Skip to main content
SpringerLink
Log in
Book cover

Co-Evolution of Secondary Metabolites pp 1–23Cite as

Fruit Scent: Biochemistry, Ecological Function, and Evolution

  • Living reference work entry
  • First Online:

Part of the book series: Reference Series in Phytochemistry ((RSP))

Abstract

Fruit scent plays an important role in human preference and has thus been studied primarily in the context of agricultural science. In wild species, fruit scent has long been speculated to play a role in mediating the mutualistic interaction between plants and fruit-eating animals that disperse their seeds. Yet until recently, empirical studies addressing this hypothesis have been all but absent. Studies in the past decade emphasized the ecological role of fruit scent as an animal attractant, as well as its evolution as a ripeness signal. But data are still limited and many questions remain open. This chapter summarizes recent developments in the study of the chemical ecology and evolution of wild fruit scent. It explores the chemistry and biochemistry of fruit scent, its use by various important seed dispersal vectors, its evolution, and other functions it may fulfill. We end with recommendation for future studies, in the hope that the next decade will be at least as fruitful as the previous one.

This is a preview of subscription content, log in via an institution.

Notes

  1. 1.

    Including mature fig syconia, which are functionally equivalent.

References

  1. Crozier A, Yokota T, Jaganath IB, Marks SC, Saltmarsh M, Clifford MN (2006) Secondary metabolites in fruits, vegetables, beverages and other plant based dietary components. In: Crozier A, Clifford MN, Ashihara H (eds) Plant secondary metabolites. Blackwell, Oxford, UK, pp 208–302

    Chapter  Google Scholar 

  2. Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372

    Article  CAS  PubMed  Google Scholar 

  3. Cipollini ML (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440

    Article  Google Scholar 

  4. Ehrlén J, Eriksson O (1993) Toxicity in fleshy fruits: a non-adaptive trait? Oikos 66:107–113

    Article  Google Scholar 

  5. Eriksson O, Ehrlén J (1998) Secondary metabolites in fleshy fruits: are adaptive explanations needed? Am Nat 152:905–907

    Article  CAS  PubMed  Google Scholar 

  6. Cipollini ML, Paulk E, Mink K, Vaughn K, Fischer T (2004) Defense tradeoffs in fleshy fruits: effects of resource variation on growth, reproduction, and fruit secondary chemistry in Solanum carolinense. J Chem Ecol 30:1–17

    Article  CAS  PubMed  Google Scholar 

  7. Whitehead SR, Bowers MD (2013) Evidence for the adaptive significance of secondary compounds in vertebrate-dispersed fruits. Am Nat 182:563–577

    Article  PubMed  Google Scholar 

  8. Whitehead SR, Bowers MD (2014) Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from piper. Funct Ecol 28:1094–1106

    Article  Google Scholar 

  9. Whitehead SR, Obando Quesada MF, Bowers MD (2015) Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats. Oikos 125:927–937

    Article  Google Scholar 

  10. Whitehead SR, Tiramani J, Bowers MD (2015) Iridoid glycosides from fruits reduce the growth of fungi associated with fruit rot. J Plant Ecol 9:357–366

    Article  Google Scholar 

  11. Izhaki I (2002) Emodin – a secondary metabolite with multiple ecological functions in higher plants. New Phytol 155:205–217

    Article  CAS  Google Scholar 

  12. Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633

    Article  CAS  PubMed  Google Scholar 

  13. Farmer EE (2014) Leaf defence. Oxford University Press, Oxford

    Book  Google Scholar 

  14. Rodríguez A, Alquézar B, Peña L (2013) Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol 197:36–48

    Article  PubMed  CAS  Google Scholar 

  15. Nevo O, Valenta K (2018) The ecology and evolution of fruit odor: implications for primate seed dispersal. Int J Primatol 39:338–355

    Article  Google Scholar 

  16. Nevo O, Valenta K, Tevlin AG, Omeja P, Styler SA, Jackson DJ, Chapman CA, Ayasse M (2017) Fruit defence syndromes: the independent evolution of mechanical and chemical defences. Evol Ecol 31:913–923

    Article  Google Scholar 

  17. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485

    Article  CAS  PubMed  Google Scholar 

  18. Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54:712–732

    Article  CAS  PubMed  Google Scholar 

  19. Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815–819

    Article  CAS  PubMed  Google Scholar 

  20. Valenta K, Nevo O, Martel C, Chapman CA (2017) Plant attractants: integrating insights from pollination and seed dispersal ecology. Evol Ecol 31:249–267

    Article  Google Scholar 

  21. Fischer KE, Chapman CA (1993) Frugivores and fruit syndromes: differences in patterns at the genus and species level. Oikos 66:472–482

    Article  Google Scholar 

  22. Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. Am Nat 145:163–191

    Article  Google Scholar 

  23. Schaefer HM, Ruxton GD (2011) Animal-plant communication. Oxford University Press, Oxford

    Book  Google Scholar 

  24. Lomáscolo SB, Schaefer HM (2010) Signal convergence in fruits: a result of selection by frugivores? J Evol Biol 23:614–624

    Article  PubMed  Google Scholar 

  25. Lomáscolo SB, Levey DJ, Kimball RT, Bolker BM, Alborn HT (2010) Dispersers shape fruit diversity in Ficus (Moraceae). Proc Natl Acad Sci 107:14668–14672

    Article  PubMed  PubMed Central  Google Scholar 

  26. Schaefer HM, Valido A, Jordano P (2014) Birds see the true colours of fruits to live off the fat of the land. Proc R Soc B Biol Sci 281:20132516–20132516

    Article  Google Scholar 

  27. Tholl D, Boland W, Hansel A, Loreto F, Röse USR, Schnitzler J-P (2006) Practical approaches to plant volatile analysis. Plant J 45:540–560

    Article  CAS  PubMed  Google Scholar 

  28. Kalko EKV, Ayasse M (2009) Study and analysis of odor involved in the behavioral ecology of bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bat, 2nd edn. The Johns Hopkins University Press, Baltimore, pp 491–499

    Google Scholar 

  29. Howe HF, Westley LC (1986) Ecology of pollination and seed dispersal. In: Crawley MJ (ed) Plant ecology. Blackwell Scientific Publications, London, pp 185–215

    Google Scholar 

  30. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569

    Article  Google Scholar 

  31. Schiestl FP (2015) Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytol 206:571–577

    Article  PubMed  Google Scholar 

  32. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, pp 147–198

    Chapter  Google Scholar 

  33. Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949

    Article  PubMed  Google Scholar 

  34. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414

    Article  CAS  PubMed  Google Scholar 

  35. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hodgkison R, Ayasse M, Kalko EKV, Häberlein C, Schulz S, Mustapha WAW, Zubaid A, Kunz TH (2007) Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two species of Paleotropical bat-dispersed figs (Ficus hispida and Ficus scortechinii). J Chem Ecol 33:2097–2110

    Article  CAS  PubMed  Google Scholar 

  38. Hodgkison R, Ayasse M, Häberlein C, Schulz S, Zubaid A, Mustapha WAW, Kunz TH, Kalko EKV (2013) Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the New and Old World tropics. Funct Ecol 27:1075–1084

    Article  Google Scholar 

  39. Nevo O, Heymann EW, Schulz S, Ayasse M (2016) Fruit odor as a ripeness signal for seed-dispersing primates? A case study on four Neotropical plant species. J Chem Ecol 42:323–328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Borges RM, Bessière JM, Hossaert-McKey M (2008) The chemical ecology of seed dispersal in monoecious and dioecious figs. Funct Ecol 22:484–493

    Article  Google Scholar 

  41. Tholl D, Sohrabi R, Huh J-H, Lee S (2011) The biochemistry of homoterpenes – common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 72:1635–1646

    Article  CAS  PubMed  Google Scholar 

  42. Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites. Int J Plant Sci 164:S93–S102

    Article  CAS  Google Scholar 

  43. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci U S A 95:4126–4133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Fischbach MA, Clardy J (2007) One pathway, many products. Nat Chem Biol 3:353–355

    Article  CAS  PubMed  Google Scholar 

  45. Degenhardt J (2008) Ecological roles of vegetative terpene volatiles. In: Schaller A (ed) Induced plant resistance to herbivory. Springer Netherlands, Dordrecht, pp 433–442

    Chapter  Google Scholar 

  46. Nevo O, Garri RO, Hernandez Salazar LT, Schulz S, Heymann EW, Ayasse M, Laska M (2015) Chemical recognition of fruit ripeness in spider monkeys (Ateles geoffroyi). Sci Rep 5:14895–14895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120

    Article  Google Scholar 

  48. Dudareva N, Negre F, Nagegowda D, Orlova I (2006) Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  49. Dudareva N, Pichersky E (2006) Floral scent metabolic pathways: their regulation and evolution. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, pp 55–78

    Chapter  Google Scholar 

  50. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280

    Article  CAS  PubMed  Google Scholar 

  51. Nevo O, Razafimandimby D, Jeffrey JAJ, Schulz S, Ayasse M (2018) Fruit scent as an evolved signal to primate seed dispersal. Sci Adv 4:eaat4871

    Article  PubMed  PubMed Central  Google Scholar 

  52. Flores F, El Yahyaoui F, de Billerbeck G, Romojaro F, Latché A, Bouzayen M, Pech J-C, Ambid C (2002) Role of ethylene in the biosynthetic pathway of aliphatic ester aroma volatiles in Charentais Cantaloupe melons. J Exp Bot 53:201–206

    Article  CAS  PubMed  Google Scholar 

  53. Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FWA, Bouwmeester HJ, Aharoni A (2004) Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 135:1865–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Peris JE, Rodríguez A, Peña L, Fedriani JM (2017) Fungal infestation boosts fruit aroma and fruit removal by mammals and birds. Sci Rep 7:5646–5646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Dudley R (2002) Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover. Addiction 97:381–388

    Article  PubMed  Google Scholar 

  56. Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656

    Article  PubMed  Google Scholar 

  57. Widhalm JR, Dudareva N (2015) A familiar ring to it: biosynthesis of plant benzoic acids. Mol Plant 8:83–97

    Article  CAS  PubMed  Google Scholar 

  58. Qualley AV, Dudareva N (2008) Aromatic volatiles and their involvement in plant defense. In: Schaller A (ed) Induced plant resistance to herbivory. Springer Netherlands, Dordrecht, pp 409–432

    Chapter  Google Scholar 

  59. Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62:113–123

    Article  CAS  PubMed  Google Scholar 

  60. Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43:439–463

    Article  CAS  Google Scholar 

  61. Brown MJ (1997) Durio, a bibliographic review. Bioversity International, New Delhi

    Google Scholar 

  62. Baldry J, Dougan J, Howard GE (1972) Volatile flavouring constituents of Durian. Phytochemistry 11:2081–2084

    Article  CAS  Google Scholar 

  63. Moser R, Düvel D, Greve R (1980) Volatile constituents and fatty acid composition of lipids in Durio zibethinus. Phytochemistry 19:79–81

    Article  CAS  Google Scholar 

  64. Wong KC, Tie DY (1995) Volatile constituents of durian (Durio zibethinus Murr.). Flavour Fragr J 10:79–83

    Article  CAS  Google Scholar 

  65. Teh BT, Lim K, Yong CH, Ng CCY, Rao SR, Rajasegaran V, Lim WK, Ong CK, Chan K, Cheng VKY, Soh PS, Swarup S, Rozen SG, Nagarajan N, Tan P (2017) The draft genome of tropical fruit durian (Durio zibethinus). Nat Genet 49:1633–1641

    Article  CAS  PubMed  Google Scholar 

  66. Voo SS, Grimes HD, Lange BM (2012) Assessing the biosynthetic capabilities of secretory glands in Citrus peel. Plant Physiol 159:81–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Widhalm JR, Jaini R, Morgan JA, Dudareva N (2015) Rethinking how volatiles are released from plant cells. Trends Plant Sci 20:545–550

    Article  CAS  PubMed  Google Scholar 

  68. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32

    Article  CAS  PubMed  Google Scholar 

  69. Borges RM, Bessière J-M, Ranganathan Y (2013) Diel variation in fig volatiles across syconium development: making sense of scents. J Chem Ecol 39:630–642

    Article  CAS  PubMed  Google Scholar 

  70. Birtic S, Ginies C, Causse M, Renard CM, Page D (2009) Changes in volatiles and glycosides during fruit maturation of two contrasted tomato (Solanum lycopersicum) lines. J Agric Food Chem 57:591–598

    Article  CAS  PubMed  Google Scholar 

  71. Valenta K, Miller CN, Monckton SK, Melin AD, Lehman SM, Styler SA, Jackson DA, Chapman CA, Lawes MJ (2016) Fruit ripening signals and cues in a Madagascan dry forest: haptic indicators reliably indicate fruit ripeness to dichromatic lemurs. Evol Biol 43:344–355

    Article  Google Scholar 

  72. Sánchez F, Korine C, Steeghs M, Laarhoven L-J, Cristescu SM, Harren FJM, Dudley R, Pinshow B (2006) Ethanol and methanol as possible odor cues for Egyptian fruit bats (Rousettus aegyptiacus). J Chem Ecol 32:1289–1300

    Article  PubMed  CAS  Google Scholar 

  73. Borges RM (2015) Fruit and seed volatiles: multiple stage settings, actors and props in an evolutionary play. J Indian Inst Sci 95:93–104

    Google Scholar 

  74. Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Regul 26:143

    Article  CAS  Google Scholar 

  75. Chapman GW, Horvat RJ, Forbus WR (1991) Physical and chemical changes during the maturation of peaches (cv. Majestic). J Agric Food Chem 39:867–870

    Article  CAS  Google Scholar 

  76. Gómez E, Ledbetter CA (1997) Development of volatile compounds during fruit maturation: characterization of apricot and plum× apricot hybrids. J Sci Food Agric 74:541–546

    Article  Google Scholar 

  77. Supriyadi S, Suzuki M, Yoshida K, Muto T, Fujita A, Watanabe N (2002) Changes in the volatile compounds and in the chemical and physical properties of snake fruit (Salacca edulis Reinw) Cv. Pondoh during maturation. J Agric Food Chem 50:7627–7633

    Article  CAS  PubMed  Google Scholar 

  78. Nevo O, Heymann EW (2015) Led by the nose: olfaction in primate feeding ecology. Evol Anthropol 24:137–148

    Article  PubMed  PubMed Central  Google Scholar 

  79. Borges RM, Ranganathan Y, Krishnan A, Ghara M, Pramanik G (2011) When should fig fruit produce volatiles? Pattern in a ripening process. Acta Oecol 37:611–618

    Article  Google Scholar 

  80. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346

    Article  PubMed  CAS  Google Scholar 

  81. Silver SC, Ostro LE, Yeager CP, Horwich R (1998) Feeding ecology of the black howler monkey (Alouatta pigra) in northern Belize. Am J Primatol 45:263–279

    Article  CAS  PubMed  Google Scholar 

  82. Korine C, Kalko EKV (2005) Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behav Ecol Sociobiol 59:12–23

    Article  Google Scholar 

  83. van der Pijl L (1982) Principles of dispersal in higher plants, 3rd edn. Springer, Berlin

    Book  Google Scholar 

  84. Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219:187–189

    Article  CAS  PubMed  Google Scholar 

  85. Herrera CM (1985) Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44:132–141

    Article  Google Scholar 

  86. Herrera CM (1986) Vertebrate-dispersed plants: why they don’t behave the way they should. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal. Dr W. Junk Publishers, Dordrecht, pp 5–18

    Chapter  Google Scholar 

  87. Lomáscolo SB, Speranza P, Kimball RT (2008) Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia 156:783–796

    Article  PubMed  Google Scholar 

  88. Wang L-F, Cowled C (2015) Bats and viruses: a new frontier of emerging infectious diseases. Wiley, New York

    Book  Google Scholar 

  89. Muscarella R, Fleming TH (2007) The role of frugivorous bats in tropical forest succession. Biol Rev 82:573–590

    Article  PubMed  Google Scholar 

  90. Kries K, Barros MAS, Duytschaever G, Orkin JD, Janiak MC, Pessoa DMA, Melin AD (2018) Colour vision variation in leaf-nosed bats (Phyllostomidae): links to cave roosting and dietary specialization. Mol Ecol. https://doi.org/10.1111/mec.14818

    Article  PubMed  Google Scholar 

  91. Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21:149–156

    Article  PubMed  Google Scholar 

  92. von Helversen D, von Helversen O (1999) Acoustic guide in bat-pollinated flower. Nature 398:759–760

    Article  CAS  Google Scholar 

  93. Simon R, Holderied MW, Koch CU, von Helversen O (2011) Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators. Science 333:631–633

    Article  CAS  PubMed  Google Scholar 

  94. Schöner MG, Schöner CR, Simon R, Grafe TU, Puechmaille SJ, Ji LL, Kerth G (2015) Bats are acoustically attracted to mutualistic carnivorous plants. Curr Biol 25:1911–1916

    Article  PubMed  CAS  Google Scholar 

  95. Kalko EKV, Condon MA (1998) Echolocation, olfaction and fruit display: how bats find fruit of flagellichorus cucurbits. Funct Ecol 12:364–372

    Article  Google Scholar 

  96. Hayden S, Bekaert M, Goodbla A, Murphy WJ, Dávalos LM, Teeling EC (2014) A cluster of olfactory receptor genes linked to frugivory in bats. Mol Biol Evol 4:1–11

    Google Scholar 

  97. Gonzalez-Terrazas TP, Martel C, Milet-Pinheiro P, Ayasse M, Kalko EKV, Tschapka M (2016) Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar. R Soc Open Sci 3:160199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Kalko EKV, Herre EA, Handley CO Jr (1996) Relation of fig fruit characteristics to fruit-eating bats in the new and Old World tropics. J Biogeogr 23:565–576

    Article  Google Scholar 

  99. Kalko EKV, Condon M (1993) Bat-plant interactions: how frugivorous leaf-nosed bats find their food. Bat Res News 35:28

    Google Scholar 

  100. Rieger JF, Jakob EM (1988) The use of olfaction in food location by frugivorous bats. Biotropica 20:161–164

    Article  Google Scholar 

  101. Thies W, Kalko EKV, Schnitzler H-U (1998) The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav Ecol Sociobiol 42:397–409

    Article  Google Scholar 

  102. Laska M (1990) Olfactory sensitivity to food odor components in the short-tailed fruit bat, Carollia perspicillata (phyllostomatidae, chiroptera). J Comp Physiol A 166:395–399

    Article  Google Scholar 

  103. Sánchez F, Korine C, Pinshow B, Dudley R (2004) The possible roles of ethanol in the relationship between plants and frugivores: first experiments with Egyptian fruit bats. Integr Comp Biol 44:290–294

    Article  PubMed  Google Scholar 

  104. Chapman CA, Russo SE (2007) Linking behavioral ecology with forest community structure. In: Campbell CJ, Fuentes A, KC MK, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 510–525

    Google Scholar 

  105. Chapman CA, Dunham AE (2018) Primate seed dispersal and forest restoration: an african perspective for a brighter future. Int J Primatol. https://doi.org/10.1007/s10764-018-0049-3

    Article  Google Scholar 

  106. Culot L, Mann DJ, Muñoz Lazo FJJ, Huynen M-C, Heymann EW (2010) Tamarins and dung beetles: an efficient diplochorous dispersal system in the Peruvian Amazonia. Biotropica 43:84–92

    Article  Google Scholar 

  107. Nevo O (2016) The chemical ecology of primate seed dispersal. PhD thesis, Georg-August-Universität Göttingen

    Google Scholar 

  108. Culot L, Muñoz Lazo FJJ, Huynen M-C, Poncin P, Heymann EW (2010) Seasonal variation in seed dispersal by tamarins alters seed rain in a secondary rain forest. Int J Primatol 31:553–569

    Article  PubMed  PubMed Central  Google Scholar 

  109. Jacobs GH (2009) Evolution of colour vision in mammals. Philos Trans R Soc Lond Ser B Biol Sci 364:2957–2967

    Article  CAS  Google Scholar 

  110. Valenta K, Edwards M, Rafaliarison RR, Johnson SE, Holmes SM, Brown KA, Dominy NJ, Lehman SM, Parra EJ, Melin AD, Portugal S (2016) Visual ecology of true lemurs suggests a cathemeral origin for the primate cone opsin polymorphism. Funct Ecol 30:932–942

    Article  Google Scholar 

  111. Melin AD, Hiramatsu C, Parr NA, Matsushita Y, Kawamura S, Fedigan LM (2014) The behavioral ecology of color vision: considering fruit conspicuity, detection distance and dietary importance. Int J Primatol 35:258–287

    Article  Google Scholar 

  112. Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc Lond Ser B Biol Sci 356:229–283

    Article  CAS  Google Scholar 

  113. Melin AD, Chiou KL, Walco ER, Bergstrom ML, Kawamura S (2017) Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator). Proc Natl Acad Sci 114:201705957–201705957

    Article  CAS  Google Scholar 

  114. Valenta K, Nevo O, Chapman CA (2018) Primate fruit color: useful concept or alluring myth? Int J Primatol 39:321–337

    Article  Google Scholar 

  115. Nevo O, Valenta K, Razafimandimby D, Melin AD, Ayasse M, Chapman CA (2018) Frugivores and the evolution of fruit colour. Biol Lett 14(9):20180377

    Article  PubMed  PubMed Central  Google Scholar 

  116. Laska M, Seibt A, Weber A (2000) “Microsmatic” primates revisited: olfactory sensitivity in the squirrel monkey. Chem Senses 25:47–53

    Article  CAS  PubMed  Google Scholar 

  117. Melin AD, Nevo O, Shirasu M, Williamson R, Garrett E, Endo M, Sakurai K, Matsushita Y, Rothman J, Touhara K, Kawamura S. Accepted. Fruit scent and observer color vision shape food-selection strategies by wild capuchin monkeys. Nat Comm

    Google Scholar 

  118. Valenta K, Brown KA, Rafaliarison RR, Styler SA, Jackson D, Lehman SM, Chapman CA, Melin AD (2015) Sensory integration during foraging: the importance of fruit hardness, colour, and odour to brown lemurs. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-015-1998-6

    Article  Google Scholar 

  119. Howe HF (1986) Seed dispersal by fruit-eating birds and mammals. In: Murray DR (ed) Seed dispersal. Academic Press, San-Diego, pp 123–189

    Chapter  Google Scholar 

  120. Daniel Kissling W, Böhning-Gaese K, Jetz W (2009) The global distribution of frugivory in birds. Glob Ecol Biogeogr 18:150–162

    Article  Google Scholar 

  121. Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol 183:621–633

    Article  CAS  Google Scholar 

  122. Bennett ATD, Théry M (2007) Avian color vision and coloration: multidisciplinary evolutionary biology. Am Nat 169:S1–S6

    Article  Google Scholar 

  123. Ordano M, Blendinger PG, Lomáscolo SB, Chacoff NP, Sánchez MS, Núñez Montellano MG, Jiménez J, Ruggera RA, Valoy M (2017) The role of trait combination in the conspicuousness of fruit display among bird-dispersed plants. Funct Ecol 31:1718–1727

    Article  Google Scholar 

  124. Valenta K, Kalbitzer U, Razafimandimby D, Omeja P, Ayasse M, Chapman CA, Nevo O (2018) The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Sci Rep. https://doi.org/10.1038/s41598-018-32604-x

  125. Howe HF, Kerckhove GA (1980) Nutmeg dispersal by tropical birds. Science 210:925–927

    Article  CAS  PubMed  Google Scholar 

  126. Clark L, Avilova KV, Beans NJ (1993) Odor thresholds in passerines. Comp Biochem Physiol A Physiol 104A:305–312

    Article  Google Scholar 

  127. Mennerat A, Bonadonna F, Perret P, Lambrechts MM (2005) Olfactory conditioning experiments in a food-searching passerine bird in semi-natural conditions. Behav Process 70:264–270

    Article  CAS  Google Scholar 

  128. Clark L, Hagelin J, Werner S (2014) The chemical senses in birds. In: Scanes CG (ed) Sturkie’s avian physiology, 6th edn. Academic Press, New York, pp 89–111

    Google Scholar 

  129. Caspers BA, Krause ET (2011) Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Biol Lett 7:184–186

    Article  PubMed  Google Scholar 

  130. Mennerat A (2008) Blue tits (Cyanistes caeruleus) respond to an experimental change in the aromatic plant odour composition of their nest. Behav Process 79:189–191

    Article  CAS  Google Scholar 

  131. Gwinner H, Berger S (2008) Starling males select green nest material by olfaction using experience-independent and experience-dependent cues. Anim Behav 75:971–976

    Article  Google Scholar 

  132. Laska M, Hernandez Salazar LT (2015) Olfaction in nonhuman primates. In: Doty RL (ed) Handbook of olfaction and gustation. Wiley, New York, pp 607–623

    Google Scholar 

  133. Hernandez Salazar LT, Laska M, Rodriguez Luna E (2003) Olfactory sensitivity for aliphatic esters in spider monkeys (Ateles geoffroyi). Behav Neurosci 117:1142–1149

    Article  PubMed  CAS  Google Scholar 

  134. Laska M, Seibt A (2002) Olfactory sensitivity for aliphatic alcohols in squirrel monkeys and pigtail macaques. J Exp Biol 205:1633–1643

    CAS  PubMed  Google Scholar 

  135. Nevitt GA (2000) Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol Bull 198:245–253

    Article  CAS  PubMed  Google Scholar 

  136. Rizvanovic A, Amundin M, Laska M (2013) Olfactory discrimination ability of Asian elephants (Elephas maximus) for structurally related odorants. Chem Senses 38:107–118

    Article  CAS  PubMed  Google Scholar 

  137. Niimura Y, Matsui A, Touhara K (2014) Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res 24:1485–1496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Schmitt MH, Shuttleworth A, Ward D, Shrader AM (2018) African elephants use plant odours to make foraging decisions across multiple spatial scales. Anim Behav 141:17–27

    Article  Google Scholar 

  139. Rasmussen LE, Lazar J, Greenwood DR (2003) Olfactory adventures of elephantine pheromones. Biochem Soc Trans 31:137–141

    Article  CAS  PubMed  Google Scholar 

  140. Bates LA, Sayialel KN, Njiraini NW, Moss CJ, Poole JH, Byrne RW (2007) Elephants classify human ethnic groups by odor and garment color. Curr Biol 17:1938–1942

    Article  CAS  PubMed  Google Scholar 

  141. Chapman LJ, Chapman CA, Wrangham RW (1992) Balanites wilsoniana: elephant dependent dispersal? J Trop Ecol 8:275–283

    Article  Google Scholar 

  142. Babweteera F, Savill P, Brown N (2007) Balanites wilsoniana: regeneration with and without elephants. Biol Conserv 134:40–47

    Article  Google Scholar 

  143. Debussche M, Isenmann P (1989) Fleshy fruit characters and the choices of bird and mammal seed dispersers in a Mediterranean region. Oikos 56:327–338

    Article  Google Scholar 

  144. Baron G, Frahm HD, Bhatnagar KP, Stephan H (1983) Comparison of brain structure volumes in insectivora and primates. III. Main olfactory bulb (MOB). J Hirnforsch 24:551–568

    CAS  PubMed  Google Scholar 

  145. Penn HJ, Crist TO (2018) From dispersal to predation: a global synthesis of ant-seed interactions. Ecol Evol 210:291

    Google Scholar 

  146. Pfeiffer M, Huttenlocher H, Ayasse M (2010) Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants: chemical mimicry in myrmecochory. Funct Ecol 24:545–555

    Article  Google Scholar 

  147. Gervais JA, Traveset A, Willson MF (1998) The potential for seed dispersal by the banana slug (Ariolimax columbianus). Am Midl Nat 140:103–110

    Article  Google Scholar 

  148. Türke M, Heinze E, Andreas K, Svendsen SM, Gossner MM, Weisser WW (2010) Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia 163:681–693

    Article  PubMed  Google Scholar 

  149. Junker RR, Parachnowitsch AL (2015) Working towards a holistic view on flower traits-how floral scents mediate plant-animal interactions in concert with other floral characters. J Indian Inst Sci 95:43–67

    Google Scholar 

  150. Melin AD, Fedigan LM, Hiramatsu C, Hiwatashi T, Parr N, Kawamura S (2009) Fig foraging by dichromatic and trichromatic Cebus capucinus in a tropical dry forest. Int J Primatol 30:753–775

    Article  Google Scholar 

  151. Pellmyr O, Thien LB (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35:76–85

    Article  Google Scholar 

  152. Rodríguez A, San Andrés V, Cervera M, Redondo A, Alquézar B, Shimada T, Gadea J, Rodrigo MJ, Zacarías L, Palou L, López MM, Castañera P, Peña L (2011) Terpene down-regulation in orange reveals the role of fruit aromas in mediating interactions with insect herbivores and pathogens. Plant Physiol 156:793–802

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Junker RR (2017) A biosynthetically informed distance measure to compare secondary metabolite profiles. Chemoecology. https://doi.org/10.1007/s00049-017-0250-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Galetti M, Guevara R, Côrtes MC, Fadini R, Von Matter S, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimarães PR, Brancalion PH, Ribeiro MC, Jordano P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090

    Article  CAS  PubMed  Google Scholar 

  155. Brodie JF (2017) Evolutionary cascades induced by large frugivores. Proc Natl Acad Sci 114:11998–12002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Kleiner A (2018) Olfactory and visual signals of animal dispersed fruits in the temperate climate of South Germany. MSc thesis, University of Ulm

    Google Scholar 

  157. Haynes KF, Millar JG (2012) Methods in chemical ecology volume 2: bioassay methods. Springer Science & Business Media, Norwell

    Google Scholar 

Download references

Acknowledgments

ON was funded by the German Science Foundation (Deutsche Forschungsgemeinschaft; grant nr. 2156/1-1) while working on this chapter. Dr. Kim Valenta and Prof. Colin A. Chapman were heavily involved in data collection in Uganda, which was used for some of the unpublished results cited here.

Author information

Authors and Affiliations

  1. Institute of Evolutionary Ecology and Conservation Genomics, Ulm University, Ulm, Germany

    Omer Nevo & Manfred Ayasse

Authors
  1. Omer Nevo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manfred Ayasse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Omer Nevo .

Editor information

Editors and Affiliations

  1. Inst.des Sci.de la Vigne et du Vin, Université de Bordeaux Inst.des Sci.de la Vigne et du Vin, Villenave d'Ornon, France

    Jean-Michel Merillon

  2. Botany Department, Mohanlal Sukhadia University Botany Department, Udaipur, Rajasthan, India

    Kishan Gopal Ramawat

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Nevo, O., Ayasse, M. (2019). Fruit Scent: Biochemistry, Ecological Function, and Evolution. In: Merillon, JM., Ramawat, K. (eds) Co-Evolution of Secondary Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-76887-8_33-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-76887-8_33-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-76887-8

  • Online ISBN: 978-3-319-76887-8

  • eBook Packages: Springer Reference Chemistry and Mat. ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics

Publish with us

Policies and ethics

Search

Navigation