Summary
Fruits that are green upon ripening (“green-ripe”) tend to be dispersed by a limited range of frugivores, whereas those that are brightly colored (“bright-ripe”) are dispersed by a wide range of birds and mammals. Because green fruits are probably less conspicuous than other colors of fruits, their pigmentation cannot be attributed to the attraction of seed dispersers. Instead, we hypothesize that a major benefit of green pigmentation is the ability to photosynthesize when ripe. Photosynthesis by fruits may lower their costs of production, and could result in fruits with greater nutrient reward. We present data on physical, chemical, and photosynthetic characteristics of ripe fleshy fruit of variable colors for 28 plant species at the La Selva Biological Station, Costa Rica. In addition to color and morphological characteristics of pulp and seeds, we report soluble solids content (refractive index), and photosynthetic/respiratory carbon-dioxide balance of ripe fruits. Carbon balance was much more dependent upon ambient light levels in green-ripe fruits than in bright-ripe fruit. In particular, data from light response curves indicated that green-ripe fruits may go into positive carbon balance at high light levels (above 300 μmol/m2/s). Rather than finding a positive relationship between soluble solids content and green fruit, as we predicted based on photosynthetic capacity, our data indicate that greater respiration rates of green-ripe fruits may result in carbon losses at low light levels. Our results were consistent with previously described morphological differences between the two color classes, with green-ripe fruits displaying significantly greater wet pulp mass, wet seed mass, and total fruit mass. Our data suggest that photosynthesis due to the retention of chlorophyll in ripe fleshy fruit may offset respiratory costs for plants with large or otherwise costly fruit, but this advantage should be evident only under high-light conditions.
Similar content being viewed by others
References
Bazzaz FA, Carlson RW, Harper JL (1979) Contribution to reproductive effort by photosynthesis of flowers and fruits. Nature 279: 554–555
Bjorkman O, Holmgren P (1963) Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol Plant 16: 889–913
Blanke MM, Lenz F (1989) Fruit photosynthesis. Plant Cell Environ 12: 31–46
Bruinisma J, Knegt E, Varga A (1975) The role of growth-regulating substances in fruit ripening. In: Ulrich R (ed) Facteurs et Regulation de la Maturation des Fruits. Centre National de la Recherche Scientifique. Anatole, France, pp 193–200
Chapin FS, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21: 423–447
Charles-Dominique P, Atramentowicz M, Charles-Dominique M, Gerard H, Hladick A, Hladik CM, Provost MF (1981) Les mammiferes frugivores arboricoles nocturnes d'une foret guyanaise: interrelations plantes-animaux. Rev Ecol (Terre Vie) 35: 341–435
Chazdon RL, Fetcher N (1984a) Light environments of tropical forests. In: Medina EA, Mooney HA, Vasquez-Yanes C (eds) Physiological ecology of plants of the wet tropics. Dr W. Junk, The Hague, Netherlands, pp 27–36
Chazdon RL, Fetcher N (1984b) Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. J Ecol 72: 553–564
Crane JC (1964) Growth substances in fruit setting and development. Ann Rev Plant Physiol 15: 303–326
DeBussche M, Cortez J, Rimbault I (1987) Variation in fleshy fruit composition in the Mediterranean region: the importance of ripening season, life-form, fruit type and geographical distribution. Oikos 49: 244–252
Dennis C (1983) Soft fruits. In: Dennis C (ed) Post-harvest Pathology of Fruits and Vegetables. Academic Press, London, England, pp 23–42
Denslow JS, Schultz JC, Vitousek P, Strain BR (1990) Growth responses of tropical shrubs to treefall gap environments. Ecology 71: 165–179
Ehleringer J, Bjorkman O, Mooney HA (1976) Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science 192: 376–377
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33: 317–345
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90
Fleming TH (1979) Do tropical frugivores compete for food? Am Zool 19: 1157–1172
Fleming TH, Breitwisch R, Whitesides GH (1987) Patterns of tropical vertebrate diversity. Ann Rev Ecol Syst 18: 91–109
Gautier-Hion A, Duplantier J-M, Quris R, Feer F, Sourd C, Decoux JP, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay J-M (1985) Fruit characters as a basis of fruit choice in a tropical forest community. Oecologia 65: 324–337
Haig D, Westoby M (1988) On limits to seed production. Am Nat 131: 757–759
Harper JL (1989) The value of a leaf. Oecologia 80: 53–58
Hazelton PK, Robel RJ (1984) Preferences and influence of paired food items on energy intake of American Robins and Gray Catbirds. J Wildl Manage 48: 198–202
Herrera CM (1985) Determinants of plant-animal coevolution: the case for mutualistic dispersal of seeds by vertebrates. Oikos 44: 132–141
Herrera CM (1987) Vertebrate-dispersed plants of the Iberian peninsula: a study of fruit characteristics. Ecol Monogr 57: 305–331
Herrera CM (1988) The fruiting ecology of Osyris quadripartita: individual variation and evolutionary potential. Ecology 69: 233–249
Horvitz C, Schemske DW (1988) A test of the pollinator limitation hypothesis for a neotropical shrub. Ecology 69: 200–206
Izhaki I, Safriel UN (1985) Why do fleshy-fruited plants of the Mediterranean scrub intercept fall- but not spring-passage of seed-dispersing birds? Oecologia 67: 40–43
Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219: 187–189
Johnson RA, Willson MF, Thompson JN, Bertin RI (1985) Nutritional values of wild fruits and consumption by migrant frugivorous birds. Ecology 66: 819–827
Jurik TW (1985) Differential costs of sexual and vegetative reproduction in wild strawberry populations. Oecologia 66: 394–403
Knight RS, Siegfried WR (1983) Inter-relationships between type, size and colour of fruits and dispersal in Southern African trees. Oecologia 56: 405–412
Lambert F (1989) Fig-eating by birds in a Malaysian lowland rain forest. J Trop Ecol 5: 401–412
Levey DJ (1987) Sugar-tasting ability and fruit selection in tropical fruit-eating birds. Auk 104: 173–179
Levey DJ, Moermond TC, Denslow JS (1984) Fruit choice in neotropical birds: the effect of distance between fruits on preference patterns. Ecology 65: 844–850
Mooney HA, Ehleringer J, Berry JA (1976) High photosynthetic capacity of a winter annual in Death Valley. Science 194: 322–323
Mooney HA, Field C, Vasquez-Yanes C (1984) Photosynthetic characteristics of wet tropical forest plants. In: Medina E, Mooney HA, Vasquez-Yanes C (eds) Physiological ecology of plants of the wet tropics. Dr W. Junk, The Hague, Netherlands. pp 113–128
Palmeirin JM, Gorchov DL, Stoleson S (1989) Trophic structure of a neotropical frugivore community: is there competition between birds ad bats? Oecologia 79: 403–413
Pijl van der L (1969) Principles of dispersal in higher plants. Springer-Verlag, Berlin
Reekie EG, Bazzaz FA (1987) Reproductive effort in plants: 1. Carbon allocation to reproduction. Am Nat 129: 876–896
SAS Institute, Inc. (1982) Statistics. SAS Institute, Inc., Cary, North Carolina
Snodderly DM (1979) Visual discriminations encountered in food foraging by a neotropical primate: implications for the evolution of color vision. pp. 237–280. In: Burtt EH Jr (ed) The behavioral significance of color. Garland STPM Press, New York, New York, pp 237–280
Stiles EW (1980) Patterns of fruit presentation and seed dispersal in bird-disseminated woody plants in the eastern deciduous forest. Am Nat 116: 670–687
Stiles EW (1982) Fruit flags: two hypotheses. Am Nat 120: 500–509
Walker D (1989) The measurement of rate of photosynthesis as a function of photon flux density and the significance and implication of these measurements. In: Barber J, Malkin R (eds) Techniques and new developments in photosynthesis research. Plenum Press, New York. pp 331–340
Wheelwright NT (1985) Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66: 808–818
Wheelwright NT, Janson CH (1985) Colors of fruit displays of bird-dispersed plants in two tropical forests. Am Nat 126: 777–799
Wheelwright NT, Orians GH (1982) Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on coevolution. Am Nat 119: 402–413
White DW, Stiles EW (1985) The use of refractometry to estimate nutrient reward of vertebrate-dispersed fruits. Ecology 66: 303–307
Williams K, Koch GW, Mooney HA (1985) The carbon balance of flowers of Diplacus aurantiacus (Scrophulariaceae). Oecologia 66: 530–535
Willson MF (1983) Plant Reproductive Ecology. Wiley, New York
Willson MF, Irvine AK, Walsh NG (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21: 133–147
Willson MF, Graff DA, Whelan CJ (1990) Color preferences of frugivorous birds in relation to the colors of fleshy fruits. Condor 92: 545–555
Willson MF, Thompson JN (1982) Phenology of color in birddispersed fruits, or why some fruits are red when they are “green”. Can J Bot 60: 701–713
Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136: 790–809
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cipollini, M.L., Levey, D.J. Why some fruits are green when they are ripe: carbon balance in fleshy fruits. Oecologia 88, 371–377 (1991). https://doi.org/10.1007/BF00317581
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00317581