic relationships in the genus Leonardoxa (Leguminosae: Caesalpinioideae) inferred from chloroplast trnL intron and trnL-trnF intergenic spacer sequences. Am. J. Bot. 88:143-49
24. Brouat C, McKey D. 2000. Origin of caulinary ant domatia and timing of their onset in plant ontogeny: evolution of a key trait in horizontally transmitted ant-plant symbiosis. Biol. J. Linn. Soc. 71:801-19
25. Brouat C, McKey D. 2001. Leaf-stem allometry, hollow stems, and the evolution of caulinary domatia in myrmecophytes. New Phytol. 151:391-406
26. Brouat C, McKey D, Bessière J-M, Pascal L, Hossaert-McKey M. 2000. Leaf volatile compounds and the distribution of ant patrolling in an ant patroling in an ant-plant protection mutualism: preliminary results on Leonardoxa (Fabaceae: Caesalpinioideae) and Petalomyrmex (Formicidae: Formicinae). Acta Oecol. 21:349-57
27. Bryant JP, Chapin FS III, Klein DR. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-68
28. Buckley RC. 1982. Ant-plant interactions: a world review. In Ant-Plant Interactions in Australia, ed. RC Buckley, pp. 111-62. The Hague/Boston/London: Junk
29. Bugg RL, Ellis RT, Carlson RW. 1989. Ichneumonidae (Hymenoptera) using extrafloral nectar of faba bean (Vicia faba L, Fabaceae) in Massachusetts. Biol. Agric. Hortic. 6:107-14
30. Chenuil A, McKey D. 1996. Molecular phylogenetic study of a myrmecophyte symbiosis: Did Leonardoxa-ant associations diversify via cospeciation? Mol. Phylogenet. Evol. 6:270-86
31. Coley PD, Barone JA. 1996. Herbivory and plant defenses in tropical forests. Annu. Rev. Ecol. Syst. 27:305-35
32. Coley PD, Bryant JP, Chapin FS III. 1985. Resource availability and plant antiherbivore defense. Science 230:895-99
33. Costa FBMC, Oliveira-Filho AT, Oliveira PS. 1992. The role of extrafloral nectaries in Qualea grandiflora (Vochysiaceae) in limiting herbivory: an experiment of ant protection in cerrado vegetation. Ecol. Entomol. 17:363-65
34. Dalecky A, Debout G, Mondor G, Rasplus J-Y, Estoup A. 2002. PCR primers for polymorphic microsatellite loci in the facultatively polygynous plant-ant Petalomyrmex phylax (Formicidae). Mol. Ecol. Notes 2:404-7
35. Davidson DW. 1997. The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol. J. Linn. Soc. 61:153-81
36. Davidson DW, Cook SC, Snelling RR, Chua TH. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science. 300:969-72
37. Davidson DW, Longino JT, Snelling RR. 1988. Pruning of host plant neighbors by ants: an experimental approach. Ecology 69:801-8
38. Davidson DW, McKey D. 1993. The evolutionary ecology of symbiotic ant-plant relationships. J. Hym. Res. 2:13-83
39. Davies SJ, Lum SKY, Chan R, Wng LK. 2001. Evolution of myrmecophytism in western malesian Macaranga (Euphorbiaceae). Evolution 55:1542-59
40. Davies SJ, Palmiotto PA, Ashton PS, Lee HS, LaFrankie JV. 1998. Comparative ecology of 11 sympatric species of Macaranga in Borneo: tree distribution in relation to horizontal and vertical resource heterogenity. J. Ecol. 86:662-73
41. Debout G, Dalecky A, Mondor G, Estoup A, Rasplus J-Y. 2002. Isolation and characterisation of polymorphic microsatellites in the tropical plant-ant Cataulacus mckeyi (Formicidae: Myrmicinae). Mol. Ecol. Notes 2:459-61
42. Dejean A, Djiéto-Lordon C. 1996. Ecological studies on the relationships between ants (Hymenoptera, Formicidae) and the myrmecophyte Scaphopetalum thonneri (Sterculiaceae). Sociobiology 28:91-102
43. Dejean A, McKey D, Gibernau M, Belin M. 2000. The arboreal ant mosaic in a Cameroonian rainforest (Hymenoptera: Formicidae). Sociobiology 35:403-23
44. Dejean A, Solano PJ, Belin-Depoux M, Cerdan P, Corbara B. 2001a. Predatory behavior of patrolling Allomerus decemarticulatus workers (Formicidae; Myrmicinae) on their host plant. Sociobiology 37:571-78
45. Dejean A, Solano PJ, Orivel J, Belin-Depoux M, Cerdan P, Corbara B. 2001b. The spread-eagling of prey by the obligate plant-ant Pheidole minutula (Myrmicinae): Similarities with dominant arboreal ants. Sociobiology 38:675-82
46. Delabie J. 2001. Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop. Entomol. 30:501-16
47. 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 118:192-202
48. delClaro K, Berto V, Reu W. 1996. Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae). J. Trop. Ecol. 12:887-92
49. Di Giusto B, Anstett MC, Dounias E, McKey D. 2001. Variation in the effectiveness of biotic defence: the case of an opportunistic ant-plant protection mutualism. Oecologia 129:367-75
50. Downhower JF. 1975. The distribution of ants on Cecropia leaves. Biotropica 7:59-62
51. Dress WJ, Newell SJ, Nastase AJ, Ford JC. 1997. Analysis of amino acids in nectar from pitchers of Sarracenia purpurea (Sarraceniaceae). Am. J. Bot. 84:1701-6
52. Duarte Rocha CF, Godoy Bergallo H. 1992. Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs. Coelomera ruficornis on Cecropia pachystachia. Oecologia 91:249-52
53. Dyer LA, Dodson CD, Beihoffer J, Letourneau DK. 2001. Trade-offs in antiherbivore defenses in Piper cenocladum: ant mutualists versus plant secondary metabolites. J. Chem. Ecol. 27:581-92
54. Eck G, Fiala B, Linsenmair KE, Proksch P. 2001. Trade off between chemical and biotic anti-herbivore defense in the Southeast Asian plant genus Macaranga. J. Chem. Ecol. 27:1979-96
55. Elias TS. 1983. Extrafloral nectaries: Their structure and distribution. In The Biology of Nectaries, ed. B Bentley, TS Elias, pp. 174-203. New York: Columbia Univ. Press
56. Farji Brener AG, Folgarait P, Protomastro J. 1992. Asociatión entre el arbuso Capparis refusa (Capparidaceae) y las hormigas Camponotus blandus y Acromyrmex striatus (Hymenoptera: Formicidae). Rev. Biol. Trop. 40:341-44
57. Federle W, Fiala B, Maschwitz U. 1998. Camponotus (Colobopsis) (Mayr 1861) and Macaranga (Thouars 1806): a specific two-partner ant-plant system from Malaysia. Trop. Zool. 11:83-94
58. Federle W, Fiala B, Zizka G, Maschwitz U. 2001. Incident daylight as orientation cue for hole-boring ants: prostomata in Macaranga ant-plants. Ins. Soc. 48:165-77
59. Federle W, Leo A, Moog J, Azarae HI, Maschwitz U. 1999. Myrmecophagy undermines ant-plant mutualisms: ant-eating Callosciurus squirrels (Rodentia: Sciuridae) damage ant-plants in Southeast Asia. Ecotropica 5:35-43
60. Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B. 1997. Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112:217-24
61. Federle W, Maschwitz U, Hölldobler B. 2002. Pruning of host plant neighbours as defence against enemy ant invasions: Crematogaster ant partners of Macaranga protected by "wax barriers" prune less than their congeners. Oecologia 132:264-70
62. Feldhaar H, Fiala B, bin Hashim R, Maschwitz U. 2000. Maintaining an ant-plant symbiosis: secondary polygyny in the Macaranga triloba-Crematogaster sp association. Naturwissenschaften 87:408-11
63. Ferguson BG, Boucher DH, Maribel Pizzi CR. 1995. Recruitment and decay of a pulse of Cecropia in Nicaraguan rain forest damaged by hurricane Joan: relation to mutualism with Azteca ants. Biotropica 27:455-60
64. Fiala B, Grunsky H, Maschwitz U, Linsenmair KE. 1994. Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97:186-92
65. Fiala B, Linsenmair KE. 1995. Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia. Biodivers. Conserv. 4:165-82
66. Fiala B, Maschwitz U. 1990. Studies on the south east Asian ant-plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insect. Soc. 37:212-31
67. Fiala B, Maschwitz U. 1991. Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism. Biol. J. Linn. Soc. 44:287-305
68. Fiala B, Maschwitz U. 1992. Domatia as most important adaptions in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Syst. Evol. 180:53-64
69. Fiala B, Maschwitz U, Tho YP, Helbig AJ. 1989. Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463-70
70. Fischer RC, Richter A, Wanek W, Mayer V. 2002. Plants feed ants: food bodies of myrmecophytic Piper and their significance for the interaction with Pheidole bicornis ants. Oecologia 133:186-92
71. Floren A, Biun A, Linsenmair KE. 2002. Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia 131:137-44
72. Folgarait PJ, Davidson DW. 1994. Antiherbivore defenses of myrmecophytic Cecropia under different light regimes. Oikos 71:305-20
73. Folgarait PJ, Davidson DW. 1995. Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments. Oecologia 104:189-206
74. Folgarait PJ, Johnson HL, Davidson DW 1994. Responses of Cecropia to experimental removal of Müllerian bodies. Funct. Ecol. 8:22-28
75. Fonseca CR. 1993. Nesting space limits colony size of the plant-ant Pseudomyrmex concolor. Oikos 67:473-82
76. Fonseca CR. 1994. Herbivory and the long-lived leaves of an Amazonian ant-tree. J. Ecol. 82:833-42
77. Fonseca CR. 1999. Amazonian ant-plant interactions and the nesting space limitation hypothesis. J. Trop. Ecol. 15:807-25
78. Fonseca CR, Ganade G. 1996. Asymmetries, compartments and null interactions in an Amazonian ant-plant community. J. Anim. Ecol. 65:339-47
79. Forster PI. 2000. The ant, the butterfly and the ant-plant: Notes on Myrmecodia beccarii (Rubiaceae), a vulnerable Queensland endemic. Haseltonia (7):2-7
80. Foster WA. 1995. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 40:443-74
81. Freitas L, Galetto L, Bernardello G, Paoli AAS. 2000. Ant exclusion and reproduction of Croton sarcopetalus (Euphorbiaceae). Flora 195:398-402
82. Galetto L, Bernardello LM. 1992. Extrafloral nectaries that attract ants in Bromeliaceae: structure and nectar composition. Can. J. Bot. 70:1101-6
83. García-Guzmán G, Dirzo R. 2001. Patterns of leaf-pathogen infection in the understory of a Mexican rain forest: incidence, spatiotemporal variation, and mechanisms of infection. Am. J. Bot. 88:634-45
84. Gartner BL. 2001. Multitasking and tradeoff in stems, and the costly dominion of domatia. New Phytol. 151:311-13
85. Gastreich KR. 1999. Trait-mediated indirect effects of a theridiid spider on an ant-plant mutualism. Ecology 80:1066-70
86. Gaume L, McKey D. 1998. Protection against herbivores of the myrmecophyte Leonardoxa africana (Baill.) Aubrev. T3 by its principal ant inhabitant Aphomomyrmex afer Emery. C. R. Acad. Sci. III 321:593-601
87. Gaume L, McKey D. 1999. An ant-plant mutualism and its host-specific parasite: Activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant-ants inhabiting the same myrmecophyte. Oikos 84:130-44
88. Gaume L, McKey D. 2002. How identity of the homopteran trophobiont affects sex allocation in a symbiotic plant-ant: the proximate role of food. Behav. Ecol. Sociobiol. 51:197-205
89. Gaume L, McKey D, Anstett M-C. 1997. Benefits conferred by 'timid' ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax. Oecologia 112:209-16
90. 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. London Ser. B 265:596-75
91. Ghazoul J. 2001. Can floral repellents pre-empt potential ant-plant conflicts? Ecol. Lett. 4:295-99
92. Gullan PJ. 1997. Relationships with ants. In Soft Scale Insects: Their Biology, Natural Enemies and Control, ed. Y Ben-Dov, CJ Hodgson, pp. 351-73. Amsterdam: Elsevier
93. Gullan PJ, Kosztarab M. 1997. Adaptations in scale insects. Annu. Rev. Entomol. 42:23-50
94. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86-95
95. Harper JL. 1989. The value of a leaf. Oecologia 80:53-58
96. Heckroth HP, Fiala B, Gullan PJ, Maschwitz U, Azarae HI. 1999. The soft scale (Coccidae) associates of Malaysian ant-plants. J. Trop. Ecol. 14:427-43
97. Heil M. 2002. Ecological costs of induced resistance. Curr. Opin. Plant Biol. 5:345-50
98. Heil M, Delsinne T, Hilpert A, Schürkens S, Andary C, et al. 2002a. Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis. Oikos 99:457-68
99. Heil M, Fiala B, Baumann B, Linsenmair KE. 2000a. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct. Ecol. 14:749-57
100. Heil M, Fiala B, Boller T, Linsenmair KE. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86:146-49
101. Heil M, Fiala B, Kaiser W, Linsenmair KE. 1998. Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct. Ecol. 12:117-22
102. Heil M, Fiala B, Linsenmair KE, Zotz G, Menke P, Maschwitz U. 1997. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via mutualistic ant partners. J. Ecol. 85:847-61
103. Heil M, Fiala B, Maschwitz U, Linsenmair KE. 2001a. On benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126:395-403
104. Heil M, Hilpert A, Fiala B, Kaiser W, bin Hashim R, et al. 2002b. Nutrient allocation of Macaranga triloba ant plants to growth, photosynthesis, and indirect defence. Funct. Ecol. 16:475-83
105. Heil M, Hilpert A, Fiala B, Linsenmair KE. 2001b. Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 126:404-8
106. Heil M, Hilpert A, Krüger R, Linsenmair KE. 2003. Competition among visitors to extrafloral nectaries as a source of ecological costs of an indirect defence. J. Trop. Ecol. In press
107. Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE. 2001c. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc. Natl. Acad. Sci. USA 98:1083-88
108. Heil M, Staehelin C, McKey D. 2000b. Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences? Naturwissenschaften 87: 555-58
109. Hölldobler B, Wilson EO. 1990. The Ants. Berlin/Heidelberg/New York: Springer. 732 pp.
110. Horvitz CC, Schemske DW. 1984. Effects of ants and an ant-tended herbivore on seed production of a neotropical herb. Ecology 65: 1369-78
111. Horvitz CC, Schemske DW. 1990. Spatiotemporal variation in insect mutualists of a neotropical herb. Ecology 71:1085-95
112. Hossaert-McKey M, Orivel J, Labeyrie E, Pascal L, Delabie JHC, Dejean A. 2001. Differential associations with ants of three co-occurring extrafloral nectary-bearing plants. EcoScience 8:325-35
113. Huxley CR, Cutler DF, eds. 1991. Ant-Plant Interactions. Oxford, UK: Oxford Univ. Press. 601 pp.
114. Ibarra-Manríquez G, Dirzo R. 1990. Arboreal myrmecophilous plants from Los Tuxtlas biological-station, Veracruz, Mexico. Rev. biol. Trop. 38:79-82
115. Inui Y, Itioka T, Murase K, Yamaoka R, Itino T. 2001. Chemical recognition of partner plant species by foundress ant queens in Macaranga-Crematogaster myrmecophytism. J. Chem. Ecol. 27:2029-40
116. Itino T, Davies SJ, Tada H, Hieda Y, Inoguchi M, et al. 2001a. Cospeciation of ants and plants. Ecol. Res. 16:787-93
117. Itino T, Itioka T, Hatada A, Hamid AA. 2001b. Effects of food rewards offered by ant-plant Macaranga on the colony size of ants. Ecol. Res. 16:775-86
118. Izzo TJ, Vasconcelos HL. 2002. Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia 133:200-5
119. Janzen DH. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249-75
120. Janzen DH. 1967a. Fire, vegetation structure, and the ant x Acacia interaction in Central America. Ecology 48:26-35
121. Janzen DH. 1967b. Interaction of the bull's-horn acacia (Acacia cornigera L.) with an ant inhabitant (Pseudomyrmex ferruginea F. Smith) in eastern Mexico. Kansas Univ. Sci. Bull. 47:315-558
122. Janzen DH. 1969. Allelopathy by myrmecophytes: the ant Azteca as an allelopathic agent of Cecropia. Ecology 50:147-53
123. Janzen DH. 1972. Protection of Barteria (Passifloraceae) by Pachysima ants (Pseudomyrmecinae) in a Nigerian rain forest. Ecology 53:885-92
124. Janzen DH. 1974. Swollen-Thorn Acacias of Central America. Washington, DC: Smithson. Inst. Press
125. Janzen DH. 1975. Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188:936-37
126. Jolivet P. 1991. Plante et fourmis: le mutualisme brisé. La Recherche 22:792-93
127. Koptur S. 1989. Is extrafloral nectar an inducible defense? In The Evolutionary Ecology of Plants, ed. JH Bock, YB Linhart, pp. 323-29. Boulder, CO: Westview
128. Koptur S. 1992. Extrafloral nectary-mediated interactions between insects and plants. In Insect-Plant Interactions, ed. EA Bernays, 4:81-129. Boca Raton, FL: CRC Press
129. Koptur S. 1994. Floral and extrafloral nectars of Costa Rican Inga trees: a comparison of their constituents and composition. Biotropica 26:276-84
130. Koptur S, Rico-Gray V, Palacios-Rios M. 1998. Ant protection of the nectaried fern Polypodium plebeium in Central Mexico. Am. J. Bot. 85:736-39
131. Koptur S, Truong N. 1998. Facultative ant-plant interactions: Nectar sugar preferences of introduced pest ant species in South Florida. Biotropica 30:179-89
132. Lanza J, Vargo EL, Pulim S, Chang YZ. 1993. Preferences of the fire ants Solenopsis invicta and S. geminata (Hymenoptera: Formicidae) for amino acid and sugar components of extrafloral nectars. Environ. Entomol. 22:411-17
133. Letourneau DK. 1990. Code of ant-plant mutualism broken by parasite. Science 248:215-17
134. Letourneau DK. 1998. Ants, stem-borers, and fungal pathogens: experimental tests of a fitness advantage in Piper ant-plants. Ecology 79:593-603
135. Letourneau DK, Barbosa P. 1999. Ants, stem borers and pubescence in Endospermum in Papua New Guinea. Biotropica 31:295-302
136. Letourneau DK, Dyer LA. 1998a. Density patterns of Piper ant-plants and associated arthropods: top-predator trophic cascades in a terrestrial system. Biotropica 30:162-69
137. Letourneau DK, Dyer LA. 1998b. Experimental test in lowland tropical forest shows top-down effects through four trophic levels. Ecology 79:1678-87
138. Limburg DD, Rosenheim JA. 2001. Extrafloral nectar consumption and its influence on survival and development of an omnivorous predator, larval Chrysoperla plorabunda (Neuroptera: Chrysopidae). Environ. Entomol. 30:595-604
139. Mackay DA, Whalen MA. 1998. Associations between ants (Hymenoptera: Formicidae) and Adriana Gaudich. (Euphorbiaceae) in East Gippsland. Aust. J. Entomol. 37:335-39
140. Madden D, Young TP. 1992. Symbiotic ants as an alternative defense against giraffe herbivory in spinescent Acacia drepanolobium. Oecologia 91:235-38
141. Maschwitz U, Schroth M, Hänel H, Tho YP. 1984. Lycaenids parasitizing symbiotic plant-ant partnerships. Oecologia 64:78-80
142. McKey D. 1974. Adaptive patterns in alkaloid physiology. Am. Nat. 108:305-20
143. McKey D. 1984. Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16:81-99
144. McKey D. 2000. Leonardoxa africana (Leguminosae: Caesalpinioideae): a complex of mostly allopatric subspecies. Adansonia 22:71-109
145. McKey D, Gaume L, Dalecky A. 1999. Les symbioses entre plantes et fourmis arboricoles. Ann. Biol. 38:169-94
146. McKey D, Meunier L. 1996. Evolution des mutualismes plantes-fourmis: quelques éléments de réflexion. Actes Coll. Insect. Soc. 10:1-9
147. Meunier L, Dalecky A, Berticat C, Gaume L, McKey D. 1999. Worker size variation and the evolution of ant-plant mutualisms: Comparative morphometrics of workers of two closely related plant-ants, Petalomyrmex phylax and Aphomomyrmex afer (Formicinae). Insect. Soc. 46:171-78
148. Moog J, Drude T, Maschwitz U. 1998. Protective function of the plant-ant Cladomyrma maschwitzi to its host, Crypteronia griffithii, and the dissolution of the mutualism (Hymenoptera: Formicidae). Sociobiology 31:105-29
149. Morawetz W, Henzl M, Wallnöfer B. 1992. Tree killing by herbicide producing ants for the establishment of pure Tococa occidentalis populations in the Peruvian Amazon. Biodivers. Conserv. 1:19-33
150. Nomura M, Itioka T, Into T. 2000. Variations in abiotic defense within myrmecophytic and non-myrmecophytic species of Macaranga in a Bornean dipterocarp forest. Ecol. Res. 15:1-11
151. Novotny V, Basset Y, Auga J, Boen W, Dal C, et al. 1999. Predation risk for herbivorous insects on tropical vegetation: A search for enemy-free space and time. Aust. J. Ecol. 24:477-83
152. O'Brien SP. 1995. Extrafloral nectaries in Chamelaucium uncinatum: A first record in the Myrtaceae. Aust. J. Bot. 43:407-13
153. O'Dowd DJ. 1979. Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale. Oecologia 43:233-48
154. O'Dowd DJ. 1980. Pearl bodies of a neotropical tree, Ochroma pyramidale: ecological implications. Am. J. Bot. 67:543-49
155. O'Dowd DJ. 1982. Pearl bodies as ant food: an ecological role for some leaf emergences of tropical plants. Biotropica 14:40-49
156. O'Dowd DJ, Catchpole EA. 1983. Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp. - ant interactions. Oecologia 59:191-200
157. Oliveira PS, Brandão CRF. 1991. The ant community associated with extrafloral nectaries in the Brazilian cerrados. See Huxley & Cutler 1991, pp. 198-212
158. Oliveira PS, Rico-Gray V, Diaz-Castelazo C, Castillo-Guevara C. 1999. Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae). Funct. Ecol. 13:623-31
159. Palmer TM, Young TP, Stanton ML. 2002. Burning bridges: priority effects and the persistence of a competitively subordinate acacia-ant in Laikipia, Kenya. Oecologia 133:372-79
160. Pemberton RW. 1993. Observations of extrafloral nectar feeding by predaceous and fungivorous mites. Proc. Entomol. Soc. Wash. 95:642-43
161. Pemberton RW, Lee JH. 1996. The influence of extrafloral nectaries on parasitism of an insect herbivore. Am. J. Bot. 83:1187-94
162. Pemberton RW, Vandenberg NJ. 1993. Extrafloral nectar feeding by ladybird beetles (Coleoptera: Coccinellidae). Proc. Entomol. Soc. Wash. 95:139-51
163. Preston KA, Ackerly DD. 2003. The evolution of allometry in modular organisms. In Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes, ed. M Pigliucci, KA Preston. Oxford, UK: Oxford Univ. Press. In press
164. Raine NE, Willmer P, Stone GN. 2002. Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in a Mexican ant-acacia. Ecology 83:3086-96
165. Rashbrook VK, Compton SG, Lawton JH. 1992. Ant-herbivore interactions: reasons for the absence of benefits to a fern with foliar nectaries. Ecology 73:2167-74
166. Rehr SS, Feeny PP, Janzen DH. 1973. Chemical defence in Central American non-ant Acacias. J. Anim. Ecol. 42:405-16
167. Renner SS, Ricklefs RE. 1998. Herbicidal activity of domatia-inhabiting ants in patches of Tococa guianensis and Clidemia heterophylla. Biotropica 30:324-27
168. Rettig E. 1904. Ameisenpflanzen-Pflanzenameisen. Beih. Bot. Centralblatt 17:89-122
169. Rhoades DF. 1979. Evolution of plant chemical defense against herbivores. In Herbivores: Their Interaction with Secondary Plant Metabolites, ed. GA Rosenthal, DH Janzen, pp. 4-53. New York/London: Academic
170. Rickson FR. 1971. Glycogen plastids in Müllerian body cells of Cecropia peltata - a higher green plant. Science 173:344-47
171. Rickson FR, Rickson MM. 1998. The cashew nut, Anacardium occidentale (Anacardiaceae), and its perennial association with ants: extrafloral nectary location and the potential for ant defense. Am. J. Bot. 85:835-49
172. Rico-Gray V, García-Franco JG, Palacios-Rios M, Díaz-Castelazo C, Parra-Tabla V, Navarro JA. 1998a. Geographical and seasonal variation in the richness of ant-plant interactions in México. Biotropica 30:190-200
173. Rico-Gray V, Palacios-Rios M, Garća-Franco JG, Mackay WP. 1998b. 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
174. Ridley HN. 1910. Symbiosis of ants and plants. Ann. Bot. 24:457-83
175. Risch SJ. 1982. How Pheidole ants help Piper plants. Brenesia 19/20:545-48
176. Risch SJ, Rickson F. 1981. Mutualism in which ants must be present before plants produce food bodies. Nature 291:149-50
177. Ruffner GA, Clark WD. 1986. Extrafloral nectar of Ferocactus acanthodes (Cactaceae): composition and its importance to ants. Am. J. Bot. 73:185-89
178. Ruhren S, Handel SN. 1999. Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries. Oecologia 119:227-30
179. Sagers CL, Ginger SM, Evans RD. 2000. Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia 123:582-86
180. Schmitz OJ, Hamback PA, Beckerman AP. 2000. Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am. Nat. 155:141-53
181. Schupp EW, Feener DH. 1991. Phylogeny, life form, and habitat dependence of ant-defended plants in a Panamanian forest. See Huxley & Cutler 1991, pp. 175-97
182. Seigler DS, Ebinger JE. 1987. Cyanogenic glycosides in ant-acacias of Mexico and Central America. Southwest. Nat. 32:499-503
183. Smith LL, Lanza J, Smith GS. 1990. Amino acid concentrations in extrafloral nectar of Impatiens sultani increase after simulated herbivory. Ecology 71:107-15
184. Sobrinho TG, Schoereder JH, Rodrigues LL, Collevatti RG. 2002. Ant visitation (Hymenoptera: Formicidae) to extrafloral nectaries increases seed set and seed viability in the tropical weed Triumfetta semitriloba. Sociobiology 39:353-68
185. Stanton ML, Palmer TM, Young TP, Evans A, Turner ML. 1999. Sterilization and canopy modification of a swollen thorn acacia tree by a plant-ant. Nature 401:578-81
186. Stapel JO, Cortesero AM, DeMoraes CM, Tumlinson JH, Lewis WJ. 1997. Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environ. Entomol. 26:617-23
187. Stapley L. 1998. The interaction of thorns and symbiotic ants as an effective defence mechanism of swollen-thorn acacias. Oecologia 115:401-5
188. Stephenson AG. 1982. The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63:663-69
189. Stone TB, Thompson AC, Pitre HN. 1985. Analysis of lipids in cotton extrafloral nectar. J. Entomol. Sci. 20:422-28
190. Suarez AV, De Moraes C, Ippolito A. 1997. Defense of Acacia collinsii by an obligate and nonobligate ant species: the significance of encroaching vegetation. Biotropica 30:480-82
191. Swift S, Lanza J. 1993. How do Passiflora vines produce more extrafloral nectar after simulated herbivory? Bull. Ecol. Soc. Am. 74:451
192. Tempel AS. 1983. Bracken fern (Pteridium aquilinum) and nectar-feeding ants: a non-mutualistic interaction. Ecology 64:1411-22
193. Tobin JE. 1995. Ecology and diversity of tropical forest canopy ants. In Forest Canopies, ed. MD Lowman, NM Nadkarni, pp. 129-47. San Diego, CA: Academic
194. Tollrian R, Harvell CD. 1999. The evolution of inducible defenses: current ideas. In The Ecology and Evolution of Inducible Defenses, ed. R Tollrian, CD Harvell, pp. 306-21. Princeton: Princeton Univ. Press
195. Treseder KK, Davidson DW, Ehleringer JR. 1995. Absorption of ant-provided carbon-dioxide and nitrogen by a tropical epiphyte. Nature 375:137-39
196. Vandermeer RK, Lofgren CS, Seawright JA. 1995. Specificity of the red imported fire ant (Hymenoptera, Formicidae) phagostimulant response to carbohydrates. Fla. Entomol. 78:144-54
197. van Rijn PCJ, Tanigoshi LK. 1999. The contribution of extrafloral nectar to survival and reproduction of the predatory mite Iphiseius degenerans on Ricinus communis. Exp. Appl. Acarol. 23:281-96
198. Vasconcelos HL. 1991. Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295-98
199. Vasconcelos HL, Casimiro AB. 1997. Influence of Azteca alfari ants on the exploitation of Cecropia trees by a leaf-cutting ant. Biotropica 29:84-92
200. Vasconcelos HL, Davidson DW. 2000. Relationship between plant size and ant associates in two Amazonian ant-plants. Biotropica 32:100-11
201. Wäckers FL, Wunderlin R. 1999. Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomol. Exp. Appl. 91:149-54
202. Wäckers FL, Zuber D, Wunderlin R, Keller F. 2001. The effect of herbivory on temporal and spatial dynamics of foliar nectar production in cotton and castor. Ann. Bot. 87:365-70
203. Wada A, Isobe Y, Yamaguchi S, Yamaoka R, Ozaki M. 2001. Taste-enhancing effects of glycine on the sweetness of glucose: a gustatory aspect of symbiosis between the ant, Camponotus japonicus, and the larvae of the lycaenid butterfly, Niphanda fusca. Chem. Senses 26:983-92
204. Whitmore TC. 1967. Studies in Macaranga, an easy genus of Malayan wayside trees. Malay. Nat. J. 20:89-99
205. Wickers S. 1997. Study of nectariferous secretion in a pioneer plant, Inga thibaudiana, in relation with ants. Acta Bot. Gall. 144:315-26
206. Wilkinson DM, Sherratt TN. 2001. Horizontally acquired mutualisms: an unsolved problem in ecology? Oikos 92:377-84
207. Willmer PG, Stone GN. 1997. How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388:165-67
208. Wirth R, Leal IR. 2001. Does rainfall affect temporal variability of ant protection in Passiflora coccinea? EcoScience 8:450-53
209. Young TP, Stubblefield CH, Isbell LA. 1997. Ants on swollen-thorn acacias: species co-existence in a simple system. Oecologia 109:98-107
210. Yu DW. 2001. Parasites of mutualisms. Biol. J. Linn. Soc. 72:529-46
211. Yu DW, Davidson DW 1997. Experimental studies of species-specificity in Cecropia-ant relationships. Ecol. Monogr. 67:273-94
212. Yu DW, Pierce NE. 1998. A castration parasite of an ant-plant mutualism. Proc. R. Soc. London Ser. B 265:375-82
213. Yu DW, Wilson HB, Pierce NE. 2001. An empirical model of species coexistence in a spatially structured environment. Ecology 82:1761-71
214. Yumoto T, Maruhashi T. 1999. Pruning behavior and intercolony competition of Tetraponera (Pachysima) aethiops (Pseudomyrmecinae, Hymenoptera) in Barteria fistulosa in a tropical forest, Democratic Republic of Congo. Ecol. Res. 14:393-404