Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis

Since its original formulation by Janzen in 1966, the hypothesis that obligate ant-plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes o...

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Published inOikos Vol. 99; no. 3; pp. 457 - 468
Main Authors Heil, Martin, Delsinne, Thibaut, Hilpert, Andrea, Schürkens, Steffen, Andary, Claude, Linsenmair, K. Eduard, Sousa S., Mario, McKey, Doyle
Format Journal Article
LanguageEnglish
Published Oxford Munksgaard International Publishers 01.12.2002
Blackwell Publishers
Blackwell
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Abstract Since its original formulation by Janzen in 1966, the hypothesis that obligate ant-plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 anti-plant and non-ant-plant species of the three unrelated genera Leonardoxa, Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti-herbivore defence). Condensed tannin content in three of four populations of the non-myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant-plants and non-ant-plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of 'trade-offs' between indirect, biotic and direct, chemical defence in ant-plants. A critical re-evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well-established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade-off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants' ant mutualists), or whether the pattern of dramatically reduced direct defence of ant-plants is caused by classes of defensive compounds not yet studied.
AbstractList Since its original formulation by Janzen in 1966, the hypothesis that obligate ant‐plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 ant‐plant and non‐ant‐plant species of the three unrelated genera Leonardoxa,Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti‐herbivore defence). 
Condensed tannin content in three of four populations of the non‐myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant‐plants and non‐ant‐plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of ‘trade‐offs’ between indirect, biotic and direct, chemical defence in ant‐plants. 
A critical re‐evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well‐established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade‐off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants’ ant mutualists), or whether the pattern of dramatically reduced direct defence of ant‐plants is caused by classes of defensive compounds not yet studied.
Since its original formulation by Janzen in 1966, the hypothesis that obligate ant-plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 anti-plant and non-ant-plant species of the three unrelated genera Leonardoxa, Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti-herbivore defence). Condensed tannin content in three of four populations of the non-myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant-plants and non-ant-plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of 'trade-offs' between indirect, biotic and direct, chemical defence in ant-plants. A critical re-evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well-established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade-off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants' ant mutualists), or whether the pattern of dramatically reduced direct defence of ant-plants is caused by classes of defensive compounds not yet studied.
Since its original formulation by Janzen in 1966, the hypothesis that obligate ant-plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 ant-plant and non-ant-plant species of the three unrelated genera Leonardoxa, Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti-herbivore defence). Condensed tannin content in three of four populations of the non-myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant-plants and non-ant-plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of 'trade-offs' between indirect, biotic and direct, chemical defence in ant-plants. A critical re-evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well-established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade-off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants' ant mutualists), or whether the pattern of dramatically reduced direct defence of ant-plants is caused by classes of defensive compounds not yet studied.
Since its original formulation by Janzen in 1966, the hypothesis that obligate ant‐plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 ant‐plant and non‐ant‐plant species of the three unrelated genera Leonardoxa, Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena , Mimosa and Prosopis ). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti‐herbivore defence). 
Condensed tannin content in three of four populations of the non‐myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant‐plants and non‐ant‐plants in the Mimosoideae and in the genus Macaranga , though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of ‘trade‐offs’ between indirect, biotic and direct, chemical defence in ant‐plants. 
A critical re‐evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well‐established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade‐off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants’ ant mutualists), or whether the pattern of dramatically reduced direct defence of ant‐plants is caused by classes of defensive compounds not yet studied.
Author Heil, Martin
Andary, Claude
Schürkens, Steffen
Linsenmair, K. Eduard
Delsinne, Thibaut
McKey, Doyle
Hilpert, Andrea
Sousa S., Mario
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Issue 3
Keywords Insecta
Formicoidea
Flavonoid
Mutualism
Phytophagous
Dicotyledones
Angiospermae
Euphorbiaceae
Chemical composition
Aculeata
Formicidae
Interspecific comparison
Allelopathy
Biological activity
Sensitivity resistance
Leguminosae
Animal plant relation
Arthropoda
Myrmecophilous
Acacia
Phenols
Defense mechanism
Spermatophyta
Hymenoptera
Invertebrata
Vegetal tannin
Language English
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– name: Blackwell Publishers
– name: Blackwell
References McKey, D.. 1984. Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16: 81-99.
Agrawal, A. A. and Dubin-Thaler, B. J.. 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.
Bazzaz, F. A. and Grace, J. (eds). 1997. Plant resource allocation. Academic Press.
Mueller-Harvey, I.. 2001. Analysis of hydrolysable tannins. Anim. Feed Sci. Technol. 91: 3-20.
Janzen, D. H.. 1974. Swollen-thorn acacias of Central America. Smithsonian Institution Press.
Jones, C. G. and Hartley, S. E.. 1999. A protein competition model of phenolic allocation. Oikos 86: 27-44.
Feeny, P.. 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry 10: 1-40.
Rudd, V. E.. 1966. Acacia cochliacantha or Acacia cymbispina in Mexico?. Leaflets of Western Botany X: 257-262.
McMurrough, I. and McDowell, J.. 1978. Chromatographic separation and automated analysis of flavanols. Anal. Biochem. 91: 92-100.
Hain, R., Reif, H. J., Krause, E. et al. 1993. Disease resistance results from foreign phyotalexin expression in a novel plant. Nature 361: 153-156.
Herms, D. A. and Mattson, W. J.. 1992. The dilemma of plants: to grow or to defend. Q. Rev. Biol. 67: 283-335.
Janzen, D. H.. 1972. Protection of Barteria (Passifloraceae) by Pachysima ants (Pseudomyrmecinae) in a Nigerian rain forest. Ecology 53: 885-892.
Seigler, D. S. and Ebinger, J. E.. 1995. Taxonomic revision of the ant-acacias (Fabaceae, Mimosoideae; Acacia, series Gummiferae) of the new world. Ann. Missouri Bot. Garden 82: 117-138.
Janzen, D. H.. 1969. Allelopathy by myrmecophytes: the ant Azteca as an allelopathic agent of Cecropia. Ecology 50: 147-153.
Shirley, B. W.. 1996. Flavonoid biosynthesis: 'new' functions for an 'old' pathway. Trends Plant Sci. 1: 377-382.
Hammerschmidt, R.. 1999a. Induced disease resistance: how do induced plants stop pathogens?. Physiol. Mol. Plant Pathol. 55: 77-84.
Blattner, F. R., Weising, K., Bänfer, G. et al. 2001. Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Mol. Phylogenet. Evol. 19.
Dyer, L. A., Dodson, C. D., Beihoffer, J. and Letourneau, D. K.. 2001. Trade-offs in antiherbivore defenses in Piper cenocladum: ant mutualists versus plant secondary metabolites. J. Chem. Ecol. 27: 581-592.
Heil, M., Fiala, B., Boller, T. and Linsenmair, K. E.. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86: 146-149.
Yu, H. and Sutton, J. C.. 1997. Morphological development and interactions of Gliocladium roseum and Botrytis cinerea in raspberry. Can. J. Phytopathol. 19: 237-245.
Hammerschmidt, R.. 1999b. Phytoalexins: what have we learned after 60 years?. Annu. Rev. Phytopathol. 37: 285-306.
Standley, . 1920. Trees and Shrubs of Mexico. - Contributions from the US National Herbarium Vol. 23.
Bieza, K. and Lois, R.. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol. 126: 1105-1115.
Letourneau, D. K. and Barbosa, P.. 1999. Ants, stem borers and pubescence in Endospermum in Papua New Guinea. Biotropica 31: 295-302.
Rehr, S. S., Feeny, P. P. and Janzen, D. H.. 1973. Chemical defence in Central American non-ant Acacias. J. Anim. Ecol. 42: 405-416.
Fiala, B., Maschwitz, U., Tho, Y. P. and Helbig, A. J.. 1989. Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79: 463-470.
Heil, M., Hilpert, A., Fiala, B. and Linsenmair, K. E.. 2001b. Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 126: 404-408.
Gaume, L., McKey, D. and 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: 209-216.
Mole, S. and Waterman, P. G.. 1987a. A critical analysis of techniques for measuring tannins in ecological studies II. Techniques for biochemically defining tannins. Oecologia 72: 148-156.
Slik, J. W. F.. 1998. A key to the Macaranga Thou. and Mallotus Lour. (Euphorbiaceae) species of east Kalimantan (Indonesia). Flora Malesiana Bull. 12: 157-178.
Brattsen, L. B., Samuelian, J. H., Long, K. Y. et al. 1983. Cyanide as a feeding stimulant for the southern armyworm, Spodoptera eridania. Ecol. Entomol. 8: 125-132.
Perello, A., Monaco, C. and Cordo, C.. 1997. Evaluation of Trichoderma harzianum and Gliocladium roseum in controlling leaf blotch of wheat (Septoria tritici) under in vitro and greenhouse conditions. Z. Pflanzenkrankheiten und Pflanzenschutz - J. Plant Diseases and Protection 104: 588-598.
Hölldobler, B. and Wilson, E. O.. 1990. The ants. Springer.
Hughes, C.. 1998. Monograph of Leucaena (Leguminosae-Mimosoidaeae). Am. Soc. Plant Taxon.
Fiala, B., Grunsky, H., Maschwitz, U. and Linsenmair, K. E.. 1994. Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97: 186-192.
Davies, S. J., Lum, S. K. Y., Chan, R. and Wng, L. K.. 2001. Evolution of myrmecophytism in western malesian Macaranga (Euphorbiaceae). Evolution 55: 1542-1559.
Steward, J. L. and Keeler, K. H.. 1988. Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)?. Oikos 53: 79-86.
Coley, P. D.. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr. 53: 209-233.
Heil, M., Fiala, B., Maschwitz, U. and Linsenmair, K. E.. 2001a. On benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126: 395-403.
Mole, S. and Waterman, P. G.. 1987b. A critical analysis of techniques for measuring tannins in ecological studies. I. Techniques for chemically defining tannins. Oecologia 72: 137-147.
Rocha, C. F. D. and Bergallo, H. G.. 1992. Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs Coelomera ruficornis on Cecropia pachystachya. Oecologia 91: 249-252.
Heil, M. and Baldwin, I. T.. 2002. Fitness costs of induced resistance - the emerging experimental support for a slippery concept. Trends Plant Sci. 7: 61-67.
Heil, M., Fiala, B., Linsenmair, K. E. et al. 1997. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via mutualistic ant partners. J. Ecol. 85: 847-861.
Beattie, A. J.. 1985. The evolutionary ecology of ant-plant mutualisms. Cambridge Univ. Press.
Seigler, D. S. and Ebinger, J. E.. 1987. Cyanogenic glycosides in ant-acacias of Mexico and Central America. Southwestern Nat. 32: 499-503.
Taiz, L. and Zeiger, E.. 1998. Plant physiology. Sinauer Associations.
Martin, J. S. and Martin, M. M.. 1982. Tannin assays in ecological studies: lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents in mature foliage of six oak species. Oecologia 54: 205-211.
Bazzaz, F. A., Chiariello, N. R., Coley, P. D. and Pitelka, L. F.. 1987. Allocating resources to reproduction and defense. BioScience 37: 58-67.
Baldwin, I. T. and Preston, C. A.. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta 208: 137-145.
Fiala, B. and 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.
Heil, M., Staehelin, C. and McKey, D.. 2000. Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences?. Naturwissenschaften 87: 555-558.
Janzen, D. H.. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20: 249-275.
Heil, M., Koch, T., Hilpert, A. et al. 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: 1083-1088.
McKey, D.. 1974. Adaptive patterns in alkaloid physiology. Am. Nat. 108: 305-320.
Treutter, D.. 1989. Chemical reaction detection of catechins and proanthocyanidins with 4-dimethylaminocinnamaldehyde. J. Chromatogr. 467: 185-193.
McKey, D.. 2000. Leonardoxa africana (Leguminoase: Caesalpinioideae): a complex of mostly allopatric subspecies. Adansonia 22: 71-109.
Eck, G., Fiala, B., Linsenmair, K. E. and Proksch, P.. 2001. Trade off between chemical and biotic anti-herbivore defense in the Southeast Asian plant genus Macaranga. J. Chem. Ecol. 27: 1979-1996.
Karban, R. and Baldwin, I. T.. 1997. Induced responses to herbivory. Univ. of Chicago Press.
Whitmore, T. C.. 1967. Studies in Macaranga, an easy genus of Malayan wayside trees. Malayan Nat. J. 20: 89-99.
Heil, M., Fiala, B., Kaiser, W. and Linsenmair, K. E.. 1998. Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct. Ecol. 12: 117-122.
Janzen, D. H.. 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.
Coley, P. D., Bryant, J. P. and Chapin, F. S. III. 1985. Resource availability and plant antiherbivore defense. Science 230: 895-899.
Davidson, D. W. and McKey, D.. 1993. The evolutionary ecology of symbiotic ant-plant relationships. J. Hymenoptera Res. 2: 13-83.
Tollrian, R. and Harvell, C. D.. 1999. The ecology and evolution of inducible defenses. Princeton Univ. Press.
Simms, E. L. and Fritz, R. S.. 1990. The ecology and evolution of host-plant resistance to insects. Trends Ecol. Evol. 5: 356-360.
Schroers, F. J., Samuels, G. J., Seifert, K. A. and Gams, W.. 1999. Classification of the mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its relationship to Bionectria ochroleuca, a
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1985; 230
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References_xml – reference: Heil, M., Fiala, B., Boller, T. and Linsenmair, K. E.. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86: 146-149.
– reference: Beattie, A. J.. 1985. The evolutionary ecology of ant-plant mutualisms. Cambridge Univ. Press.
– reference: McKey, D.. 1984. Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16: 81-99.
– reference: Taiz, L. and Zeiger, E.. 1998. Plant physiology. Sinauer Associations.
– reference: Hughes, C.. 1998. Monograph of Leucaena (Leguminosae-Mimosoidaeae). Am. Soc. Plant Taxon.
– reference: Feeny, P.. 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry 10: 1-40.
– reference: Brattsen, L. B., Samuelian, J. H., Long, K. Y. et al. 1983. Cyanide as a feeding stimulant for the southern armyworm, Spodoptera eridania. Ecol. Entomol. 8: 125-132.
– reference: Heil, M., Fiala, B., Linsenmair, K. E. et al. 1997. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via mutualistic ant partners. J. Ecol. 85: 847-861.
– reference: Heil, M., Fiala, B., Kaiser, W. and Linsenmair, K. E.. 1998. Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct. Ecol. 12: 117-122.
– reference: Heil, M., Koch, T., Hilpert, A. et al. 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: 1083-1088.
– reference: Heil, M., Hilpert, A., Fiala, B. and Linsenmair, K. E.. 2001b. Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 126: 404-408.
– reference: Janzen, D. H.. 1974. Swollen-thorn acacias of Central America. Smithsonian Institution Press.
– reference: McKey, D.. 2000. Leonardoxa africana (Leguminoase: Caesalpinioideae): a complex of mostly allopatric subspecies. Adansonia 22: 71-109.
– reference: Steward, J. L. and Keeler, K. H.. 1988. Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)?. Oikos 53: 79-86.
– reference: Bazzaz, F. A. and Grace, J. (eds). 1997. Plant resource allocation. Academic Press.
– reference: Fiala, B. and 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.
– reference: Herms, D. A. and Mattson, W. J.. 1992. The dilemma of plants: to grow or to defend. Q. Rev. Biol. 67: 283-335.
– reference: Janzen, D. H.. 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.
– reference: McKey, D.. 1974. Adaptive patterns in alkaloid physiology. Am. Nat. 108: 305-320.
– reference: Davies, S. J., Lum, S. K. Y., Chan, R. and Wng, L. K.. 2001. Evolution of myrmecophytism in western malesian Macaranga (Euphorbiaceae). Evolution 55: 1542-1559.
– reference: Schroers, F. J., Samuels, G. J., Seifert, K. A. and Gams, W.. 1999. Classification of the mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its relationship to Bionectria ochroleuca, and notes on other Gliocladium-like fungi. Mycologia 91: 365-385.
– reference: Seigler, D. S. and Ebinger, J. E.. 1987. Cyanogenic glycosides in ant-acacias of Mexico and Central America. Southwestern Nat. 32: 499-503.
– reference: Janzen, D. H.. 1967a. Fire, vegetation structure, and the ant×Acacia interaction in Central America. Ecology 48: 26-35.
– reference: Heil, M., Fiala, B., Maschwitz, U. and Linsenmair, K. E.. 2001a. On benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126: 395-403.
– reference: Hammerschmidt, R.. 1999b. Phytoalexins: what have we learned after 60 years?. Annu. Rev. Phytopathol. 37: 285-306.
– reference: Fiala, B., Maschwitz, U., Tho, Y. P. and Helbig, A. J.. 1989. Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79: 463-470.
– reference: Bazzaz, F. A., Chiariello, N. R., Coley, P. D. and Pitelka, L. F.. 1987. Allocating resources to reproduction and defense. BioScience 37: 58-67.
– reference: Tollrian, R. and Harvell, C. D.. 1999. The ecology and evolution of inducible defenses. Princeton Univ. Press.
– reference: Heil, M. and Baldwin, I. T.. 2002. Fitness costs of induced resistance - the emerging experimental support for a slippery concept. Trends Plant Sci. 7: 61-67.
– reference: McMurrough, I. and McDowell, J.. 1978. Chromatographic separation and automated analysis of flavanols. Anal. Biochem. 91: 92-100.
– reference: Davidson, D. W. and McKey, D.. 1993. The evolutionary ecology of symbiotic ant-plant relationships. J. Hymenoptera Res. 2: 13-83.
– reference: Schofield, P., Mbugua, D. M. and Pell, A. N.. 2001. Analysis of condensed tannins: a review. Anim. Feed Sci. Technol. 91: 21-40.
– reference: Shirley, B. W.. 1996. Flavonoid biosynthesis: 'new' functions for an 'old' pathway. Trends Plant Sci. 1: 377-382.
– reference: Coley, P. D., Bryant, J. P. and Chapin, F. S. III. 1985. Resource availability and plant antiherbivore defense. Science 230: 895-899.
– reference: Letourneau, D. K.. 1998. Ants, stem-borers, and fungal pathogens: experimental tests of a fitness advantage in Piper ant-plants. Ecology 79: 593-603.
– reference: Bieza, K. and Lois, R.. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol. 126: 1105-1115.
– reference: Hölldobler, B. and Wilson, E. O.. 1990. The ants. Springer.
– reference: Rocha, C. F. D. and Bergallo, H. G.. 1992. Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs Coelomera ruficornis on Cecropia pachystachya. Oecologia 91: 249-252.
– reference: Mueller-Harvey, I.. 2001. Analysis of hydrolysable tannins. Anim. Feed Sci. Technol. 91: 3-20.
– reference: Jones, C. G. and Hartley, S. E.. 1999. A protein competition model of phenolic allocation. Oikos 86: 27-44.
– reference: Eck, G., Fiala, B., Linsenmair, K. E. and Proksch, P.. 2001. Trade off between chemical and biotic anti-herbivore defense in the Southeast Asian plant genus Macaranga. J. Chem. Ecol. 27: 1979-1996.
– reference: Karban, R. and Baldwin, I. T.. 1997. Induced responses to herbivory. Univ. of Chicago Press.
– reference: Hain, R., Reif, H. J., Krause, E. et al. 1993. Disease resistance results from foreign phyotalexin expression in a novel plant. Nature 361: 153-156.
– reference: Letourneau, D. K. and Barbosa, P.. 1999. Ants, stem borers and pubescence in Endospermum in Papua New Guinea. Biotropica 31: 295-302.
– reference: Yu, H. and Sutton, J. C.. 1997. Morphological development and interactions of Gliocladium roseum and Botrytis cinerea in raspberry. Can. J. Phytopathol. 19: 237-245.
– reference: Slik, J. W. F.. 1998. A key to the Macaranga Thou. and Mallotus Lour. (Euphorbiaceae) species of east Kalimantan (Indonesia). Flora Malesiana Bull. 12: 157-178.
– reference: Rehr, S. S., Feeny, P. P. and Janzen, D. H.. 1973. Chemical defence in Central American non-ant Acacias. J. Anim. Ecol. 42: 405-416.
– reference: Blattner, F. R., Weising, K., Bänfer, G. et al. 2001. Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Mol. Phylogenet. Evol. 19.
– reference: Mole, S. and Waterman, P. G.. 1987a. A critical analysis of techniques for measuring tannins in ecological studies II. Techniques for biochemically defining tannins. Oecologia 72: 148-156.
– reference: Janzen, D. H.. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20: 249-275.
– reference: Mole, S. and Waterman, P. G.. 1987b. A critical analysis of techniques for measuring tannins in ecological studies. I. Techniques for chemically defining tannins. Oecologia 72: 137-147.
– reference: Seigler, D. S. and Ebinger, J. E.. 1995. Taxonomic revision of the ant-acacias (Fabaceae, Mimosoideae; Acacia, series Gummiferae) of the new world. Ann. Missouri Bot. Garden 82: 117-138.
– reference: Heil, M., Staehelin, C. and McKey, D.. 2000. Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences?. Naturwissenschaften 87: 555-558.
– reference: Gaume, L., McKey, D. and 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: 209-216.
– reference: Simms, E. L. and Fritz, R. S.. 1990. The ecology and evolution of host-plant resistance to insects. Trends Ecol. Evol. 5: 356-360.
– reference: Standley, . 1920. Trees and Shrubs of Mexico. - Contributions from the US National Herbarium Vol. 23.
– reference: Whitmore, T. C.. 1967. Studies in Macaranga, an easy genus of Malayan wayside trees. Malayan Nat. J. 20: 89-99.
– reference: Perello, A., Monaco, C. and Cordo, C.. 1997. Evaluation of Trichoderma harzianum and Gliocladium roseum in controlling leaf blotch of wheat (Septoria tritici) under in vitro and greenhouse conditions. Z. Pflanzenkrankheiten und Pflanzenschutz - J. Plant Diseases and Protection 104: 588-598.
– reference: Agrawal, A. A. and Dubin-Thaler, B. J.. 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.
– reference: Dyer, L. A., Dodson, C. D., Beihoffer, J. and Letourneau, D. K.. 2001. Trade-offs in antiherbivore defenses in Piper cenocladum: ant mutualists versus plant secondary metabolites. J. Chem. Ecol. 27: 581-592.
– reference: Janzen, D. H.. 1972. Protection of Barteria (Passifloraceae) by Pachysima ants (Pseudomyrmecinae) in a Nigerian rain forest. Ecology 53: 885-892.
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SSID ssj0007774
Score 1.9896312
Snippet Since its original formulation by Janzen in 1966, the hypothesis that obligate ant-plants (myrmecophytes) defended effectively against herbivores by resident...
Since its original formulation by Janzen in 1966, the hypothesis that obligate ant‐plants (myrmecophytes) defended effectively against herbivores by resident...
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pascalfrancis
crossref
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jstor
istex
SourceType Aggregation Database
Index Database
Enrichment Source
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StartPage 457
SubjectTerms Animal and plant ecology
Animal, plant and microbial ecology
Ants
Autoecology
Biological and medical sciences
Caterpillars
Flavonoids
Fundamental and applied biological sciences. Psychology
Fungal spores
Herbivores
Leaves
Phytophagous insects
Plants
Plants and fungi
Species
Tannins
Title Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis
URI https://api.istex.fr/ark:/67375/WNG-9WCX8M1L-W/fulltext.pdf
https://www.jstor.org/stable/3547834
https://onlinelibrary.wiley.com/doi/abs/10.1034%2Fj.1600-0706.2002.11954.x
https://www.proquest.com/docview/18676689
Volume 99
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