A framework for comparing pollinator performance: effectiveness and efficiency
Ne'eman, G., Jürgens, A., Newstrom-Lloyd, L., Potts, S. G. and Dafni, A. (2009) A framework for comparing pollinator performance: effectiveness and efficiency. Biological Review, 85 (3). pp. 435-451. ISSN 1464-7931
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To link to this article DOI: 10.1111/j.1469-185X.2009.00108.x
Measuring pollinator performance has become increasingly important with emerging needs for risk assessment in conservation and sustainable agriculture that require multi-year and multi-site comparisons across studies. However, comparing pollinator performance across studies is difficult because of the diversity of concepts and disparate methods in use. Our review of the literature shows many unresolved ambiguities. Two different assessment concepts predominate: the first estimates stigmatic pollen deposition and the underlying pollinator behaviour parameters, while the second estimates the pollinator’s contribution to plant reproductive success, for example in terms of seed set. Both concepts include a number of parameters combined in diverse ways and named under a diversity of synonyms and homonyms. However, these concepts are overlapping because pollen deposition success is the most frequently used proxy for assessing the pollinator’s contribution to plant reproductive success. We analyse the diverse concepts and methods in the context of a new proposed conceptual framework with a modular approach based on pollen deposition, visit frequency, and contribution to seed set relative to the plant’s maximum female reproductive potential. A system of equations is proposed to optimize the balance between idealised theoretical concepts and practical operational methods. Our framework permits comparisons over a range of floral phenotypes, and spatial and temporal scales, because scaling up is based on the same fundamental unit of analysis, the single visit.
● Aigner, P. A. (2001). Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? Oikos 95, 177. ● Aigner, P. A. (2004). Floral specialization without trade-offs: optimal corolla flare in contrasting pollination environments. Ecology 85, 2560–2569. ● Aigner, P. A. (2006).The evolution of specialized floral phenotypes in a fine-grained pollination environment. In Plant Pollinator Interactions from specialization to generalization (eds. N. M. Waser, J. Ollerton), pp. 23–46. University of Chicago Press, Chicago. ● Andersson, S. (1988). Size dependent pollination efficiency in Anchusa officinalis (Boraginaceae): causes and consequences. Oecologia 76, 125–130. ● Andersson, S. (1996). Floral variation in Saxifraga granulata - phenotypic selection, quantitative genetics and predicted response to selection. Heredity 77, 217–23. ● Armbruster,W. S. (1988).Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69, 1746–761. ● Arroyo, J. & Dafni, A. (1995). Variation in habitat, season, flower traits, and pollinators in dimorphic Narcissus tazetta L. (Amaryllidaceae) in Israel. New Phytologist 129, 135–145. ● Ashman, T.-L., Galloway, F. & Stanton, M. L. (1993). Apparent vs. effective mating in an experimental population of Raphanus sativus. Oecologia 96, 102–107. ● Ashman, T.-L. & Stanton, M. L. (1991). Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana spp. spicata (Malvaceae). Ecology 72, 993–1003. ● Beatie, A. J. (1976). Plant dispersion, pollination and gene flow in Viola. Oecologia 25, 291–300. ● Bertin, R. I. (1982). Floral biology, hummingbird pollination and fruit production of trumpet creeper (Campsis radicans, Bignoniaceae). American Journal of Botany 69, 122–34. Bertin,R. I. (1986).Consequences of mixed pollinations in Campsis radicans. Oecologia 70, 1–5. ● Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlem¨uller, R., Edwards, M., Peeters, T., Schaffers, A. P., Potts, S. G., Kleukers, R., Thomas, C. D., Settele, J. & Kunin, W. E. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–54. ●Bloch, D., Werdenberg, N. & Erhardt, A. (2006). Pollination crisis in the butterfly-pollinated wild carnation Dianthus carthusianorum? New Phytologist 169, 699–706. Bond,W. J. (1994). Do mutualismsmatter? Assessing the impact of pollinators disperser disruption on plant extinction. Philosophical Transactions of the Royal Society of London Series B 344, 83–90. ●Bosch, M. & Waser, N. M. (2001). Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126, 76–83. ● Burd, M. (1994). Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Reviews 60, 83–139. ● Byers, D.L. &Waller, D. M. (1999).Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30, 479–513. ● Calzoni, G. L. & Speranza, A. (1998). Insect controlled pollination in Japanese plum (Prunus salicinia Lindl.). Scientia Horticulturae 72, 227–37. ● Campbell, D. R. (1989). Measurements of selection in a hermaphroditic plant: variation in male and female pollination success. Evolution 43, 318–18. ● Cane, J. H. & Schiffhauer, D. (2001). Pollinator genetics and pollination: do honey bee colonies selected for pollen-hoarding field better pollinators of cranberry Vaccinium macrocarpon? Ecological Entomology 26, 117–17. ● Cane, J. H. & Schiffhauer, D. (2003). Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). American Journal of Botany 90, 1425–32. ● Canto-Aguilar, M. A. & Parra-Tabla, V. (2000). Importance of conserving alternative pollinators: assessing the pollination efficiency of the squash bee, Peponapis limitaris in Cucurbita moschata (Cucurbitaceae). Journal of Insect Conservation 4, 203–10. ● Cauich, O., Quezada-Euan, J. J., Macias-Macias, J. O., Reyes-Oregel, V., Medina-Peralta, S.& Parra-Tabla, V. (2004). Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera:Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical Mexico. Journal of Economic Entomology 97, 475–81. ● Charlesworth, D. & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–68. ● Corbet, S. A. (1998). Fruit and seed production in relation to pollination and resources in bluebell, Hyacinthoides non-scripta. Oecologia 114, 349–60. ● Crepet, W. L. (1983).The role of insect pollination in the evolution of angiosperms. In Pollination Biology (ed. L Real), pp. 31–48. Academic Press, New York. ● Crome, F.&Irvine, A. (1986). ‘Two bob each way’: the pollination and breeding system of the Australian rainforest tree Syzigium cormiflorum (Myrtaceae). Biotropica 18, 115–25. ● Cruden, R. W. (1977). Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31, 32–46. ● Cruden, R. W., Baker, K. K., Cullinan T. E., Disbrow, K. A., Douglas, K. L., Weier, J. A. & Willmott, S. R. (1990). The mating system and pollination biology of three species of Verbena (Verbenaceae). Journal of the Iowa Acadamy of Science 97, 178–83. ● Cruden, R.W. (2002). Pollen grains: why so many? Plant Systematics and Evolution 222, 143–65. ● Dafni, A., Eisikowitch, D. & Ivri, Y. (1987). Nectar flow and pollinator’s efficiency in two co-occurring species of Capparis (Capparaceae) in Israel. Plant Systematics and Evolution 157, 181–86. ● Dafni, A. & Firmage, D. (2000). Pollen viability and longevity: practical, ecological and evolutionary implications. Plant Systematics and Evolution 222, 113–32. ● Dafni, A., Pacini, E. & Nepi, M. (2005). Pollen and stigma biology. In Practical Pollination Biology (eds. A. Dafni, P. G. Kevan, B. C. Husband), pp. 83–142. Enviroquest, Cambridge (Ontario, Canada). ● De jong, T. J., Waser, N. M., & Klinkhamer, P. G. L. (1993). geitonogamy: the neglected side of selfing. Trends in Ecology and Evolution 8, 321–325. ● De jong, T. J., Waser, N. M. , Price, M. V. & Ring, R. M. (1992). Plant size, geitonogamy and seed set in Ipomopsis aggregata. Oecologia 89, 310–15. ● Dieringer, G. (1992). Pollinator effectiveness and seed set in populations of Agalinis strictifolia (Scrophulariaceae). American Journal of Botany 79, 1018–23. ● Di Pasquale, C.&Jacobi, C.M. (1998).Dynamics of pollination: A model of insect-mediated pollen transfer in self-incompatible plants. Ecological Modelling 109, 25–34. ● Donovan, B. J. & Read, P. E. C. (1991). Efficiency of honey bees as pollinators of kiwifruit. Acta Horticulturae 288, 220–24. Eltz, T. (2006). Tracing pollinator footprint on natural flowers. Journal of Chemical Ecolology 32, 907–915. ● Falque, M., Lesdalons, C. & Eskes, A. B. (1996). Comparison of two cacao (Theobroma cacao L.) clones for the effect of pollination intensity on fruit set and seed content. Sexual Plant Reproduction 9, 221–27. ● Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R. & Thomson, J. D. (2004). Pollination syndromes and floral specialization. Annual Reviews of Ecology, Evolution and Systematics 35, 375–403. ● Fishbein, M. & Venable, D. L. (1996). Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77, 1961–73. ● Fumero-Cab´an, J. J. & Mel´endez-Ackerman, E. J. (2007). Relative pollination efficiency of floral visitors of Pitcairnia angustifolia (Boraginaceae). American Journal of Botany 94, 419–424. ● Galen, C. & Newport, M. E. A. (1987). Bumble bee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia 74, 20–23. ● Galen, C. & Stanton, M. L. (1989). Bumble bee pollination and floral morphology: factors influencing pollen dispersal in the alpine sky pilot, Polemonium viscosum (Polemoniaceae). American Journal of Botany 76, 419–26. ● G´omez, J. M. & Zamora, R. (1999). Generalization in the interaction between Hormathophylla spinosa (Cruciferae) and its pollinators. Ecology 80, 796–805. ● Grant, V. (1971). Plant Speciation. Columbia University Press, New York. Grimaldi, D. (1991). The co-radiations of pollinating insects and angiosperms in the Cretaceous. Annals of the Missouri Botanical Garden 86, 373–406. ● Gross, C. L. (2005). Pollination efficiency and pollinator effectiveness. In Practical Pollination Biology (eds. A. Dafni, P. G. Kevan, B. C. Husband), pp. 354–63. Enviroquest, Cambridge (Ontario, Canada). ● Gudin, S. & Arene, L. (1991). Influence of the pH of the stigmatic exudates on male–female interaction in Rosa hybrida L. Sexual Plant Reproduction 4, 110–12. ● Guo, Y-H., Sperry, R., Cook, C. D. K. & Cox, P. A. (1990). The pollination ecology of Zannichellia palustris L. (Zannichelliaceae). Aquatic Botany 38, 341–56. ● Harder, L. D. & Wilson, W. G. (1994). Floral evolution and male reproductive success: Optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evolutionary Ecology 8, 542–59. ● Harder, L. D.&Wilson, W. G. (1998).Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79, 2789–807. ● Herrera, C. M. (1987). Components of pollinator ‘quality’: comparative analysis of a diverse insect assemblage. Oikos 50, 79–90. ● Herrera, C. M. (1990). Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos 58, 277–88. ● Hiei, K. & Suzuki, K. (2001). Visitation frequency of Melampyrum roseum var. japonicum (Scrophulariaceae) by three bumblebee species and its relation to pollination efficiency. Canadian Journal of Botany 79, 1167–74. ● Hoffmann, I. (2006). Seasonal changes in the pollination system of Micromereia fruticosa L. (Lamiaceae) and its efficiency in two populations on Mt. Carmel. M.Sc. thesis. Univ. Haifa, Israel. Inouye, D. W., Gill, D. E., Dudash, M. R. & Fenster, C. B. (1994). A model and lexicon for pollen fate. American Journal of Botany 81, 1517–30. ● Ivey, C. T., Martinez, P. & Wyatt, R. (2003). Variation in pollinator effectiveness in swamp milkweed, Asclepias incarnata (Apocynaceae). American Journal of Botany 90, 214–25. ● Janzen, D. H. (1977). A note on optimal mate selection by plants. American Naturalist 111, 365–71. ● Javorek, S. K., Mackenzie, K. E. & Vander Kloet, S. P. (2002). Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Annals of the Entomological Society of America 95, 345–51. ● Johnson, S. D. & Steiner, K. E. (2000). Generalization versus specialization in plant pollinator systems. Trends in Ecology and Evolution 15, 140–44. ● Kandori, I. (2002). Diverse visitors with various pollinator importance and temporal change in the important pollinators of Geranium thunbergii (Geraniaceae). Ecological Research 17, 283–94. ● Kearns, C. A. & Inouye, D. W. (1993). Techniques for Pollination Biologists. Boulder: University Press of Colorado. Kearns, C. A., Inouye, D. W. & Waser, N. M. (1998). Endangered mutualism: conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics 29, 83–112. ● Keys, R. N., Buchmann, S. L. & Smith, S. E. (1995). Pollination effectiveness and pollination efficiency of insects foraging Prosopis velutina in south-eastern Arizona. Journal Applied Ecology 32, 519–27. ● Klein, A. M., Steffan-Dewenter, I. & Tscharntke, T. (2003). Pollination of Coffea canephora in relation to local and regional agroforestry management. Journal Applied Ecology 40, 837–45. ● Lau, J. A. & Galloway, L. F. (2004). Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae). Oecologia 141, 562–76. ● Lebuhn, G. & Holsinger, K. (1998). A sensitivity analysis of pollen-dispensing schedules. Evolutionary Ecology 12, 111–21. ● Lee, T. D. (1984). Patterns of fruit maturation: a gametophyte competition hypothesis. American Naturalist 123, 427–32. ● Lord, E. M. & Russell, S. D. (2002). The mechanisms of pollination and fertilization in plants. Annual Review of Cell and Developmental Biology 18, 81–105. ● Mayfield, M., Waser, N. M. & Price, M. (2001). Exploring the ‘Most effective pollinator principle’ with complex flowers: bumblebees and Ipomopsis aggregata. Annals of Botany 88, 591–96. ● Meisles, S. & Chiasson, H. (1997). Effectiveness of Bombus impatiens Cr. as pollinators of greenhouse sweet peppers (Capsicum annuum L.). Acta Horticulturae 437, 425–29. ● Mesquida, J. & Renard, M. (1981). Pollination of male-fertile and male-sterile lines of winter oilseed rape (Brassica napus L. var. oleifera Metzger) by honeybees (Apis mellifera L.): Incidences on plant phenology and yield (in French). Apidologie 12, 345–62. ● Mitchell, R. J. (1997).Effects on pollination intensity on Lesquerella fendleri seed set: variation among plants. Oecologia 109, 382–88. ● Montalvo, A. M. & Ackerman, J. D. (1986). Relative pollinator effectiveness and evolution of floral traits in Spathiphyllum friedrichsthalii (Araceae). American Journal of Botany 73, 1665–76. ● Morandin, L. A., Laverty, T. M. & Kevan, P. G. (2001). Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. Journal of Economic Entomology 94, 462–67. ● Morison, N., Vaissiere, B. E., Martin, F., Pecaut, P. & Cambon, G. (2000). Pollination of globe artichoke (Cynara scolymus L.) by honey bees (Apis mellifera L.) to produce hybrid seed under enclosure. Apidologie 31, 115–28. ● Morris, W. F., Price, M. V., Waser, N. M., Thomson, J. D., Thomson, B.&Stratton, D. A. (1994). Systematic increase in pollen carryover and its consequences for geitonogamy in plant populations. Oikos 71, 431–40. ● Motten, A. F. (1986). Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecological Monographs 56, 21–42. ● Motten, A. F., Campbell, D. R., Alexander, D. E. & Miller, H. L. (1981). Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62, 1278–87. ● Muchhala, N. (2003). Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae). Oecologia 134, 373–80. ● Nepi, M. & Pacini, E. (1993). Pollination, pollen viability and pistil receptivity in Cucurbita pepo. Annals of Botany 72, 527–36. ● Niesenbaum, R. A. (1999). The effects of pollen load size and donor diversity on pollen performance, selective abortion, and progeny vigor in Mirabilis jalapa (Nyctaginaceae). American Journal of Botany 86, 261–68. ● Niesenbaum, R. A. & Casper, B. B. (1994). Pollen tube numbers and selective fruit maturation in Lindera benzoin. American Naturalist 144, 184–91. ● Olsen, K. M. (1997). Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109, 114–21. ● Ornelas, J. F., Jim´enez, L., Gonz´ales, C. & Hern´andez, A. (2004). Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropicalmontane cloud forest. I Hummingbirds’ effectiveness as pollen vectors. American Journal of Botany 91, 1052–60. ● Osorio-Beristain, M., Dominguez, C. A., eguiarte, L. E. & benrey, B. (1997). Pollination efficiency of native and invading africanized bees in the tropical dry forest annual plant, Kallstroemia grandiflora Torr ex Gray. Apidologie 28, 11–16. ● Parker, F. D. (1981). How efficient are bees in pollinating sunflowers? Journal of the Kansas Entomological Society 54, 61–67. ● Pettersson, M. W. (1991). Pollination by a guild of fluctuating moth populations: option for unspecialization in Silene vulgaris. Journal of Ecology 79, 591–604. ● Potts, S. G., Dafni, A.&Ne’eman G. (2001). Pollination of a core flowering shrub species in Mediterranean phrygana: variations in pollinator diversity, abundance and effectiveness in response to fire. Oikos 92, 71–80. ● Price, M. V. & Waser, N. M. (1979). Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature 277, 294–97. ● Primack, R. B. & Silander, J. A. (1975). Measuring the relative importance of different pollinators to plants. Nature 255, 143–44. ● Ramsey, M. & Vaughton, G. (2000). Pollen quality limits seed set in Burchardia umbellata (Colchicaceae). American Journal of Botany 87, 845–52. ● Rathcke, B. (1983). Competition and facilitation among plants for pollination. In Pollination Biology, (ed. L. Real), pp. 305–29. Academic Press, New York. ● Richards, A. J. (1986). Plant Breeding Systems. Allen and Unwin, London. Richards, K. W. (1987). Diversity, density, efficiency, and effectiveness of pollinators of cicer milkvetch, Astragalus cicer L. Canadian Journal of Zooogy 65, 2168–68. ● Richards, K. W. (1996). Comparative efficacy of bee species for pollination of legume seed crops. In The Conservation of Bees (Linnean Society Symposium Series) (eds. A. Matheson, C. O’Toole, I. Williams, S. L. Buchmann, P. Westrich), pp. 81–104. Academic Press, London. ● Rodet, G., Vaissi`ere, B. E., Br´evault, T. & Grossa, J-P. T. (1998). Status of self-pollen in bee pollination efficiency of white clover (Trifolium repens L.). Oecologia 114, 93–99. ● Sage, T. L., Husband, B. C. & Routley, M. T. (2005). Plant breeding systems and pollen dispersal: intrinsic attributes of the breeding system. In Practical Pollination Biology (eds. A. Dafni, P. G. Kevan, B. C. Husband), pp. 23–49. Enviroquest, Cambridge (Ontario, Canada). ● Sahli, H. F. & Conner, J. K. (2006). Characterizing ecological generalization in plant-pollination systems. Oecologia 148, 365–72. ● Saleh, A. & Chittka, L. (2006). The importance of experience in interpretation of conspecific chemical signals. Behavioral Ecology and Sociobiology 61, 215–220. ● Sampson, B. J. & Cane, J. H. (2000). Pollination efficiencies of three bee (Hymenoptera: Apoidea) species visiting rabbiteye blueberry. Journal of Economic Entomology 93, 1726–31. ● Schemske, D. W. & Bradshaw, H. D. Jr. (1999). Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences U.S.A. 96, 11910–15. ● Schemske, D. W. & Horvitz, C. C. (1984). Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225, 519–21. ● Schlindwein, C.&Wittman, D. (1995). Specialized solitary bees as effective pollinators of South Brazilian species of Notocactus and Gymnocalycium (Cactaceae). Bradleya 13, 25–34. ● Schneider, D., Stern, R. A., Eisikowitch, D. &Goldway, M. (2002). The relationship between floral structure and honeybee pollination efficiency in ‘Jonathan’ and ‘Topred’ apple cultivars. Journal of Horticultural Science & Biotechnology 77, 48–51. ● Sih, A. & Baltus, M. S. (1987). patch size, pollinator behavior and pollinator limitation in catnip. Ecology 68, 1679–95. ● Sihag, R. C. (1997). Determining the efficiency of pollinators. In Pollination Biology: Basic and Applied Principles (ed. R. C. Sihag), pp. 171–86. Scientific Publishers, Hisar Rajendra. Snow, A. A., Spira, T. P., Simpson, R. & Klips, R. A. (1996).The ecology of geitonogamous pollination. In Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (eds. D. G. Lloyd, S. C. H. Barrett), pp. 191–216. Chapman & Hall, New York. ● Spears, E. (1983). A direct measure of pollinator effectiveness. Oecologia 57, 196–99. ● Stebbins, G. L. (1970). Adaptive radiation of reproductive characteristics in angiosperms, I: Pollination mechanisms. Annual Review of Ecology and Systematics 1, 307–26. ● Stephenson, A. G. (1981). Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12, 253–79. ● Sugden, E. (1986). Anthecology and pollinator efficacy of Styrax officinale subsp. redivivum (Styracaceae). American Journal of Botany 73, 919–30. ● Suzuki, K. & Akazome, Y. (2000). Flexibility of pollinator-flower relationship in Isodon umbrosus and I. effuses (Lamiaceae) and its relation to fruit-set and seed-set. Journal of Plant Research 113, 149–55. ● Suzuki, K., Dohzono, I., Hiei, K. & Fukuda, Y. (2002). Pollination effectiveness of the three bumblebee species on flowers of Hosta sieboldiana (Liliaceae) and its relation to floral structure and pollinator size. Plant Species Biology 17, 139–46. ● Tamura, S. & Kudo, G. (2000). Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis. Plant Ecology 147, 185–92. ● Tandon, R., Manohara, T. N., Nijalingappa, B. H. M. & Shivanna, K. R. (2001). Pollination and pollen–pistil interaction in oil palm, Elaeis guineensis. Annals of Botany 87, 831–38. ● Thomson, J. D. (2001). How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system. Oecologia 126, 386–94. ● Thomson, J. D. (2006). Tactics for male reproductive success in plants: contrasting insights of sex allocation theory and pollen presentation theory. Integrative and Comparative Biology 46, 390–97. ● Thomson, J. D., Wilson, P., Valenzuela, M. & Malzone, M. (2000). Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biology 15, 11–29. ● Titze, A. (2000).The efficiency of insect pollination of the neophyte Impatiens glandulifera (Balsaminaceae). Nordic Journal of Botany 20, 33–42. ● Vaissi`ere, B. E. (1991). Honey bees, Apis mellifera L. (Hymenoptera: Apidae), as pollinators of upland cotton, Gossypium hirsutum L. (Malvaceae), for hybrid seed production. PhD thesis. Texas A&M Univ., College Station. Vaissi`ere, B. E., Rodet, G., Cousin, M., Botella, L. & Torre Grossa, J-P. (1996). Pollination effectiveness of honey bees (Hymenoptera: Apidae) in a kiwifruit orchard. Journal of Economic Entomology 89, 453–61. ● Van Praagh, G. P. & Hauschildt, H. (1991). Evaluation of shoot-bending, pruning and pollination for increasing fruit-set and yield on young ‘Cox’ trees. Acta Horticulturae 288, 244–48. Vazquez, D. P., Morris,W. F. & Jordano, P. (2005). Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8, 1088–1094. ● Vaughton, G. & Ramsey, M. (2000). Pollinators and seed production. In Seed Development and Germination (eds. J. Kigel, G. Galili), pp. 475–90. New Marcel Dekker, York, Basel, Hong Kong. Vicens, N. & Bosch, J. (2000). Pollination efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on ‘Red Delicious’ Apple. Environmental Entomology 29, 235–40. ● Waser, N. M., Chittka, L., Neal, M. V., Williams, M. & Ollerton J. (1996). Generalization in pollination systems, and why it matters. Ecology 77, 1043–60. ● Waser, N. M. & Price, M. V. (1983). Pollinator behavior and natural selection for flower colour in Delphinium nelsonii. Nature 302, 422–24. ● Waser, N. M. & Price, M. V. (1990). Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collectanea Botanica 19, 9–20. ● Wilcock, C. C. & Neiland, M. R. M. (2002). Pollination failure in plants: why it happens and when it matters. Trends in Plant Science 7, 270–77. ● Willmott, A. P. & Burquez, A. (1996). The pollination of Merremia palmeri (Convolvulaceae): Can hawkmoths be trusted? American Journal of Botany 83, 1050–56. ● Wilson, P. (1995). Selection for pollination success and the mechanical fit of Impatiens flowers around bumblebee bodies. Biological Journal of the Linnean Society 55, 355–83. ● Wilson, P. & Thomson, J. D. (1991). Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72, 1503–07. ● Wilson, P. & Thomson J. D. (1996). How do flowers diverge? In Floral Biology (eds. D. G. Lloyd, S. C. H. Barrett), pp. 88–111. Chapman & Hall, New York ● Young, H. J. (2002). Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). American Journal of Botany 89, 433–40.
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