Correlations between physical and chemical defences in plants: Tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

New Phytologist

Volumn 198, Issue 1, 2013, Pages 252-263

  Moles, Angela T ^a   Peco, Begoña ^b   Wallis, Ian R ^c   Foley, William J ^c   Poore, Alistair G B ^a   Seabloom, Eric W ^d   Vesk, Peter A ^e   Bisigato, Alejandro J ^f   Cella Pizarro, Lucrecia ^f   Clark, Connie J ^g   Cohen, Philippe S ^h   Cornwell, William K ⁱ   Edwards, Will ^j   Ejrnæs, Rasmus ^k   Gonzales Ojeda, Therany ^l   Graae, Bente J ^m,n   Hay, Gregory ^o   Lumbwe, Fainess C ^p   Magaña Rodríguez, Benjamín ^q   Moore, Ben D ^j,r   Peri, Pablo L ^s   Poulsen, John R ^g   Stegen, James C ^t   Veldtman, Ruan ^u,v   von Zeipel, Hugo ^w   Andrew, Nigel R ^x   Boulter, Sarah L ^y   Borer, Elizabeth T ^d   Cornelissen, Johannes H C ⁱ   Farji Brener, Alejandro G ^z   Degabriel, Jane L ^j   Jurado, Enrique ^aa   Kyhn, Line A ^ab   Low, Bill ^ac   Mulder, Christa P H ^ad   Reardon Smith, Kathryn ^ae   Rodríguez Velázquez, Jorge ^af   De Fortier, An ^ag   Zheng, Zheng ^ah   Blendinger, Pedro G ^ai   Enquist, Brian J ^aj   Facelli, Jose M ⁿ   Knight, Tiffany ^ak   Majer, Jonathan D ^al   Martínez Ramos, Miguel ^af   Mcquillan, Peter ^am   Hui, Francis K C ^a   more..

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^g WOODS HOLE RESEARCH CENTER   (United States)

^h STANFORD UNIVERSITY   (United States)

ⁱ VU UNIVERSITY AMSTERDAM   (Netherlands)

^j JAMES COOK UNIVERSITY   (Australia)

^k AARHUS UNIVERSITY   (Denmark)

^l UNIVERSIDAD NACIONAL DE SAN ANTONIO ABAD DEL CUSCO   (Peru)

^m UMEÅ UNIVERSITY   (Sweden)

ⁿ NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^o UNIVERSITY OF ADELAIDE   (Australia)

^p UNIVERSITY OF ZAMBIA   (Zambia)

^q VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^r WESTERN SYDNEY UNIVERSITY   (Australia)

^s UNIVERSIDAD NACIONAL DE LA PATAGONIA AUSTRAL   (Argentina)

^t PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^u STELLENBOSCH UNIVERSITY   (South Africa)

^v SOUTH AFRICAN NATIONAL BIODIVERSITY INSTITUTE   (South Africa)

^w MID SWEDEN UNIVERSITY   (Sweden)

^x UNIVERSITY OF NEW ENGLAND   (Australia)

^y GRIFFITH UNIVERSITY   (Australia)

^z LABORATORIO ECOTONO   (Argentina)

^aa UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

^ab NATIONAL ENVIRONMENTAL RESEARCH INSTITUTE   (Denmark)

^ac Low Ecological Services   (Australia)

^ad UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^ae UNIVERSITY OF SOUTHERN QUEENSLAND   (Australia)

^af INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS Y SUSTENTABILIDAD   (Mexico)

^ag UNIVERSITY OF ZULULAND   (South Africa)

^ah KEY LABORATORY OF TROPICAL FOREST ECOLOGY   (China)

^ai UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

^aj University of Arizona   (United States)

^ak WASHINGTON UNIVERSITY   (United States)

^al CURTIN UNIVERSITY   (Australia)

^am UNIVERSITY OF TASMANIA   (Australia)

more..

Author keywords

Cyanogenesis; Extrafloral nectaries; Hair; Leaf toughness; Lipid; Plant herbivore interactions; Spines; Tannin

Indexed keywords

ABUNDANCE; ANTIHERBIVORE DEFENSE; COEXISTENCE; DATA SET; FELID; GROWTH FORM; HERBIVORY; LIFE HISTORY TRAIT; LIPID; NECTARY; PHYLOGENY; PLANT-HERBIVORE INTERACTION; SKIN; TANNIN; TRADE-OFF; TRICHOME;

ARTICLE; CHEMISTRY; CLUSTER ANALYSIS; IMMUNOLOGY; PLANT; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT;

CLUSTER ANALYSIS; PLANTS; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT, HERITABLE;

EID: 84874195500     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12116     Document Type: Article

References (90)

1. Agrawal AA. 2007. Macroevolution of plant defense strategies. Trends in Ecology & Evolution 22: 103-109.
2. Agrawal AA. 2011. Current trends in the evolutionary ecology of plant defense. Functional Ecology 25: 420-432.
3. Agrawal AA, Fishbein M. 2006. Plant defense syndromes. Ecology 87: S132-S149.
4. Agrawal AA, Konno K. 2009. Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annual Review of Ecology Evolution and Systematics 40: 311-331.
5. Agrawal AA, Lajeunesse MJ, Fishbein M. 2008. Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomologia Experimentalis Et Applicata 128: 126-138.
6. Angiosperm Phylogeny Group III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society. 161: 105-121.
7. Ballhorn DJ, Kautz S, Lieberei R. 2010. Comparing responses of generalist and specialist herbivores to various cyanogenic plant features. Entomologia Experimentalis Et Applicata 134: 245-259.
8. Barbehenn RV, Constabel CP. 2011. Tannins in plant-herbivore interactions. Phytochemistry 72: 1551-1565.
9. Choong MF, Lucas PW, Ong JSY, Pereira B, Tan HTW, Turner IM. 1992. Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytologist 121: 597-610.
10. Clarke KR, Somerfield PJ, Gorley RN. 2008. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. Journal of Experimental Marine Biology and Ecology 366: 56-89.
11. Clissold FJ, Sanson GD, Read J, Simpson SJ. 2009. Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology 90: 3393-3405.
12. Coley PD. 1988. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74: 531-536.
13. Coley PD, Bryant JP, Chapin FS. 1985. Resource availability and plant antiherbivore defense. Science 230: 895-899.
14. Cooke J, Leishman MR. 2012. Tradeoffs between foliar silicon and carbon-based defences: evidence from vegetation communities of contrasting soil types. Oikos 121: 2052-2060.
15. Cornelissen JHC, Gwynn-Jones D, van Logtestijn RSP, Quested HM, Callaghan TV, Aerts R. 2009. A hypothesised triangular model combining tradeoffs of foliar defence quality and quantity: support from subarctic seed plant species. In: Ming D, Werger MJA, eds. A spectrum of ecological studies. Chongqing, China: Southwest China Normal University Press, 36-44.
16. Costantini P, Linting M, Porzio GC. 2009. Mining performance data through nonlinear PCA with optimal scaling. Applied Stochastic Models in Business and Industry 26: 85-101.
17. Cyr H, Pace ML. 1993. Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361: 148-150.
18. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
19. Djamin A, Pathak MD. 1967. Role of silica in resistance to Asiatic rice borer Chilo suppressalis (Walker) in rice varieties. Journal of Economic Entomology 60: 347-351.
20. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 11: 539-548.
21. Duffey SS, Stout MJ. 1996. Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology 32: 3-37.
22. Eck G, Fiala B, Linsenmair KE, Bin Hashim R, Proksch P. 2001. Trade-off between chemical and biotic antiherbivore defense in the south east Asian plant genus Macaranga. Journal of Chemical Ecology 27: 1979-1996.
23. Ellis RN, Kroonenberg PM, Harch BD, Basford KE. 2006. Non-linear principal component analysis: an alternative method for finding patterns in environmental data. Environmetrics 17: 1-11.
24. Feeny P. 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry 10: 1-40.
25. Franceschi VR, Nakata PA. 2005. Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56: 41-71.
26. Fritz RS, Hochwender CG, Lewkiewicz DA, Bothwell S, Orians CM. 2001. Seedling herbivory by slugs in a willow hybrid system: developmental changes in damage, chemical defense, and plant performance. Oecologia 129: 87-97.
27. Furstenburg D, Vanhoven W. 1994. Condensed tannin as anti-defoliate agent against browsing by giraffe (Giraffa camelopardalis) in the Kruger National Park. Comparative Biochemistry and Physiology A - Physiology 107: 425-431.
28. Galimuhtasib HU, Smith CC, Higgins JJ. 1992. The effect of silica in grasses on the feeding behavior of the prairie vole, Microtus ochrogaster. Ecology 73: 1724-1729.
29. Garland T, Harvey PH, Ives TR. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41: 18-32.
30. van Gelder HA, Poorter L, Sterck FJ. 2006. Wood mechanics, allometry, and life-history variation in a tropical rain forest tree community. New Phytologist 171: 367-378.
31. Gifi A. 1991. Nonlinear multivariate analysis. Chichester, UK: Wiley.
32. Grace JB. 2006. Structural equation modeling and natural systems. Cambridge, UK: Cambridge University Press.
33. Haddad NM, Hicks WM. 2000. Host pubescence and the behavior and performance of the butterfly Papilio troilus (Lepidoptera: Papilionidae). Environmental Entomology 29: 299-303.
34. Hanley ME, Lamont BB. 2002. Relationships between physical and chemical attributes of congeneric seedlings: how important is seedling defence? Functional Ecology 16: 216-222.
35. Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM. 2007. Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology Evolution and Systematics 8: 157-178.
36. Hay ME, Fenical W. 1988. Marine plant-herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics 19: 111-145.
37. Herms DA, Mattson WJ. 1992. The dilemma of plants: to grow or defend. Quarterly Review of Biology 67: 283-335.
38. Iddles TL, Read J, Sanson GD. 2003. The potential contribution of biomechanical properties to anti-herbivore defence in seedlings of six Australian rainforest trees. Australian Journal of Botany 51: 119-128.
39. Janzen DH. 1966. Coevolution of mutualism between ants and Acacias in Central America. Evolution 20: 249-275.
40. Janzen DH. 1974. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6: 69-103.
41. Jones AS, Lamont BB, Fairbanks MM, Rafferty CM. 2003. Kangaroos avoid eating seedlings with or near others with volatile essential oils. Journal of Chemical Ecology 29: 2621-2635.
42. Karban R, Meyers JH. 1989. Induced plant responses to herbivory. Annual Review of Ecology and Systematics 20: 331-348.
43. Kempel A, Schadler M, Chrobock T, Fischer M, van Kleunen M. 2011. Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proceedings of the National Academy of Sciences, USA 108: 5685-5689.
44. Koricheva J. 2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83: 176-190.
45. Koricheva J, Nykanen H, Gianoli E. 2004. Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? American Naturalist 163: E64-E75.
46. Koricheva J, Romero GQ. 2012. You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants. Biology Letters 8: 628-630.
47. Korth KL, Doege SJ, Park SH, Goggin FL, Wang Q, Gomez SK, Liu G, Jia L, Nakata PA. 2006. Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiology 141: 188-195.
48. Kricher J. 2011. Tropical ecology. Princeton, NJ, USA: Princeton University Press.
49. Kursar TA, Coley PD. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochemical Systematics and Ecology 31: 929-949.
50. Legendre P, Legendre L. 1998. Numerical ecology. Amsterdam, the Netherlands: Elsevier Scientific Publishing Company.
51. Leimu R, Koricheva J. 2006. A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112: 1-9.
52. Levin DA. 1976. Alkaloid-bearing plants: an ecogeographic perspective. American Naturalist 110: 261-284.
53. Lincoln DE. 1985. Host plant protein and phenolic resin effects on larval growth and survival of a butterfly. Journal of Chemical Ecology 11: 1459-1467.
54. Mabberley DJ. 1997. The Plant book. Cambridge, UK: Cambridge University Press.
55. Marko G, Gyuricza V, Bernath J, Altbacker V. 2008. Essential oil yield and composition reflect browsing damage of junipers. Journal of Chemical Ecology 34: 1545-1552.
56. Massey FP, Ennos AR, Hartley SE. 2006. Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. Journal of Animal Ecology 75: 595-603.
57. Moles AT, Wallis IR, Foley WJ, Warton DI, Stegen JC, Bisigato AJ, Cella-Pizarro L, Clark CJ, Cohen PS, Cornwell WK et al. 2011. Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytologist 191: 777-788.
58. Moles AT, Westoby M. 2000. Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos 90: 517-524.
59. Moles AT, Westoby M. 2006. Seed size and plant strategy across the whole life cycle. Oikos 113: 91-105.
60. Morris WF, Traw MB, Bergelson J. 2006. On testing for a tradeoff between constitutive and induced resistance. Oikos 112: 102-110.
61. Mueller-Harvey I. 2006. Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86: 2010-2037.
62. Ness JH, Morris WF, Bronstein JL. 2009. For ant-protected plants, the best defense is a hungry offense. Ecology 90: 2823-2831.
63. Núñez-Farfán J, Fornoni J, Valverde PL. 2007. The evolution of resistance and tolerance to herbivores. Annual Review of Ecology Evolution and Systematics 38: 541-566.
64. Paul VJ, Hay ME. 1986. Seaweed susceptibility to herbivory: chemical and morphological correlates. Marine Ecology Progress Series 33: 255-264.
65. Peeters PJ. 2002. Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biological Journal of the Linnean Society 77: 43-65.
66. Perez-Harguindeguy N, Diaz S, Vendramini F, Cornelissen JHC, Gurvich DE, Cabido M. 2003. Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecology 28: 642-650.
67. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA et al. 2012. Global patterns in the impact of marine herbivores on benthic primary producers. Ecology Letters 15: 912-922.
68. R Development Core Team. 2007. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
69. Read J, Sanson GD, Caldwell E, Clissold FJ, Chatain A, Peeters P, Lamont BB, De Garine-Wichatitsky M, Jaffre T, Kerr S. 2009. Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia. Annals of Botany 103: 757-767.
70. Regan HM, Colyvan M, Burgman MA. 2002. A taxonomy and treatment of uncertainty for ecology and conservation biology. Ecological Applications 12: 618-628.
71. Rehr SS, Feeny PP, Janzen DH. 1973. Chemical defence of central American non-ant acacias. Journal of Animal Ecology 42: 405-416.
72. Rhoades DF, Cates RG. 1976. Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry 10: 168-213.
73. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
74. Roslin T, Salminen JP. 2008. Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117: 1560-1568.
75. Rudgers JA, Strauss SY, Wendel JE. 2004. Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). American Journal of Botany 91: 871-880.
76. Sammel MD, Ryan LM, Legler JM. 1997. Latent variable models for mixed discrete and continuous outcomes. Journal of the Royal Statistical Society Series B 59: 667-678.
77. Shimada T. 2006. Salivary proteins as a defense against dietary tannins. Journal of Chemical Ecology 32: 1149-1163.
78. Silanikove N, Shinder D, Gilboa N, Eyal M, Nitsan Z. 1996. Binding of poly(ethylene glycol) to samples of forage plants as an assay of tannins and their negative effects on ruminal degradation. Journal of Agricultural and Food Chemistry 44: 3230-3234.
79. da Silva DM, Batalha MA. 2011. Defense syndromes against herbivory in a cerrado plant community. Plant Ecology 212: 181-193.
80. Spalinger DE, Collins WB, Hanley TA, Cassara NE, Carnahan AM. 2010. The impact of tannins on protein, dry matter, and energy digestion in moose (Alces alces). Canadian Journal of Zoology-Revue Canadienne De Zoologie 88: 977-987.
81. Steward JL, Keeler KH. 1988. Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae). Oikos 53: 79-86.
82. Strauss SY, Agrawal AA. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution 14: 179-185.
83. Tanentzap AJ, Lee WG, Dugdale JS, Patrick BP, Fenner M, Walker S, Coomes DA. 2011. Differential responses of vertebrate and invertebrate herbivores to traits of New Zealand subalpine shrubs. Ecology 92: 994-999.
84. Travers-Martin N, Muller C. 2008. Matching plant defence syndromes with performance and preference of a specialist herbivore. Functional Ecology 22: 1033-1043.
85. Turner IM. 1994. Sclerophylly - primarily protective? Functional Ecology 8: 669-675.
86. Twigg LE, Socha LV. 1996. Physical versus chemical defence mechanisms in toxic Gastrolobium. Oecologia 108: 21-28.
87. Ward D, Spiegel M, Saltz D. 1997. Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. Journal of Chemical Ecology 23: 333-346.
88. Webb CO, Ackerly DD, Kembel SW. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098-2100.
89. Weiher E, van der Werf A, Thompson K, Roderick M, Garnier E, Eriksson O. 1999. Challenging Theophrastus: a common core list of plant traits for functional ecology. Journal of Vegetation Science 10: 609-620.
90. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M et al. 2004. The world-wide leaf economics spectrum. Nature 428: 821-827.