The ontogeny of plant indirect defenses

Perspectives in Plant Ecology, Evolution and Systematics

Volumn 15, Issue 5, 2013, Pages 245-254

  Quintero, Carolina ^a   Barton, Kasey E ^b   Boege, Karina ^c  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Domatia; Extrafloral nectaries; Ontogeny; Plant rewards; Tritrophic interactions; Volatile organic compounds

Indexed keywords

COLONY; FITNESS; HERBIVORE; NATURAL SELECTION; NESTING; ONTOGENY; PLANT; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; SUCCESSION; VOLATILE ORGANIC COMPOUND;

FORMICIDAE;

EID: 84885870733     PISSN: 14338319     EISSN: 16180437     Source Type: Journal    
DOI: 10.1016/j.ppees.2013.08.003     Document Type: Review

References (89)

1. Barton K.E., Koricheva J. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 2010, 175:481-493.
2. Blatrix R., Renard D., Djieto-Lordon C., McKey D. The cost of myrmecophytism: insights from allometry of stem secondary growth. Ann. Bot.-London 2012, 110:943-951.
3. Boege K., Marquis R.J. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 2005, 20:441-448.
4. Bronstein J.L., Alarcon R., Geber M. The evolution of plant-insect mutualisms. New Phytol. 2006, 172:412-428.
5. Brouat C., McKey D. Origin of caulinary ant domatia and timing of their onset in plant ontogeny: evolution of a key trait in horizontally transmitted ant-plant symbioses. Biol. J. Linn. Soc. 2000, 71:801-819.
6. Brouat C., McKey D. Leaf-stem allometry, hollow stems, and the evolution of caulinary domatia in myrmecophytes. New Phytol. 2001, 151:391-406.
7. Chamberlain S.A., Holland J.N. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 2009, 90:2384-2392.
8. Chamberlain S.A., Kilpatrick J.R., Holland J.N. Do extrafloral nectar resources, species abundances, and body sizes contribute to the structure of ant-plant mutualistic networks?. Oecologia 2010, 164:741-750.
9. Chou J.C., Mullin C.A. Phenologic and tissue distribution of sesquiterpene lactones in cultivated sunflower (Helianthus annuus L). J. Plant Physiol. 1993, 142:657-663.
10. Clark C.J., Poulsen J.R., Levey D.J. Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 2012, 93:554-564.
11. Cole R.A. Volatile components produced during ontogeny of some cultivated crucifers. J. Sci. Food Agric. 1980, 31:549-557.
12. Dejean A., Djieto-Lordon C., Cereghino R., Leponce M. Ontogenetic succession and the ant mosaic: an empirical approach using pioneer trees. Basic Appl. Ecol. 2008, 9:316-323.
13. Del Val E., Dirzo R. Does ontogeny cause changes in the defensive strategies of the myrmecophyte Cecropia peltata?. Plant Ecol. 2003, 169:35-41.
14. Djieto-Lordon C., Dejean A., Gibernau M., Hossaert-McKey M., McKey D. Symbiotic mutualism with a community of opportunistic ants: protection, competition, and ant occupancy of the myrmecophyte Barteria nigritana (Passifloraceae). Acta Oecol. 2004, 26:109-116.
15. Djieto-Lordon C., Dejean A., Ring R.A., Nkongmeneck B.A., Lauga J., McKey D. Ecology of an improbable association: the pseudomyrmecine plant-ant Tetraponera tessmanni and the myrmecophytic liana Vitex thyrsiflora (Lamiaceae) in Cameroon. Biotropica 2005, 37:421-430.
16. Doak P., Wagner D., Watson A. Variable extrafloral nectary expression and its consequences in quaking aspen. Can. J. Bot. 2007, 85:1-9.
17. Falcao P.F., Melo-de-Pinna G.F.D., Leal I.R., Almeida-Cortez J.S. Morphology and anatomy of extrafloral nectaries in Solanum stramonifolium (Solanaceae). Can. J. Bot. 2003, 81:859-864.
18. Feldhaar H., Fiala B., Hashim R.B., Maschwitz U. Patterns of the Crematogaster-Macaranga association: the ant partner makes the difference. Insectes Soc. 2003, 50:9-19.
19. Fiala B., Grunsky H., Maschwitz U., Linsenmair K.E. Diversity of ant-plant interactions - protective efficacy in Macaranga species with different degrees of ant association. Oecologia 1994, 97:186-192.
20. Fiala B., Maschwitz U. Domatia as most important adaptations in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Syst. Evol. 1992, 180:53-64.
21. Fonseca C.R. Nesting space limits colony size of the plant-ant Pseudomyrmex concolor. Oikos 1993, 67:473-482.
22. Fonseca C.R. Amazonian ant-plant interactions and the nesting space limitation hypothesis. J. Trop. Ecol. 1999, 15:807-825.
23. Fonseca C.R., Benson W.W. Ontogenetic succession in Amazonian ant trees. Oikos 2003, 102:407-412.
24. Frederickson M.E., Gordon D.M. The intertwined population biology of two Amazonian myrmecophytes and their symbiotic ants. Ecology 2009, 90:1595-1607.
25. Gaume L., Zacharias M., Grosbois V., Borges R.M. The fitness consequences of bearing domatia and having the right ant partner: experiments with protective and non-protective ants in a semi-myrmecophyte. Oecologia 2005, 145:76-86.
26. Gurevitch J., Hedges L.V. Meta-analysis: combining results of independent experiments. Design and Analysis of Ecological Experiments 2001, 347-369. Oxford University Press, Oxford. S.M. Scheiner, J. Gurevitch (Eds.).
27. Handa C., Okubo T., Yoneyama A., Nakamura M., Sakaguchi M., Takahashi N., Okamoto M., Tanaka-Oda A., Kenzo T., Ichie T., Itioka T. Change in biomass of symbiotic ants throughout the ontogeny of a myrmecophyte, Macaranga beccariana (Euphorbiaceae). J. Plant Res. 2013, 126:73-79.
28. Hare J.D. Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. J. Chem. Ecol. 2010, 36:1363-1374.
29. Hare J.D., Sun J.J. Production of herbivore-induced plant volatiles is constrained seasonally in the field but predation on herbivores is not. J. Chem. Ecol. 2011, 37:430-442.
30. Heil M. Indirect defence via tritrophic interactions. New Phytol. 2008, 178:41-61.
31. Heil M., Fiala B., Baumann B., Linsenmair K.E. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct. Ecol. 2000, 14:749-757.
32. Heil M., Fiala B., Linsenmair K.E., Zotz G., Menke P., Maschwitz U. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via symbiotic ant partners. J. Ecol. 1997, 85:847-861.
33. Heil M., Gonzalez-Teuber M., Clement L.W., Kautz S., Verhaagh M., Bueno J.C.S. Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18091-18096.
34. Heil M., Hilpert A., Fiala B., Linsenmair K.E. Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 2001, 126:404-408.
35. Heil M., McKey D. Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu. Rev. Ecol. Evol. Syst. 2003, 34:425-453.
36. Herms D.A., Mattson W.J. The dilemma of plants - to grow or defend. Q. Rev. Biol. 1992, 67:283-335.
37. Holland J.N., Chamberlain S.A., Horn K.C. Optimal defence theory predicts investment in extrafloral nectar resources in an ant-plant mutualism. J. Ecol. 2009, 97:89-96.
38. Itino T., Itioka T. Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species. Ecol. Res. 2001, 16:765-774.
39. Itino T., Itioka T., Hatada A., Hamid A.A. Effects of food rewards offered by ant-plant Macaranga on the colony size of ants. Ecol. Res. 2001, 16:775-786.
40. Izzo T.J., Vasconcelos H.L. Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia 2002, 133:200-205.
41. Izzo T.J., Vasconcelos H.L. Ants and plant size shape the structure of the arthropod community of Hirtella myrmecophila, an Amazonian ant-plant. Ecol. Entomol. 2005, 30:650-656.
42. Kessler A., Heil M. The multiple faces of indirect defences and their agents of natural selection. Funct. Ecol. 2011, 25:348-357.
43. Kobayashi S., Asai T., Fujimoto Y., Kohshima S. Anti-herbivore structures of Paulownia tomentosa: morphology, distribution, chemical constituents and changes during shoot and leaf development. Ann. Bot.-London 2008, 101:1035-1047.
44. Kollner T.G., Schnee C., Gershenzon J., Degenhardt J. The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 2004, 65:1895-1902.
45. Kost C., Heil M. The defensive role of volatile emission and extrafloral nectar secretion for lima bean in nature. J. Chem. Ecol. 2008, 34:2-13.
46. Kwok K.E., Laird R.A. Plant age and the inducibility of extrafloral nectaries in Vicia faba. Plant Ecol. 2012, 10.1007/s11258-012-0138-x.
47. Lapola D.M., Bruna E.M., de Willink C.G., Vasconcelos H.L. Ant-tended Hemiptera in Amazonian myrmecophytes: patterns of abundance and implications for mutualism function (Hymenoptera: Formicidae). Sociobiology 2005, 46:433-442.
48. Leroy C., Jauneau A., Quilichini A., Dejean A., Orivel J. Comparative structure and ontogeny of the foliar domatia in three neotropical myrmecophytes. Am. J. Bot. 2010, 97:557-565.
49. Llandres A.L., Rodriguez-Girones M.A., Dirzo R. Plant stages with biotic, indirect defences are more palatable and suffer less herbivory than their undefended counterparts. Biol. J. Linn. Soc. 2010, 101:536-543.
50. Longino J.T. Taxonomy of the Cecropia-inhabiting Azteca ants. J. Nat. Hist. 1991, 25:1571-1602.
51. Mattiacci L., Rudelli S., Rocca B.A., Genini S., Dorn S. Systemically-induced response of cabbage plants against a specialist herbivore, Prieris brasicae. Chemoecology 2001, 11:167-173.
52. McKey D. Adaptive patterns in alkaloid physiology. Am. Nat. 1974, 108:305-320.
53. McKey D. The distribution of secondary compounds within plants. Herbivores: Their Interaction with Secondary Plant Metabolites 1979, 55-133. Academic Press, London. G.A. Rosenthal, D.H. Janzen (Eds.).
54. Mckey D. Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 1984, 16:81-99.
55. Michelangeli F.A. Ant protection against herbivory in three species of Tococa (Melastomataceae) occupying different environments. Biotropica 2003, 35:181-188.
56. Miller T.E.X. Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 2007, 116:500-512.
57. Moles A.T., Westoby M. What do seedlings die from and what are the implications for evolution of seed size?. Oikos 2004, 106:193-199.
58. Moog J., Atzinger K., Hashim R., Maschwitz U. Do tenants always pay their rent? The Asian ant-plant Pometia pinnata (Sapindaceae) and its leaf domatia provide free access to generalist ants. Asian Myrmecol. 2008, 2:17-32.
59. Moog J., Feldhaar H., Maschwitz U. On the caulinary domatia of the SE-Asian ant-plant Zanthoxylum myriacanthum Wall. ex Hook. f. (Rutaceae) their influence on branch statics, and the protection against herbivory. Sociobiology 2002, 40:547-574.
60. Nishi A.H., Romero G.Q. Colonization pattern of Cecropia by Azteca ants: Influence of plant ontogeny, environment and host plant choice by queens. Sociobiology 2008, 52:367-376.
61. Nomura M., Itioka T., Murase K. Non-ant antiherbivore defenses before plant-ant colonization in Macaranga myrmecophytes. Popul. Ecol. 2001, 43:207-212.
62. Noy-Meir, Briske D.D. Response of wild wheat populations to grazing in Mediterranean grasslands: the relative influence of defoliation, competition, mulch and genotype. J. Appl. Ecol. 2002, 39:259-278.
63. Orivel J., Lambs L., Male P.J.G., Leroy C., Grangier J., Otto T., Quilichini A., Dejean A. Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants. Oecologia 2011, 165:369-376.
64. Palmer T.M. Spatial habitat heterogeneity influences competition and coexistence in an African acacia ant guild. Ecology 2003, 84:2843-2855.
65. Palmer T.M., Doak D.F., Stanton M.L., Bronstein J.L., Kiers E.T., Young T.P., Goheen J.R., Pringle R.M. Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17234-17239.
66. Pringle E.G., Dirzo R., Gordon D.M. Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies. Oecologia 2012, 170:677-685.
67. Radhika V., Kost C., Bartram S., Heil M., Boland W. Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 2008, 228:449-457.
68. Rico-Gray V., Oliveira P.S. The ecology and evolution of ant-plant interactions 2007, 331p. The University of Chicago Press, Chicago and London. J.N. Thompson (Ed.).
69. Rios R.S., Marquis R.J., Flunker J.C. Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata (Fabaceae). Oecologia 2008, 156:577-588.
70. Rosenberg M.S., Adams D.C., Gurevitch J. MetaWin: Statistical Software for Meta-analysis. Version 2.1 2002, Sinauer, Sunderland, MA.
71. Rostas M., Eggert K. Ontogenetic and spatio-temporal patterns of induced volatiles in Glycine max in the light of the optimal defence hypothesis. Chemoecology 2008, 18:29-38.
72. Rosumek F.B., Silveira F.A.O., Neves F.D., Barbosa N.P.D., Diniz L., Oki Y., Pezzini F., Fernandes G.W., Cornelissen T. Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 2009, 160:537-549.
73. Rudgers J.A. Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 2004, 85:192-205.
74. Shenoy M., Borges R.M. Geographical variation in an ant-plant interaction correlates with domatia occupancy, local ant diversity, and interlopers. Biol. J. Linn. Soc. 2010, 100:538-551.
75. Shiojiri K., Karban R. Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 2006, 149:214-220.
76. Shiojiri K., Karban R., Ishizaki S. Plant age, seasonality, and plant communication in sagebrush. J. Plant Interact. 2011, 6:85-88.
77. Solano P.J., Durou S., Corbara B., Quilichini A., Cerdan P., Belin-Depoux M., Delabie J.H.C., Dejean A. Myrmecophytes of the understory of French Guianian rainforests: their distribution and their associated ants. Sociobiology 2003, 41:605-614.
78. Stamp N. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 2003, 78:23-55.
79. Stanton M.L., Palmer T.M., Young T.P. Competition-colonization trade-offs in a guild of African Acacia-ants. Ecol. Monogr. 2002, 72:347-363.
80. Stanton M.L., Palmer T.M., Young T.P., Evans A., Turner M.L. Sterilization and canopy modification of a swollen thorn acacia tree by a plant-ant. Nature 1999, 401:578-581.
81. Trager M.D., Bhotika S., Hostetler J.A., Andrade G.V., Rodriguez-Cabal M.A., McKeon C.S., Osenberg C.W., Bolker B.M. Benefits for plants in ant-plant protective mutualisms: a meta-analysis. Plos One 2010, 5(12):e14308. 10.1371/journal.pone.0014308.
82. Trager M.D., Bruna E.M. Effects of plant age, experimental nutrient addition and ant occupancy on herbivory in a neotropical myrmecophyte. J. Ecol. 2006, 94:1156-1163.
83. Veena T., Kumar A.R.V., Ganeshaiah K.N. Factors affecting ant (Formicidae, Hymenoptera) visits to the extrafloral nectaries of Croton bonplandianum Baill. Proc. Indian Acad. Sci. Anim. Sci. 1989, 98:57-64.
84. Villamil N., Marquez-Guzman J., Boege K. Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries. Ann. Bot.-London 2013, 10.1093/aob/mct005.
85. Wackers F.L., Bonifay C. How to be sweet? Extrafloral nectar allocation by Gossypium hirsutum fits optimal defense theory predictions. Ecology 2004, 85:1512-1518.
86. Wooley S.C., Donaldson J.R., Gusse A.C., Lindroth R.L., Stevens M.T. Extrafloral nectaries in aspen (Populus tremuloides): heritable genetic variation and herbivore-induced expression. Ann. Bot.-London 2007, 100:1337-1346.
87. Young B., Wagner D., Doak P., Clausen T. Within-plant distribution of phenolic glycosides and extrafloral nectaries in trembling Aspen (Populus tremuloides; Salicaceae). Am. J. Bot. 2010, 97:601-610.
88. Young T.P., Stubblefield C.H., Isbell L.A. Ants on swollen thorn acacias: species coexistence in a simple system. Oecologia 1997, 109:98-107.
89. Zhu J.W., Park K.C. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J. Chem. Ecol. 2005, 31:1733-1746.