Start making scents: The challenge of integrating chemistry into pollination ecology

Entomologia Experimentalis et Applicata

Volumn 128, Issue 1, 2008, Pages 196-207

  Raguso, Robert A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Balancing selection; Floral color; Floral scent; Foraging; Generalized plant volatiles; Olfaction; Path analysis; Pollination syndromes; Vision

Indexed keywords

FLOODED SOIL; FLORA; FORAGING BEHAVIOR; OLFACTION; PATH ANALYSIS; PHENOTYPE; POLLINATION; POLLINATOR; SCENT MARKING; SPECIALIZATION;

EID: 46249120109     PISSN: 00138703     EISSN: 15707458     Source Type: Journal    
DOI: 10.1111/j.1570-7458.2008.00683.x     Document Type: Conference Paper

References (127)

1. Adler LS (2000) The ecological significance of toxic nectar. Oikos 91 : 409 420.
2. Adler LS Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86 : 2968 2978.
3. Afik O, Dag A, Kerem Z Shafir S (2006) Analyses of avocado (Persea americana) nectar properties and their perception by honey bees (Apis mellifera). Journal of Chemical Ecology 32 : 1949 1963.
4. Aigner PA (2001) Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? Oikos 95 : 177 184.
5. Aigner PA Scott PE (2002) Use and pollination of a hawkmoth plant, Nicotiana attenuata, by migrant hummingbirds. Southwestern Naturalist 47 : 1 11.
6. Andersen JF Metcalf RL (1986) Identification of a volatile attractant for Diabrotica (Coleoptera; Chrysomelidae) and Acalymma (Coleoptera; Chrysomelidae) spp. from blossoms of Cucurbita maxima Duchesne. Journal of Chemical Ecology 12 : 687 699.
7. Andrews ES, Theis N Adler LS (2007) Pollinator and herbivore attraction to Cucurbita floral volatiles. Journal of Chemical Ecology 33 : 1682 1691.
8. Angioy A-M, Stensmyr MC, Urru I, Puliafito M, Collu I Hansson BS (2003) Function of the heater: the dead horse arum revisited. Proceedings of the Royal Society of London B (Suppl 271 : S13 S15.
9. Armbruster WS McCormick KD (1990) Diel foraging patterns of male euglossine bees: ecological causes and evolutionary responses by plants. Biotropica 22 : 160 171.
10. Ashman T-L (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81 : 2577 2591.
11. Ashman T-L, Bradburn M, Cole DH, Blaney BH Raguso RA (2005) The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86 : 2099 2105.
12. Balkenius A Kelber A (2004) Colour constancy in diurnal and nocturnal hawkmoths. The Journal of Experimental Biology 207 : 3307 3316.
13. Balkenius A Kelber A (2006) Colour preferences influence odour learning in the hawkmoth, Macroglossum stellatarum. Naturwissenschaften 93 : 255 258.
14. Balkenius A, Rosén W Kelber A (2006) Nocturnal and diurnal hawkmoths give different weight to visual and olfactory flower cues. Journal of Comparative Physiology A 192 : 431 437.
15. Barth F (1991) Insects and Flowers. The Biology of a Partnership. Princeton University Press, Princeton, NJ, USA.
16. Bartlet E, Kiddle G, Williams I Wallsgrove R (1999) Wound-induced increases in the glucosinolate content of oilseed rape and their effect on subsequent herbivory by a crucifer specialist. Entomologia Experimentalis et Applicata 91 : 163 167.
17. Bernhardt P, Sage T, Weston P, Azuma H, Lam M et al 2003) The pollination of Trimenia moorei (Trimeniaceae): floral volatiles, insect/wind pollen vectors and stigmatic self-incompatibility in a basal angiosperm. Annals of Botany 92 : 445 458.
18. Bezemer TM, de Deyn GB, Bossinga TM, van Dam NM, Harvey JA van der Putten WH (2005) Soil community composition drives aboveground plant-herbivore- parasitoid interactions. Ecology Letters 8 : 652 661.
19. Borg-Karlson A-K, Unelius CR, Valterova I Nilsson LA (1996) Floral fragrance chemistry in the early flowering shrub Daphne mezereum. Phytochemistry 41 : 1477 1483.
20. Bradshaw HD, Jr & Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426 : 176 178.
21. de Bruxelles GL Roberts MR (2001) Signals regulating multiple responses to wounding and herbivores. Critical Reviews in Plant Sciences 20 : 487 521.
22. Carlsson MA Hansson BS (2006) Detection and coding of flower volatiles in nectar-foraging insects. Biology of Floral Scent (ed. by N Dudareva E Pichersky pp. 243 261. CRC Press, Boca Raton, FL, USA.
23. Chittka L (1997) Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded - why? Israel Journal of Plant Science 45 : 115 127.
24. Chittka L Brockmann A (2005) Perception space - the final frontier. PLoS Biology 3 : e137 (Doi:).
25. Conner JK (1996) Understanding natural selection: an approach integrating selection gradients, multiplicative fitness components and path analysis. Ethology, Ecology and Evolution 8 : 387 397.
26. De Moraes CM, Lewis WJ, Paré PW, Alborn HT Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393 : 570 573.
27. De Moraes CM, Mescher MC Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410 : 577 580.
28. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. Biology of Floral Scent (ed. by N Dudareva E Pichersky pp. 147 198. CRC Press, Boca Raton, FL, USA.
29. Dobson HEM, Danielson EM van Wesep ID (1999) Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biology 14 : 153 166.
30. Dobson HEM, Groth I Bergström G (1996) Pollen advertisement: chemical contrasts between whole-flower and pollen odors. American Journal of Botany 83 : 877 885.
31. Dötterl S, Füssel U, Jürgens A Aas G (2005) 1,4-Dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee. Journal of Chemical Ecology 31 : 2993 2998.
32. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ Chittka L (2006) Bees associate warmth with floral colour. Nature 442 : 525.
33. Endler JA (1987) Predation, light intensity and courtship behaviour in Poecilia reticulate (Pisces: Poeciliidae). Animal Behaviour 35 : 1376 1385.
34. Fenster CB, Armbruster WS, Wilson P, Dudash MR Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35 : 375 403.
35. Fineblum WL Rausher MD (1997) Do floral pigmentation genes also influence resistance to enemies: the W locus in Ipomoea purpurea. Ecology 78 : 1646 1654.
36. Fraenkel GS (1959) The raison d'être of secondary plant substances. Science 129 : 1466 1470.
37. Frey FM (2005) Color polymorphism in Claytonia virginica. Evolution 58 : 2426 2437.
38. Galetto L Bernardello G (2004) Floral nectaries, nectar production dynamics and chemical composition in six Ipomoea species (Convolvulaceae) in relation to pollinators. Annals of Botany 94 : 269 280.
39. Ghazoul J (2001) Can floral repellents pre-empt potential ant-plant conflicts? Ecology Letters 4 : 294 299.
40. Gómez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. The American Naturalist 162 : 242 256.
41. Goyret J, Markwell PM Raguso RA (2007) The effect of olfactory and visual stimuli decoupling on the foraging behavior of Manduca sexta. Journal of Experimental Biology 210 : 1398 1405.
42. Goyret J Raguso RA (2006) The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. Journal of Experimental Biology 209 : 1586 1593.
43. Harder LD Barrett SCH (2007) Ecology and Evolution of Flowers. Oxford University Press, Oxford, UK.
44. Healy SD Hurly TA (2001) Foraging and spatial learning in hummingbirds. Cognitive Ecology of Pollination (ed. by L Chittka JD Thomson pp. 127 147. Cambridge University Press, Cambridge, UK.
45. von Helversen D von Helversen O (1999) Acoustic guide in bat-pollinated flower. Nature 398 : 759 760.
46. Herrera CM (1990a) Daily patterns of pollinator activity, differential pollinating effectiveness and floral resource availability in a summer-flowering Mediterranean shrub. Oikos 58 : 277 288.
47. Herrera CM (1990b) The adaptedness of the floral phenotype in a relict endemic, hawkmoth-pollinated violet. 1. Reproductive correlates of floral variation. Biological Journal of the Linnean Society 40 : 263 274.
48. Herrera CM (1993) Selection on floral morphology and environmental determinants of fecundity in a hawkmoth-pollinated violet. Ecological Monographs 63 : 251 275.
49. Herrera CM (1995) Microclimate and individual variation in pollinators: flowering plants are more than their flowers. Ecology 76 : 1516 1524.
50. Herrera CM (1996) Floral traits and plant adaptation to insect pollinators: a devil's advocate approach. Floral Biology (ed. by DG Lloyd SCH Barrett pp. 65 87. Chapman & Hall, New York, NY, USA.
51. Hilker M Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 32 : 1379 1397.
52. Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M et al 2007) Single gene-mediated shift in pollinator attraction in petunia. The Plant Cell 19 : 779 790.
53. Horvitz CC Schemske DW (2002) Effects of plant size, leaf herbivory, local competition and fruit production on survival, growth and future reproduction of a neotropical herb. Journal of Ecology 90 : 279 290.
54. Irwin RE, Strauss SY, Storz S, Emerson A Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84 : 1733 1743.
55. Janzen DH (1985) A host plant is more than its chemistry. Illinois Natural History Survey Bulletin 33 : 141 174.
56. Johnson SD Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends in Ecology and Evolution 15 : 140 143.
57. Johnson SD, Hargreaves AL Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87 : 2709 2716.
58. Johnson SD, Linder HP Steiner KE (1998) Phylogeny and radiation of pollination systems in Disa (Orchidaceae). American Journal of Botany 85 : 402 411.
59. Jordano P, Bascompte J Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6 : 69 81.
60. Jordano P, Bascompte J Olesen JM (2006) The ecological consequences of complex topology and nested structure in pollination webs. Plant-Pollinator Interactions; from Specialization to Generalization (ed. by NM Waser J Ollerton pp. 173 199. University of Chicago Press, Chicago, IL, USA.
61. Jürgens A, Dötterl S Meve U (2006) The chemical nature of fetid floral odours in Stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytologist 172 : 452 468.
62. Kaczorowski RL, Gardener MC Holtsford TP (2005) Nectar traits in Nicotiana section Alatae (Solanaceae) in relation to floral traits, pollinators, and mating system. American Journal of Botany 92 : 1270 1283.
63. Kay KM Schemske DW (2004) Geographic patterns in plant-pollinator mutualistic networks: comment. Ecology 85 : 875 878.
64. Kelber A (1997) Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. Journal of Experimental Biology 200 : 826 835.
65. Kelber A Hénique U (1999) Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum L. Journal of Comparative Physiology A 184 : 535 541.
66. Kessler D Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. The Plant Journal 49 : 840 854.
67. Knudsen JT, Eriksson R, Gershenzon J Ståhl B (2006) Diversity and distribution of floral scent. The Botanical Review 72 : 1 120.
68. Kombrink E Schmelzer E (2001) The hypersensitive response and its role in local and systemic disease resistance. European Journal of Plant Pathology 107 : 69 78.
69. Lande R Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37 : 1210 1226.
70. Levin RA, Raguso RA McDade LA (2001) Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58 : 429 440.
71. Liu F, Chen J, Chai J, Zhang X, Bai X et al 2007) Adaptive functions of defensive plant phenolics and a non-linear bee response to nectar components. Functional Ecology 21 : 96 100.
72. Majetic CJ, Raguso RA, Tonsor SJ Ashman T-L (2007) Flower color-flower scent associations in polymorphic Hesperis matronalis (Brassicaceae). Phytochemistry 68 : 865 874.
73. Manning JC Goldblatt P (2005) Radiation of pollination systems in the Cape genus Tritoniopsis (Iridaceae: Crocoideae) and the development of bimodal pollination strategies. International Journal of Plant Sciences 166 : 459 474.
74. Medán D, Basilio AM, Devoto M, Bartoloni NJ, Tortea JP Petanidou T (2006) Measuring generalization and connectance in temperate, year-long active systems. Plant-Pollinator Interactions; from Specialization to Generalization (ed. by NM Waser J Ollerton pp. 244 259. University of Chicago Press, Chicago, IL, USA.
75. Memmott J (1999) The structure of a plant-pollinator food web. Ecology Letters 2 : 276 280.
76. Menzel R Shmida A (1993) The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a case study. Biological Reviews 68 : 81 120.
77. Metcalf RL Metcalf ER (1992) Plant Kairomones in Insect Ecology and Control. Chapman & Hall, New York, NY, USA.
78. Mitchell RJ (1993) Path analysis: pollination. Design and Analysis of Ecological Experiments (ed. by SM Scheiner J Gurevitch pp. 211 231. Chapman & Hall, New York, NY, USA.
79. Miyake T Yafuso M (2003) Floral scents affect reproductive success in fly-pollinated Alocasia odora (Araceae). American Journal of Botany 90 : 370 376.
80. Moré M, Sérsic AN Cocucci AA (2006) Restriction of pollinator assemblage through flower length and width in three long-tongued hawkmoth-pollinated species of Mandevilla (Apocynaceae, Apocynoideae). Annals of the Missouri Botanical Garden 94 : 485 504.
81. Mothershead K Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81 : 30 40.
82. Muchhala N (2006) The pollination biology of Burmeistera (Campanulaceae): specialization and syndromes. American Journal of Botany 93 : 1081 1089.
83. Nefdt RJC Compton SG (1996) Regulation of seed and pollinator production in the fig-fig wasp mutualism. Journal of Animal Ecology 65 : 170 182.
84. Nepi M, Guarnieri M Pacini E (2001) Nectar secretion, reabsorption and sugar composition in male and female flowers of Cucurbita pepo. International Journal of Plant Sciences 162 : 353 358.
85. Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant-pollinator systems. Journal of Ecology 84 : 767 769.
86. Ollerton J Watts S (2000) Phenotype space and floral typology : towards an objective assessment of pollination syndromes. Scandinavian Association for Pollination Ecology honours Knut Faegri (ed. by Ø Totland, WS Armbruster, C Fenster, U Molau, LA Nilsson, JM Olesen, J Ollerton, M Philipp J Ågren pp. 149 159. Norwegian Academy of Science and Letters 39, Oslo, Norway.
87. Ômura H, Honda K Hayashi N (2000) Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage butterfly, Pieris rapae. Journal of Chemical Ecology 26 : 655 666.
88. van Poecke RMP Dicke M (2004) Indirect defense of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biology 6 : 387 401.
89. Raguso RA (2004a) Why are some nectars scented? Ecology 85 : 1486 1494.
90. Raguso RA (2004b) Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Current Opinion in Plant Biology 7 : 434 440.
91. Raguso RA (2004c) Why do flowers smell? The chemical ecology of fragrance-driven pollination. Advances in Insect Chemical Ecology (ed. by RT Cardé JG Millar pp. 151 178. Cambridge University Press, Cambridge, UK.
92. Raguso RA Willis MA (2002) Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Animal Behaviour 63 : 685 695.
93. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S et al 2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434 : 732 737.
94. Rojas JC Wyatt TD (1999) Role of visual cues and interaction with host odour during the host-finding behaviour of the cabbage moth. Entomologia Experimentalis et Applicata 91 : 59 65.
95. Roy BA Raguso RA (1997) Olfactory vs. visual cues in a floral mimicry system. Oecologia 109 : 414 426.
96. Ryan MJ (1990) Sexual selection, sensory systems and sensory exploitation. Oxford Surveys in Evolutionary Biology 7 : 156 195.
97. Schaefer HM, Schaefer V Levey DJ (2004) How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19 : 577 584.
98. Scheiner SM, Donohue K, Dorn LA, Mazur SJ Wolfe LM (2002) Reducing environmental bias when measuring natural selection. Evolution 56 : 2156 2167.
99. Schemske DW Horvitz CC (1988) Plant-animal interactions and fruit production in a neotropical herb: a path analysis. Ecology 69 : 1128 1137.
100. Schiestl FP Marion-Poll F (2002) Detection of physiologically active flower volatiles using gas chromatography coupled with electroantennography. Molecular Methods of Plant Analysis, Vol. 21. Analysis of Taste and Aroma (ed. by JF Jackson, HF Linskens R Inman pp. 173 198. Springer, Berlin, Germany.
101. Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C et al 2004) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302 : 437 438.
102. Schiestl FP, Steinebrunner F, Schulz C, von Reuss S, Francke W et al 2006) Evolution of 'pollinator' attracting signals in fungi. Biology Letters 2 : 401 404.
103. Sime KR Baldwin IT (2003) Opportunistic out-crossing in Nicotiana attenuata (Solanaceae), a predominantly self-fertilizing native tobacco. BMC Ecology 3 : 1 9.
104. Simms EL Bucher MA (1996) Pleiotropic effects of flower-color intensity on herbivore performance on Ipomoea purpurea. Evolution 50 : 957 963.
105. Singaravelan N, Inbar M, Nee'Man G, Distl M, Wink M Izhaki I (2006) The effects of nectar-nicotine on colony fitness of caged honeybees. Journal of Chemical Ecology 32 : 42 59.
106. Stang M, Klinkhamer PGL van der Meijden E (2006) Size constraints and flower abundance determine the number of interactions in a plant-flower visitor web. Oikos 112 : 111 121.
107. Strauss SY (1997) Floral characters link herbivores, pollinators and plant fitness. Ecology 78 : 1640 1645.
108. Strauss SY Whittall JB (2007) Non-pollinator agents of selection on floral traits. Ecology and Evolution of Flowers (ed. by LD Harder SCH Barrett pp. 120 138. Oxford University Press, Oxford, UK.
109. Temeles EJ (1996) A new dimension to hummingbird-flower relationships. Oecologia 105 : 517 523.
110. Thaler JS, Karban R, Ullman DE, Boege K Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131 : 227 235.
111. Theis N (2006) Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology 32 : 917 927.
112. Theis N, Lerdau M Raguso RA (2007) The challenge of attracting pollinators while evading floral herbivores: patterns of fragrance emission in Cirsium arvense and Cirsium repandum (Asteraceae). International Journal of Plant Sciences 168 : 587 601.
113. Theis N Raguso RA (2005) The effect of pollination on floral fragrance in thistles. Journal of Chemical Ecology 31 : 2581 2600.
114. Tholl D Röse USR (2006) Detection and identification of floral scent compounds. Biology of Floral Scent (ed. by N Dudareva E Pichersky pp. 3 26. CRC Press, Boca Raton, FL, USA.
115. Vázquez DP (2005) Degree distribution in plant-/animal mutualistic networks: forbidden links or random interactions? Oikos 108 : 421 426.
116. Vázquez DP Aizen MA (2003) Null model analyses of specialization in plant-pollinator interactions. Ecology 84 : 2493 2501.
117. Vázquez DP Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant-pollinator interactions. Ecology 85 : 1251 1257.
118. Vázquez DP Aizen MA (2006) Community-wide patters of specialization in plant-pollinator interactions revealed by null models. Plant-Pollinator Interactions; from Specialization to Generalization (ed. by NM Waser J Ollerton pp. 200 219. University of Chicago Press, IL, USA.
119. Waser NM, Chittka L, Price MV, Williams NM Ollerton J (1996) Generalization in pollination systems and why it matters. Ecology 77 : 1043 1060.
120. Waser NM Ollerton J (2006) Plant-Pollinator Interactions : From Specialization to Generalization. University of Chicago Press, Chicago, IL, USA.
121. Waser NM Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collectanea Botanica (Barcelona) 19 : 9 20.
122. Weiss MR (1997) Innate colour preferences and flexible colour learning in the pipevine swallowtail. Animal Behaviour 53 : 1043 1052.
123. Whittall JB Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447 : 707 710.
124. Willmer PG Stone GN (1997) How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388 : 165 167.
125. Wilson P, Castellanos MC, Hogue JN, Thomson JD Armbruster WS (2004) A multivariate search for pollination syndromes among penstemons. Oikos 104 : 345 361.
126. Wilson P, Castellanos MC, Wolfe AD Thomson JD (2006) Shifts between bee and bird pollination among penstemons. Plant-Pollinator Interactions: From Specialization to Generalization (ed. by NM Waser J Ollerton pp. 47 68. University of Chicago Press, Chicago, IL, USA.
127. Zuk M, Rotenberry JT Simmons LW (1998) Calling songs of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evolution 52 : 166 171.