Evolutionary ecology of secondary compounds in ripe fruit: Case studies with capsaicin and emodin

Seed Dispersal: Theory and its Application in a Changing World

Volumn , Issue , 2007, Pages 37-58

  Levey, Douglas J ^a,b   Tewksbury, Joshua J ^b   Izhaki, Ido ^c   Tsahar, Ella ^d   Haak, David C ^b  

^a University of Florida   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF HAIFA   (Israel)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 40449109221     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (109)

1. Afik, D. and Karasov, W.H. (1995) The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76, 2247-2257.
2. Andelt, W.F., Burnham, K.P. and Baker, D.L. (1994) Effectiveness of capsaicin and Bitrex repellents for deterring browsing by captive Mule Deer. Journal of Wildlife Management 58, 330-334.
3. Anderson, J.A., Bor-Kang, L., Williams, H.J. and Scott, A.I. (1988) Deoxygenation of phenolic natural products: enzymatic conversion of emodin to chrysophanol. Journal of the American Chemical Society 110, 1623-1624.
4. Bairlein, F. (1996) Fruit-eating in birds and its nutritional consequences. Comparative Biochemistry and Physiology 113A, 215-224.
5. Barnea, A., Yom-Tov, Y. and Friedman, J. (1991) Does ingestion by birds affect seed germination. Functional Ecology 5, 394-402.
6. Berenbaum, M.R. (1995a) The chemistry of defense: theory and practice. Proceedings of the National Academy of Sciences 92, 2-8.
7. Berenbaum, M.R. (1995b) Turnabout is fair play: secondary roles for primary metabolites. Journal of Chemical Ecology 21, 125-139.
8. Blum, E., Liu, K., Mazourek, M., Yoo, E.Y., Jahn, M. and Paran, I. (2002) Molecular mapping of the C locus for presence of pungency in Capsicum. Genome 45, 702-705.
9. Bosland, P.W. (1994) Chiles: history, cultivation, and uses. In: Charalambous, G. (ed.) Spices, Herbs and Edible Fungi. Elsevier, Amsterdam, pp. 347-366.
10. Bosland, P.W. (1998) Chiles: a gift from a fiery God. HortScience 34, 809-811.
11. Bradshaw, H.D. and Schemske, D.W. (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176-178.
12. Cichewicz, R.H. and Thorpe, P.A. (1996) The antimicrobial properties of chile peppers (Capsicum species) and their uses in Mayan medicine. Journal of Ethnopharmacology 2, 61-70.
13. Cipollini, M.L. (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Revista Chilena de Hitoria Natural 73, 421-440.
14. Cipollini, M.L. and Levey, D.J. (1997a) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. American Naturalist 150, 346-372.
15. Cipollini, M.L. and Levey, D.J. (1997b) Antifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal. Ecology 78, 799-809.
16. Cipollini, M.L. and Levey, D.J. (1997c) Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78, 782-798.
17. Cipollini, M.L. and Stiles, E.W. (1991) Antifungal activity of ripe ericaceous fruits: phenolicacid interactions and palatability for dispersers. Biochemical Systematics and Ecology 20, 501-514.
18. Cipollini, M.L. and Stiles, E.W. (1992) Relative risks of microbial rot for fleshy fruits: significance with respect to dispersal and selection for secondary defense. Advances in Ecological Research 23, 35-91.
19. Cipollini, M.L. and Stiles, E.W. (1993) Fruit rot, antifungal defense, and palatability of fleshy fruits for frugivorous birds. Ecology 74, 751-762.
20. Cipollini, M.L., Paulk, E., Mink, K., Vaughn, K. and Fischer, T. (2004) Defense tradeoffs in fleshy fruits: effects of resource variation on growth, reproduction, and fruit secondary chemistry in Solanum carolinense. Journal of Chemical Ecology 30, 1-17.
21. Coley, P.D. (1986) Costs and benefits of defence by tannins in a neotropical tree. Oecologica 70, 352-368.
22. Cordell, G.A. and Araujo, O.E. (1993) Capsaicin: identification, nomenclature, and pharmacotherapy. Annals of Pharmacotherapy 27, 330-6.
23. D'arcy, W.G. and Eshbaugh, W.H. (1974) New World peppers (Capsicum-Solanaceae) north of Columbia: a resume. Baileya 19, 93-105.
24. Debkirtaniya, S., Ghosh, M.R., Mitra, S.R., Adityachaudhury, N. and Chatterjee, A. (1980) Note on the insecticidal properties of the fruits of chilli. Indian Journal of Agricultural Sciences 50, 510-512.
25. Dewick, P.M. (1998) Medicinal Natural Products: A Biosynthetic Approach. John Wiley and Sons, New York.
26. Dixon, R.A. and Paiva, N.L. (1995) Stress-induced phenylpropanoid metabolism. Plant and Cell 7, 1085-1097.
27. Ehrlen, J. and Eriksson, O. (1993) Toxicity in fleshy fruits: a non-adaptive trait? Oikos 66, 107-113.
28. Estrada, B., Pomar, F., Diaz, J., Merino, F., Bernal, M.A. (1999) Pungency level in fruits of the Padron pepper with different water supply. Scientia Horticulturae 81, 385-396.
29. Estrada, B., Bernal, M.A., Diaz, J., Pomar, F. and Merino, F. (2000) Fruit development in Capsicum annuum: changes in capsaicin, lignin, free phenolics, and peroxidase patterns. Journal of Agricultural and Food Chemistry 48, 6234-6239.
30. Evans, W.C. (1996) Trease & Evans'Pharmacognosy, 4th edn. W.B. Saunders Company, London.
31. Fujiwake, H., Suzuki, T. and Iwai, K. (1982) Formation and metabolism of the pungent principle of Capsicum fruits. 11. Capsaicinoid formation in the protoplast from the placenta of Capsicum fruits. Agricultural and Biological Chemistry 46, 2591-2592.
32. Gourley, L.C. and Howell, E. (1984) Factors in buckthorn invasion documented: control measure checked (Wisconsin). Restoration and Management Notes 2, 87.
33. Govindarajan, V.S. (1986) Capsicum: production, technology, chemistry, and quality. 3. Chemistry of the color, aroma, and pungency stimuli. CRC Critical Reviews in Food Science and Nutrition 24, 245-355.
34. Govindarajan, V.S. and Sathyanarayana, M.N. (1991) Capsicum: production, technology, chemistry, and quality. 5. Impact on physiology, pharmacology, nutrition, and metabolism -structure, pungency, pain, and desensitization sequences. Critical Reviews in Food Science and Nutrition 29, 435-474.
35. Govindarajan, V.S., Rajalakshmi, D. and Chand, N. (1987) Capsicum: production, technology, chemistry, and quality. 4. Evaluation of quality. CRC Critical Reviews in Food Science and Nutrition 25, 185-282.
36. Hall, R.D. and Yeoman, M.M. (1991) The influence of intracellular pools of phenylalanine derivatives upon the synthesis of capsaicin by immobilized cell-cultures of the chilie pepper Capsicum frutescens. Planta 185, 72-80.
37. Hamilton, J.G., Zangerl, A.R., DeLucia, E.H. and Berenbaum, M.R. (2001) The carbonnutrient balance hypothesis: its rise and fall. Ecology Letters 4, 86-95.
38. Harborne, J.B., Baxter, H. and Moss, G.P. (1999) Phytochemical Dictionary. A Handbook of Bioactive Compounds from Plants. Taylor and Francis, London.
39. Hasan, H.A.H. (1998) Studies on toxigenic fungi in roasted foodstuff (salted seed) and halotolerant activity of emodin-producing Aspergillus wentii. Folia Microbiologica 43, 383-391.
40. Herms, D.A. and Mattson, W.J. (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283-335.
41. Herrera, C.M. (1982) Defense of ripe fruits from pests: its significance in relation to plant-disperser interactions. American Naturalist 120, 218-241.
42. Herrera, C.M. (1984) A study of avian frugivores, bird-dispersed plants, and their interactions in Mediterranean scrublands. Ecological Monographs 54, 1-20.
43. Herrera, C.M. (2002) Seed dispersal by vertebrates. In: Herrera, C.M. and Pellmyr, O. (eds) Plant-Animal Interactions: An Evolutionary Approach. Blackwell Science, Oxford, pp. 185-210.
44. Howe, H.F. (1977) Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58, 539-50.
45. Hulme, P.E. and Benkman, C.W. (2002) Granivory. In: Herrera, C. and Pellmyr, O. (eds) Plant-Animal Interactions: An Evolutionary Approach. Blackwell Science, Oxford, pp. 132-156.
46. Irwin, R.E., Adler, L.S. and Brody, A.K. (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85, 1503-1511.
47. Iwai, K., Suzuki, T. and Fujiwake, H. (1979) Formation and accumulation of pungent principle of hot pepper fruits, Capsaicin and its analogs, in Capsicum-annuun var annuun cv. karayatsubusa at different growth-stages after flowering. Agricultural and Biological Chemistry 43, 2493-2498.
48. Izhaki, I. (2002a) Emodin: a secondary metabolite with multiple ecological functions in higher plants. New Phytologist 155, 205-217.
49. Izhaki, I. (2002b) The role of fruit traits in determining fruit removal in East Mediterranean ecosystems. In: Levey, D.J., Silva, W.R. and Galetti, M. (eds) Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation. CAB International, Wallingford, UK, pp. 161-175.
50. Izhaki, I. and Safriel, U.N. (1985) Why do fleshy-fruited plants of the Mediterranean scrub intercept fall-passage but not spring-passage of seed-dispersing migratory birds? Oecologia 67, 40-43.
51. Izhaki, I., Tsahar, E., Paluy, I. and Friedman, J. (2002) Within-population variation and interrelationships between morphology, nutritional content, and secondary compounds of Rhamnus alaternus fruits. New Phytologist 156, 217-223.
52. Janzen, D.H. (1971) Seed predation by animals. Annual Review of Ecology and Systematics 2, 465-492.
53. Janzen, D.H. (1977) Why fruits rot, seeds mould, and meat spoils. American Naturalist 111, 691-713.
54. Jordano, P. (2000) Fruits and frugivory. In: Fenner, M. (ed.) Seeds: The Ecology of Regeneration in Natural Plant Communities. CAB International, Wallingford, UK, pp. 105-151.
55. Kawada, T., Watanabe, T., Katsura, K., Takami, H. and Iwai, K. (1985) Formation and metabolism of pungent principle of Capsicum fruits. 15. Microdetermination of capsaicin by high-performance liquid-chromatography with electrochemical detection. Journal of Chromatography 329, 99-105.
56. Kessler, A. and Baldwin, I.T. (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299-328.
57. Kim, Y.M., Lee, C.H. and Lee, H.S. (2004) Anthraquinones isolated from Cassia tora (Leguminosae) seed show an antifungal property against phytopathogenic fungi. Journal of Agricultural and Food Chemistry 52, 6096-6100.
58. Koricheva, J. (2002) The carbon-nutrient balance hypothesis is dead: long live the carbonnutrient balance hypothesis?. Oikos 98, 537-539.
59. Lerdau, M. and Coley, P.D. (2002) Benefits of the carbon-nutrient balance hypothesis. Oikos 98, 534-536.
60. Levey, D.J. (2004) The evolutionary ecology of ethanol production and alcoholism. Integrative and Comparative Biology 44, 284-289.
61. Levey, D.J. and Cipollini, M.L. (1998) A glycoalkaloid in ripe fruit deters consumption by cedar waxwings. Auk 115, 359-367.
62. Levey, D.J. and Martínez del Rio, C. (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk 118, 819-831.
63. Levey, D.J., Tewksbury, J.J., Cipollini, M.L. and Carlo, T.A. (2006) A field test of the directed deterrence hypothesis in two species of wild chili. Oecologia 150, 61-68.
64. Lotan, A. (2005) The impact of environmental conditions on the morphology, nutritional value and secondary metabolites in Ochradenus baccatus fruits. MSc thesis, University of Haifa, Israel.
65. Lund, S.T. and Bohlman, J. (2006) The molecular basis for wine grape quality: a volatile subject. Science 311, 804-805.
66. Mack, A.L. (2000) Did fleshy fruit evolve as a defence against seed loss rather than as a dispersal mechanism?. Journal of Biosciences 25, 93-97.
67. McCarty, J., Levey, D.J., Greenberg, C. and Sargent, S. (2002) Spatial and temporal variation in fruit use by wildlife in a forested landscape. Forest Ecology and Management 164, 277-291.
68. McLeod, M.J., Guttman, S.I. and Eshbaugh, W.H. (1982) Early evolution of chile peppers (Capsicum). Economic Botany 36, 361-386.
69. Murray, K.G., Russell, S., Picone, C.M., Winnett-Murray, K., Sherwood, W. and Kuhlmann, M.L. (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75, 989-994.
70. Norman, D.M., Mason, J.R. and Clark, L. (1992) Capsaicin effects on consumption of food by cedar waxwings and house finches. Wilson Bulletin 104, 549-551.
71. Oh, N.-S., Shin, D.-B., In, M.-J., Chang, Y.-I. and Han, M. (2004) Effects of capsaicin on the growth and ethanol production of Zygosaccharomyces rouxii KFY80 isolated from Gochujang (fermented hot pepper paste). Food Science and Biotechnology 13, 749-753.
72. Paneitz, A. and Westendorf, J. (1999) Anthranoid contents of rhubarb (Rheum undulatum L.) and other Rheum species and their toxicological relevance. European Food Research and Technology 210, 97-101.
73. Sagers, C.L. and Coley, P.D. (1995) Benefits and costs of defence in a neotropical shrub. Ecology 76, 1835-1843.
74. Santilli, F., Mori, L. and Galardi, L. (2004) Evaluation of three repellents for the prevention of damage to olive seedlings by deer. European Journal of Wildlife Research 50, 85-89.
75. Schaefer, H.M., Schmidt, V. and Winkler, H. (2003) Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos 102, 318-329.
76. Schafer, E.W., Bowles, W.A. and Hurlbut, J. (1983) The acute oral toxicity, repellency, and hazard potential of 998 chemicals to one or more species of wild and domestic birds. Archives of Environmental Contamination and Toxicology 12, 355-382.
77. Sherburne, J.A. (1972) Effect of seasonal changes in the abundance and chemistry of the fleshy fruits of northeastern woody shrubs on patterns of exploitation by frugivorous birds. PhD thesis, Cornell University, Ithaca, New York.
78. Singaravelan, N., Ne'eman, G., Inbar, M. and Izhaki, I. (2005) Feeding responses of freeflying honeybees to secondary compounds mimicking floral nectar. Journal of Chemical Ecology 31, 2791-2804.
79. Singaravelan, N., Inbar, M., Ne'eman, G., Distl, M., Wink, M. and Izhaki, I. (2006) The effects of nectar-nicotine on colony fitness of caged honeybees. Journal of Chemical Ecology 32, 49-58.
80. Stamp, N. (2003a) Out of the quagmire of plant defence hypotheses. Quarterly Review of Biology 78, 23-55.
81. Stamp, N. (2003b) Theory of plant defensive level: example of process and pitfalls in development of ecological theory. Oikos 102, 672-678.
82. Stanley, M.C. and Lill, A. (2001) Response of silvereyes (Zosterops lateralis) to dietary tannins: the paradox of secondary metabolites in ripe fruit. Australian Journal of Zoology 49, 633-640.
83. Struempf, H.M. and Martínez del Rio, C. (1999) Amygdalin, a cyanogenic glycoside in ripe fruit, does not deter consumption by cedar waxwings. Auk 116, 749-758.
84. Sukrasno, N. and Yeoman, M.M. (1993) Phenylpropanoid metabolism during growth and development of Capsicum frutescens fruits. Phytochemistry 32, 839-844.
85. Suzuki, T. and Iwai, K. (1984) Constituents of red pepper species: chemistry, biochemistry, pharmacology, and food science of the pungent principle of Capsicum species. In: Brossi, A. (ed.) The Alkaloids: Chemistry and Pharmacology. Academic Press, Orlando, Florida, pp. 227-299.
86. Tadmor-Melamed, H., Markman, S., Arieli, A., Distl, M., Wink, M. and Izhaki, I. (2004) Limited ability of Palestine sunbirds (Nectarinia osea) to cope with pyridine alkaloids in nectar of tree tobacco (Nicotiana glauca). Functional Ecology 18, 844-850.
87. Tang, A.M.C., Corlett, R.T. and Hyde, K.D. (2005) The persistence of ripe fleshy fruits in the presence and absence of frugivores. Oecologia 142, 232-237.
88. Tewksbury, J.J. (2002) Fruits, frugivores and the evolutionary arms race. New Phytologist 156, 137-139.
89. Tewksbury, J.J. and Nabhan, G.P. (2001) Directed deterrence by capsaicin in chillies. Nature 412, 403-404.
90. Tewksbury, J.J., Nabhan, G.P., Norman, D.M., Suzan, H., Toxill, J. and Donovan, J. (1999) In situ conservation of wild chiles and their biotic associates. Conservation Biology 13, 98-107.
91. Tewksbury, J.J., Manchego, C., Haak, D. and Levey, D.J. (2006) Where did the chili get its spice? Biogeography of capsaicinoid production in ancestral wild chili species. Journal of Chemical Ecology 32, 547-564.
92. Thompson, J.N. and Willson, M.F. (1979) Evolution of temperate fruit-bird interactions: phenological strategies. Evolution 33, 973-982.
93. Thomson, R.H. (1987) Naturally Occurring Quinines. III. Recent Advances. Chapman and Hall, London.
94. Thomson, R.H. (1997) Naturally Occurring Quinines. IV. Recent Advances. Blackie Academic and Professional, Chapman and Hall, London.
95. Tsahar, E., Friedman, J. and Izhaki, I. (2002) Impact of fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp. Oikos 99, 290-299.
96. Tsahar, E., Friedman, J. and Izhaki, I. (2003) Secondary metabolite emodin increases food assimilation efficiency of yellow-vented bulbuls (Pycnonotus xanthopygos). Auk 120, 411-417.
97. Tsang, A.C.W. and Corlett, R.T. (2005) Reproductive biology of the Ilex species (Aquifoliaceae) in Hong Kong, China. Canadian Journal of Botany 83, 1645-1654.
98. Wagner, K.K. and Nolte, D.L. (2000) Evaluation of Hot Sauce® as a repellent for forest animals. Wildlife Society Bulletin 28, 76-83.
99. Wahaj, S.A., Levey, D.J., Sanders, A.K. and Cipollini, M.L. (1998) Control of gut retention time by secondary metabolites in ripe Solanum fruits. Ecology 79, 2309-2319.
100. Walsh, B.M. and Hoot, S.B. (2001) Phylogenetic relationships of Capsicum (Solanaceae) using DNA sequences from two noncoding regions: the chloroplast atpB-rbcL spacer region and nuclear waxy introns. International Journal of Plant Sciences 162, 1409-1418.
101. Wang, H.H. (1993) Antitrichomonal action of emodin in mice. Journal of Ethnopharmacology 40, 111-116.
102. Wang, H.H. and Chung, J.G. (1997) Emodin-induced inhibition of growth and DNA damage in the Heliobacter pylori. Current Microbiology 35, 262-266.
103. Wells, J.M., Cole, R.J. and Kirksey, J.W. (1975) Emodin, a toxic metabolite of Aspergillus wentii isolated from weevil-damaged chestnuts. Applied Microbiology 30, 26-28.
104. Whittaker, R.H. and Feeny, P.P. (1971) Allelochemics: chemical interactions between species. Science 171, 757-770.
105. Wink, M. (1998) Modes of action of alkaloids. In: Roberts, M.F. and Wink, M. (eds) Alkaloids. Biochemistry, Ecology, and Medicinal Applications. Plenum Press, New York, pp. 301-326.
106. Wink, M. and Schimmer, O. (1999) Modes of action of defensive secondary metabolites. In: Wink, M. (ed.) Function of Plant Secondary Metabolites and their Exploitation in Biotechnology. Academic Press, Sheffield, UK, pp. 1-16.
107. Witmer, M.C. (2001) Nutritional interactions and fruit removal: springtime consumption of Viburnum opulus fruits by cedar waxwings. Ecology 82, 3120-3130.
108. Yang, Y.C., Lim, M.Y. and Lee, H.S. (2003) Emodin isolated from Cassia obtusifolia (Leguminosae) seed shows larvicidal activity against three mosquito species. Journal of Agricultural and Food Chemistry 51, 7629-7631.
109. Zeyrek, F.Y. (2005) In vitro activity of capsaicin against Helicobacter pylori. Annals of Microbiology 55, 125-127.