title: How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales.
abstract: The colors of fleshy fruits are considered to be a signal to seed-dispersing animals, but their diversity remains poorly understood. Using an avian color space to derive a sensory morphospace for fruit color, we tested four hypotheses of fruit color diversity: fruit colors occupy a limited area of the color space; they are less diverse than flower colors; fruit colors within localities are similar to each other; and fruit color diversity reflects phylogeny. The global fruit color diversity of 948 primarily bird-dispersed plant species and the color diversity of localities were compared with null models of random, unconstrained evolution of fruit color. Fruit color diversity was further compared with the diversity of 1300 flower colors. Tests of phylogenetic effects on fruit color were used to assess the degree of correspondence with phylogeny. Global and local fruit color diversity was limited compared with null models and fruits have achieved only half the color diversity of flowers. Interestingly, we found little indication of phylogenetic conservatism. Constraints resulting from the chemical properties of pigments probably limit global fruit and flower color diversity. Different types of selection on fruits and flowers may further explain the smaller color diversity of fruits.
authors: Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, 79104, Freiburg, Germany.|Department of Ecology and Evolutionary Biology, Yale University, PO Box 208105, New Haven, CT, 06520, USA.
authors: Kalliope E
authors: KE
authors: Stournaras
authors: Department of Ecology and Evolutionary Biology, Yale University, PO Box 208105, New Haven, CT, 06520, USA.
authors: Eugenia
authors: E
authors: Lo
authors: Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325, Frankfurt/Main, Germany.|Department of Biological Sciences, Goethe Universität, Max-von-Laue-Straße 9, 60438, Frankfurt/Main, Germany.
authors: Katrin
authors: K
authors: Böhning-Gaese
authors: Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna km 16, Ilhéus, Bahia, CEP 45662-900, Brazil.
authors: Eliana
authors: E
authors: Cazetta
authors: Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325, Frankfurt/Main, Germany.
authors: D
authors: D
authors: Matthias Dehling
authors: Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325, Frankfurt/Main, Germany.
authors: Matthias
authors: M
authors: Schleuning
authors: Museum of Comparative Zoology and Department of Organismic & Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.
authors: Mary Caswell
authors: MC
authors: Stoddard
authors: Department of Ecology and Evolutionary Biology, Yale University, PO Box 208105, New Haven, CT, 06520, USA.
authors: Michael J
authors: MJ
authors: Donoghue
authors: Department of Ecology and Evolutionary Biology, Yale University, PO Box 208105, New Haven, CT, 06520, USA.
authors: Richard O
authors: RO
authors: Prum
authors: Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, 79104, Freiburg, Germany.
authors: H
authors: H
authors: Martin Schaefer
mesh_terms: D000818:Animals; D001717:Birds; D003116:Color; D035264:Flowers / Q000502:physiology; D005638:Fruit / Q000145:classification / Q000502:physiology*; D010802:Phylogeny; D010858:Pigmentation / Q000502:physiology*
references: APG 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.
references: Arnold SEJ, Faruq S, Savolainen V, McOwan PW, Chittka L. 2010. FReD: the floral reflectance database - a web portal for analyses of flower colour. PLoS ONE 5: 1-9.
references: Blomberg SP, Garland T Jr., Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717-745.
references: Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17: 341-346.
references: Bowmaker JK, Heath LA, Wilkie SE, Hunt DM. 1997. Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Research 37: 2183-2194.
references: Burns KC, Cazetta E, Galetti M, Valido A, Schaefer HM. 2009. Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits? Oecologia 159: 337-343.
references: Cantino PD, Doyle JA, Graham SW, Judd WS, Olmstead RG, Soltis DE, Soltis PS, Donoghue MJ. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56: 822-846.
references: Catoni C, Schaefer HM, Peters A. 2008. Fruit for health: the effect of flavonoids on humoral immune response and food selection in a frugivorous bird. Functional Ecology 22: 649-654.
references: Cazzonelli CI. 2011. Carotenoids in nature: insights from plants and beyond. Functional Plant Biology 38: 833-847.
references: Chittka L, Schürkens S. 2001. Successful invasion of a floral market. Nature 411: 653.
references: Chittka L, Thomson JD, Waser NM. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86: 361-377.
references: Donatti CI, Galetti M, Pizo MA, Guimarães PR, Jordano P. 2007. Living in the land of ghosts: fruit traits and the importance of large mammals as seed dispersers in the Pantanal. In: Dennis AJ, Schupp EW, Green RA, Westcott DA, eds. Seed dispersal: theory and its implications in a changing world. Wallingford, UK: Commonwealth Agricultural Bureau International, 104-123.
references: Endler JA, Mielke PW Jr. 2005. Comparing entire colour patterns as birds see them. Biological Journal of the Linnean Society 86: 405-431.
references: Endler JA, Westcott DA, Madden JR, Robson T. 2005. Animal visual signals and the evolution of color patterns: sensory processing illuminates signal evolution. Evolution 59: 1795-1818.
references: Fischer KE, Chapman CA. 1993. Frugivores and fruit syndromes: differences in patterns at the genus and species level. Oikos 66: 472-482.
references: Flörchinger M, Braun J, Böhning-Gaese K, Schaefer HM. 2010. Fruit size, crop mass, and plant height explain differential fruit choice of primates and birds. Oecologia 164: 151-161.
references: Friis EM, Pedersen KR, Crane PR. 2006. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232: 251-293.
references: Glover BJ, Whitney HM. 2010. Structural colour and iridescence in plants: the poorly studied relations of pigment colour. Annals of Botany 105: 505-511.
references: Goldsmith TH. 1990. Optimization, constraint, and history in the evolution of eyes. Quarterly Review of Biology 65: 281-322.
references: Goodwin TW. 1976. Distribution of carotenoids. In: Goodwin TW, ed. Chemistry and biochemistry of plant pigments. New York, NY, USA: Academic Press, 225-261.
references: Gould KS. 2004. Nature's Swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine & Biotechnology 2004: 314-320.
references: Gumbert A, Kunze J, Chittka L. 1999. Floral colour diversity in plant communities, bee colour space and a null model. Proceedings of the Royal Society B, Biological Sciences 266: 1711-1716.
references: Harms KE, Wright SJ, Calderón O, Hernández A, Herre EA. 2000. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404: 493-495.
references: Hart NS, Hunt DM. 2007. Avian visual pigments: characteristics, spectral tuning, and evolution. American Naturalist 169: 7-26.
references: Herrera CM. 1984. Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65: 609-617.
references: Herrera CM. 1996. Floral traits and plant adaptation to insect pollinators: a devil's advocate approach. In: Lloyd DG, Barrett SCH, eds. Floral biology. New York, NY, USA: Chapman and Hall, 65-87.
references: Herrera CM. 2005. Plant generalization on pollinators: species property or local phenomenon? American Journal of Botany 92: 13-20.
references: Hormaetxe K, Hernández A, Becerril JM, Gercía-Plazaola JI. 2004. Role of red carotenoids in photoprotection during winter acclimation in Buxus sempervirens leaves. Plant Biology 6: 325-332.
references: Janson CH. 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219: 187-189.
references: Jordano P. 2000. Fruits and frugivory. In: Fenner M, ed. Seeds: the ecology of regeneration in plant communities. Wallingford, UK: CAB International, 125-165.
references: Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
references: Lee DW. 1991. Ultrastructural basis and function of iridescent blue colour of fruits in Elaeocarpus. Nature 349: 260-262.
references: Lee DW, Taylor GT, Irvine AK. 2000. Structural fruit coloration in Delarbrea michieana (Araliaceae). International Journal of Plant Sciences 161: 297-300.
references: Lomáscolo SB, Levey DJ, Kimball RT, Bolker BM, Alborn HT. 2010. Dispersers shape fruit diversity in Ficus (Moraceae). Proceedings of the National Academy of Sciences 107: 14668-14672.
references: Lomáscolo SB, Schaefer HM. 2010. Signal convergence in fruits: a result of selection by frugivores? Journal of Evolutionary Biology 23: 614-624.
references: McGhee GR. 1999. Theoretical morphology: the concept and its applications. New York, NY, USA: Columbia University Press.
references: McGhee GR. 2007. The geometry of evolution: adaptive landscapes and theoretical morphospaces. New York, NY, USA: Cambridge University Press.
references: Noë R, Hammerstein P. 1994. Biological markets: supply and demand determine the effect and mating mutualism of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology 35: 1-11.
references: Osorio D, Vorobyev M. 2008. A review of the evolution of animal colour vision and visual communication signals. Vision Research 48: 2042-2051.
references: Patterson BD, Stotz DF, Solari S, Fitzpatrick JW, Pacheco V. 1998. Contrasting patterns of elevational zonation for birds and mammals in the Andes of southeastern Peru. Journal of Biogeography 25: 593-607.
references: Russo SE, Augspurger CK. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7: 1058-1067.
references: Sanders HL. 1968. Marine benthic diversity: a comparative study. American Naturalist 102: 243-282.
references: Schaefer HM, Rentzsch M, Breuer M. 2008. Anthocyanins reduce fungal growth in fruits. Natural Product Communications 3: 1267-1272.
references: Schaefer HM, Ruxton GD. 2011. Plant-animal communication. New York, NY, USA: Oxford University Press.
references: Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology & Evolution 19: 577-584.
references: Schaefer HM, Schaefer V, Vorobyev M. 2007. Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals? American Naturalist 169: 159-169.
references: Schaefer HM, Schmidt V. 2004. Detectability and content as opposing signal characteristics in fruits. Proceedings of the Royal Society B, Biological Sciences 271: 370-373.
references: Schmidt V, Schaefer HM, Winkler H. 2004. Conspicuousness, not colour as foraging cue in plant-animal signalling. Oikos 106: 551-557.
references: Smillie RM, Hetherington SE. 1999. Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica 36: 451-463.
references: Smith SA, Beaulieu JM, Donoghue MJ. 2010. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences, USA 107: 5897-5902.
references: Snow DW. 1971. Evolutionary aspects of fruit-eating by birds. Ibis 113: 194-202.
references: Stoddard MC, Prum RO. 2008. Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. American Naturalist 171: 755-776.
references: Stoddard MC, Prum RO. 2011. How colorful are birds? Evolution of the avian plumage color gamut. Behavioral Ecology 22: 1042-1052.
references: Stoddard MC, Stevens M. 2011. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65: 2004-2013.
references: Strauss SY, Whittall JB. 2006. Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH, eds. Ecology and evolution of flowers. New York, NY, USA: Oxford University Press, 120-135.
references: Sumner P, Mollon JD. 2003. Colors of primate pelage and skin: objective assessment of conspicuousness. American Journal of Primatology 59: 67-91.
references: Valido A, Schaefer HM, Jordano P. 2011. Colour, design and reward: phenotypic integration of fleshy fruit displays. Journal of Evolutionary Biology 24: 751-760.
references: Vignolini S, Rudall PJ, Rowland AV, Reed A, Moyroud E, Faden RB, Baumberg JJ, Glover BJ, Steiner U. 2012. Pointillist structural color in Pollia fruit. Proceedings of the National Academy of Sciences, USA 109: 15712-15715.
references: Vorobyev M. 2003. Coloured oil droplets enhance colour discrimination. Proceedings of the Royal Society B, Biological Sciences 270: 1255-1261.
references: Vorobyev M, Osorio D. 1998. Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society B, Biological Sciences 265: 351-358.
references: Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. 1996. Generalization in pollination systems, and why it matters. Ecology 77: 1043-1060.
references: Webb CO, Ackerly DD, Kembel SW. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098-2100.
references: Webb CO, Donoghue MJ. 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5: 181-183.
references: Wheelwright NT. 1988. Fruit-eating birds and bird-dispersed plants in the tropics and temperate zone. Trends in Ecology & Evolution 3: 270-274.
references: Wheelwright NT, Janson CH. 1985. Colors of fruit displays of bird-dispersed plants in two tropical forests. American Naturalist 126: 777-799.
references: Whitney KD. 2009. Comparative evolution of flower and fruit morphology. Proceedings of the Royal Society B, Biological Sciences 276: 2941-2947.
references: Willson MF, Irvine AK, Walsh NG. 1989. Geographic comparisons in some Australian vertebrate dispersal syndromes and New Zealand plant communities, with geographic comparisons. Biotropica 21: 133-147.
references: Willson MF, Whelan CJ. 1990. The evolution of fruit color in fleshy-fruited plants. American Naturalist 136: 790-809.
references: Young AJ. 1991. The photoprotective role of carotenoids in higher plants. Physiologia Plantarum 83: 702-708.