The Botanical Review

, Volume 60, Issue 1, pp 83–139 | Cite as

Bateman’s principle and plant reproduction: The role of pollen limitation in fruit and seed set

  • Martin Burd


Bateman’s principle states that male fitness is usually limited by the number of matings achieved, while female fitness is usually limited by the resources available for reproduction. When applied to flowering plants this principle leads to the expectation that pollen limitation of fruit and seed set will be uncommon. However, if male searching for mates (including pollen dissemination via external agents) is not sufficiently successful, then the reproductive success of both sexes (or both sex functions in hermaphroditic plants) will be limited by number of matings rather than by resources, and Bateman’s principle cannot be expected to apply. Limitation of female success due to inadequate pollen receipt appears to be a common phenomenon in plants. Using published data on 258 species in which fecundity was reported for natural pollination and hand pollination with outcross pollen, I found significant pollen limitation at some times or in some sites in 159 of the 258 species (62%). When experiments were performed multiple times within a growing season, or in multiple sites or years, the statistical significance of pollen limitation commonly varied among times, sites or years, indicating that the pollination environment is not constant. There is some indication that, across species, supplemental pollen leads to increased fruit set more often than increased seed set within fruits, pointing to the importance of gamete packaging strategies in plant reproduction. Species that are highly self-incompatible obtain a greater benefit relative to natural pollination from artificial application of excess outcross pollen than do self-compatible species. This suggests that inadequate pollen receipt is a primary cause of low fecundity rates in perennial plants, which are often self-incompatible. Because flowering plants often allocate considerable resources to pollinator attraction, both export and receipt of pollen could be limited primarily by resource investment in floral advertisement and rewards. But whatever investment is made is attraction, pollinator behavioral stochasticity usually produces wide variation among flowers in reproductive success through both male and female functions. In such circumstances the optimal deployment of resources among megaspores, microspores, and pollinator attraction may often require more flowers or more ovules per flower than will usually be fertilized, in order to benefit from chance fluctuations that bring in large number of pollen grains. Maximizing seed set for the entire plant in a stochastic pollination environment might thus entail a packaging strategy for flower number or ovule number per flower that makes pollen limitation of fruit or seed set likely. Pollen availability may limit female success in individual flowers, entire plants (in a season or over a lifetime), or populations. The appropriate level must be distinguished depending on the nature of the question being addressed.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Ackerman, J. D. 1989. Limitations to sexual reproduction inEncyclia krugerii (Orchidaceae). Syst. Bot.14:101–109.Google Scholar
  2. — &A. M. Montalvo. 1990. Short- and long-term limitations to fruit production in a tropical orchid. Ecology71:263–272.Google Scholar
  3. — &J. C. Montero Oliver. 1985. Reproductive biology ofOncidium variegatum: moon phases, pollination and fruit set. Amer. Orchid Soc. Bull.54:326–329.Google Scholar
  4. Ågren, J. 1989. Seed size and number inRubus chamaemorus: between-habitat variation, and effects of defoliation and supplemental pollination. J. Ecol.77:1080–1092.Google Scholar
  5. — &D. W. Schemske. 1991. Pollination by deceipt in a neotropical monoecious herb,Begonia involucrata. Biotropica23:235–241.Google Scholar
  6. — &M. F. Willson. 1992. Determinants of seed production inGeranium maculatum. Oecologia92:177–182.Google Scholar
  7. Alexander, H. M. 1987. Pollination limitation in a population ofSilene alba infected by the anther-smutUstilago violacea. J. Ecol.75:771–780.Google Scholar
  8. Allen, T. F. H. &T. W. Hoekstra. 1992. Toward a Unified Ecology. Columbia Univ. Press, New York.Google Scholar
  9. Aluri, R. J. S. 1990. The explosive pollination mechanism and mating system of the weedyHyptis suaveolens (Lamiaceae). Pl. Spec. Biol.5:235–241.Google Scholar
  10. Anderson, R. C. &M. H. Beare. 1983. Breeding system and pollination ecology ofTrientalis borealis (Primulaceae). Amer. J. Bot.70:408–415.Google Scholar
  11. Andersson, S. 1988. Size-dependent pollination efficiency inAnchusa officinalis (Boraginaceae): causes and consequences. Oecologia76:125–130.Google Scholar
  12. —. 1989. The evolution of self-fertility inCrepis tectorum (Asteraceae). Pl. Syst. Evol.168:227–236.Google Scholar
  13. Arnold, R. M. 1982. Pollination, predation, and seed set inLinaria vulgaris (Scrophulariaceae). Amer. Midl. Naturalist107:360–369.Google Scholar
  14. Arroyo, M. T. K. &P. Uslar. 1993. Breeding systems in a temperate mediterranean-type climate montane sclerophyllous forest in central Chile. Bot. J. Linn. Soc.111:83–102.Google Scholar
  15. Augspurger, C. K. &K. P. Hogan. 1983. Wind dispersal of fruits with variable seed number in a tropical tree (Lonchcarpus pentaphyllus: Leguminosae). Amer. J. Bot.70:1031–1037.Google Scholar
  16. Banks, J. A. 1980. The reproductive biology ofErythronium propullans Gray and sympatric populations ofE. albidum Nutt. (Liliaceae). Bull. Torrey Bot. Club107:181–188.Google Scholar
  17. Barrett, S. C. H. 1980. Sexual reproduction inEichornia crassipes (water hyacinth) II. Seed production in natural populations. J. Appl. Ecol.17:113–124.Google Scholar
  18. — &K. Helenurm. 1987. The reproductive biology of boreal forest herbs. I. Breeding systems and pollination. Canad. J. Bot.65:2036–2046.Google Scholar
  19. Bateman, A. J. 1948 Intra-sexual selection inDrosophila. Heredity2:349–368PubMedGoogle Scholar
  20. Bawa, K. S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution28:85–92.Google Scholar
  21. — &J. H. Beach. 1981. Evolution of sexual systems in flowering plants. Ann. Missouri Bot. Gard.68:254–274.Google Scholar
  22. — &C. J. Webb. 1984. Flower, fruit and seed abortion in tropical forest trees: implications for the evolution of paternal and maternal reproductive patterns. Amer. J. Bot.71:736–751.Google Scholar
  23. Bell, G. 1985. On the function of flowers. Proc. Roy. Soc. LondonB224:223–265.Google Scholar
  24. —,L. Lefebvre, L.-A. Giraldeau &D. Weary. 1984. Partial preferences of insects for the male flowers of an annual herb. Oecologia64:287–294.Google Scholar
  25. Benseler, R. W. 1975. Floral biology of California buckeye. Madroño23:41–52.Google Scholar
  26. Berry, P. E. &R. N. Calvo. 1989. Wind pollination, self-incompatibility, and altitudinal shifts in pollination systems in the high Andean genusEspeletia (Asteraceae). Amer. J. Bot.76:1602–1614.Google Scholar
  27. ——. 1991. Pollinator limitation and position dependent fruit set in the high Andean orchidMyrosmodes cochleare (Orchidaceae). Pl. Syst. Evol.174:93–101.Google Scholar
  28. Bertin, R. I. 1982a. Floral biology, hummingbird pollination and fruit production of trumpet creeper (Campsis radicans, Bignoniaceae). Amer. J. Bot.69:122–134.Google Scholar
  29. —. 1982b. The ecology of sex expression in red buckeye. Ecology63:445–456.Google Scholar
  30. — 1988. Paternity in plants. Pages 30–59in J. Lovett Doust and L. Lovett Doust, (eds.), Plant Reproductive Ecology: Patterns and Strategies. Oxford Univ. Press, Oxford.Google Scholar
  31. — &O. D. V. Sholes. 1993. Weather, pollination and the phenology ofGeranium maculatum. Amer. Midl. Naturalist129:52–66.Google Scholar
  32. Bierzychudek, P. 1981. Pollinator limitation of plant reproductive effort. Amer. Naturalist117:838–840.Google Scholar
  33. Bosch, J. 1992. Floral biology and pollinators of three co-occurringCistus species (Cistaceae). Bot. J. Linn. Soc.109:39–55.Google Scholar
  34. Broyles, S. B. &R. Wyatt. 1990. Paternity analysis in a natural population ofAsclepias exaltata: multiple paternity, functional gender, and the “pollen-donation hypothesis.” Evolution44:1454–1468.Google Scholar
  35. —. 1991. The breeding system ofZephyranthes atamasco (Amaryllidaceae). Bull. Torrey Bot. Club118:137–140.Google Scholar
  36. Burd, M. 1994. Ovule packaging in stochastic pollination and fertilization environments. Evolution (in press).Google Scholar
  37. — &G. Head. 1992. Phenological aspects of male and female function in hermaphroditic plants. Amer. Naturalist140:305–324.Google Scholar
  38. Calvo, R. N. 1990. Four-year growth and reproduction ofCyclopogon cranichoides (Orchidaceae) in South Florida. Amer. J. Bot.77:736–741.Google Scholar
  39. —. 1993. Evolutionary demography of orchids: intensity and frequency of pollination and the cost of fruiting. Ecology74:1033–1042.Google Scholar
  40. Campbell, D. R. 1985. Pollinator sharing and seed set of Stellariapubera: competition for pollination. Ecology66:544–553.Google Scholar
  41. —. 1991. Effects of floral traits on sequential components of fitness inIpomopsis aggregata. Amer. Naturalist137:713–737.Google Scholar
  42. — &K. J. Halama. 1993. Resource and pollen limitation to lifetime seed production in a natural plant population. Ecology74:1043–1051.Google Scholar
  43. —,N. M. Waser, M. V. Price, E. A. Lynch &R. J. Mitchell. 1991. Components of phenotypic selection: pollen export and flower corolla width inIpomopsis aggregata. Evolution45:1458–1467.Google Scholar
  44. Carr, D. E. 1991. Sexual dimorphism and fruit production in a dioecious understory tree,Ilex opaca.Oecologia 85:381–388.Google Scholar
  45. —,E. A. Powell &D. W. Kyhos. 1986. Self-incompatibility in the Hawaiian Madiinae (Compositae): an exception to Baker’s rule. Evolution40:430–434.Google Scholar
  46. Casper, B. B. 1983. The efficiency of pollen transfer and rates of embryo initiation inCryptantha (Boraginaceae). Oecologia59:262–268.Google Scholar
  47. Charlesworth, D. 1989. Evolution of low female fertility in plants: pollen limitation, resource allocation, and genetic load. Trends Ecol. Evol.4:289–292.Google Scholar
  48. — &B. Charlesworth. 1987. The effect of investment in attractive structures on allocation to male and female functions in plants. Evolution41:948–968.Google Scholar
  49. Charnov, E. L. 1979. Simultaneous hermaphroditism and sexual selection. Proc. Natl. Acad. Sci. U.S.A.76:2480–2484PubMedGoogle Scholar
  50. — &J. J. Bull. 1986. Sex allocation, pollinator attraction and fruit dispersal in cosexual plants. J. Theor. Biol.118:321–325.Google Scholar
  51. Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton Univ. Press, Princeton.Google Scholar
  52. Cohen, D. &R. Dukas. 1990. The optimal number of female flowers and the fruits-to-flowers ratio in plants under pollination and resources limitation. Amer. Naturalist135:218–241.Google Scholar
  53. Cole, F. R. &D. H. Firmage. 1984. The floral ecology ofPlantanthera blephariglottis. Amer. J. Bot.71:700–710.Google Scholar
  54. Copland, B. J. &R. J. Whelan. 1989. Seasonal variation in flowering intensity and pollination limitation of fruit set in four co-occurringBanksia species. J. Ecol.77:509–526.Google Scholar
  55. Crome, F. H. J. &A. K. Irvine. 1986. “Two bob each way”: the pollination and breeding system of the Australian rain forest treeSyzygium cormiflorum (Myrtaceae). Biotropica18:115–125.Google Scholar
  56. Cruzan, M. B. 1990. Pollen-pollen and pollen-style interactions during pollen tube growth inErythronium grandiflorum (Liliaceae). Amer. J. Bot.77:116–122.Google Scholar
  57. —,P. R. Neal &M. F. Willson. 1988. Floral display inPhyla incisa: consequences for male and female reproductive success. Evolution42:505–515.Google Scholar
  58. De Oliveira, P. E. A. M. &M. Sazima. 1990. Pollination biology of two species ofKielmeyera (Guttiferae) from Brazilian cerrado vegetation. Pl. Syst. Evol.172:35–49.Google Scholar
  59. Delph, L. F. &C. M. Lively. 1992. Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos63:161–170.Google Scholar
  60. Devlin, B. &A. G. Stephenson. 1987. Sexual variations among plants of a perfect-flowered species. Amer. Naturalist130:199–218.Google Scholar
  61. Dickinson, T. A. &J. B. Phipps. 1986. Studies inCrataegus (Rosaceae: Maloideae) XIV. The breeding system ofCrataegus crus-galli sensu lato in Ontario. Amer. J. Bot.73:116–130.Google Scholar
  62. Dieringer, G. 1992. Pollinator limitation in populations ofAgalinis strictifolia (Scrophulariaceae). Bull. Torrey Bot. Club119:131–136.Google Scholar
  63. Dole, J. &K. Ritland. 1993. Inbreeding depression in twoMimulus taxa measured by multigenerational changes in the inbreeding coefficient. Evolution47:361–373.Google Scholar
  64. Dudash, M. R. 1993. Variation in pollen limitation among individuals ofSabatia angularis (Gentianaceae). Ecology74:959–962.Google Scholar
  65. Dulberger, R., A. Levy &D. Palevitch. 1981. Andromonoecy inSolanum marginatum. Bot. Gaz.142:259–266.Google Scholar
  66. Ehrlén, J. 1992. Proximate limits to seed production in a herbaceous perennial legume,Lathyrus vernus. Ecology73:1820–1831.Google Scholar
  67. Elam, D. R. &Y. B. Linhart. 1988. Pollination and seed production inIpomopsis aggregata: differences among and within flower color morphs. Amer. J. Bot.75:1262–1274.Google Scholar
  68. Eriksson, O.1987. Regulation of seed-set and gender variation in the hermaphroditic plantPotentilla anserina. Oikos49:165–171.Google Scholar
  69. Feil, J. P. 1992. Reproductive ecology of dioeciousSiparuna (Monimiaceae) in Ecuador—a case of gall midge pollination. Bot. J. Linn. Soc.110:171–203.Google Scholar
  70. Feinsinger, P. 1983. Coevolution and pollination. Pages 282–310in D. J. Futuyma and M. Slatkin (eds.), Coevolution. Sinauer, Sunderland, Mass.Google Scholar
  71. —,G. Murray, S. Kinsman &W. H. Busby. 1986. Floral neighborhood and pollination success in four hummingbird-pollinated cloud forest species. Ecology67:449–464.Google Scholar
  72. Firmage, D. H. &F. R. Cole. 1988. Reproductive success and inflorescence size ofCalopogon tuberosus (Orchidaceae). Amer. J. Bot.75:1371–1377.Google Scholar
  73. Flanagan, L. B. &W. Moser. 1985. Flowering phenology, floral display and reproductive success in dioeciousAralia nudicaulis L. (Araliaceae). Oecologia68:23–28.Google Scholar
  74. Fox, J. F. 1992. Pollen limitation of reproductive effort in willows. Oecologia90:283–287.Google Scholar
  75. Frankie, G. W., P. A. Opler &K. J. Bawa. 1976. Foraging behavior of solitary bees: implications for outcrossing of a neotropical forest tree species. J. Ecol.64:1049–1057.Google Scholar
  76. Galen, C. 1985. Regulation of seed-set inPolemonium viscosum: floral scents, pollination, and resources. Ecology66:792–797.Google Scholar
  77. — &M. L. Stanton. 1989. Bumble bee pollination and floral morphology: factors influencing pollen dispersal in the alpine sky pilot,Polemonium viscosum. Amer. J. Bot.76:419–426.Google Scholar
  78. Ganders, F. R. 1975. Fecundity in distylous and self-incompatible homostylous plants ofMitchella repens (Rubiaceae). Evolution29:186–189.Google Scholar
  79. Garwood, N. C. &C. C. Horvitz. 1985. Factors limiting fruit and seed production of a temperate shrub,Staphylea trifolia L. (Staphyleaceae). Amer. J. Bot.72:453–466.Google Scholar
  80. Geber, M. A. 1985. The relationship of plant size to self-pollination inMertensia ciliata. Ecology66:762–772.Google Scholar
  81. Goldingay, R. L. &R. J. Whelan. 1990. Breeding system and tests for pollen limitation in two species ofBanksia. Austral. J. Bot.38:63–71.Google Scholar
  82. Gorchov, D. L. 1988. Effects of pollen and resources on seed number and other fitness components inAmelanchier arborea (Rosaceae: Maloideae). Amer. J. Bot.75:1275–1285.Google Scholar
  83. Gross, R. S. &P. A. Werner. 1983. Relationships among flowering phenology, insect visitors, and seed set of individuals: experimental studies on four co-occurring species of goldenrod (Solidago: Compositae). Ecol. Monogr.53:95–117.Google Scholar
  84. Gwynne, D. T. 1991. Sexual competition among females: what causes courtship-role reversal? Trends Ecol. Evol.6:118–121.Google Scholar
  85. Haber, W. A. &G. W. Frankie. 1982. Pollination ofLuehea (Tiliaceae) in Costa Rican deciduous forest. Ecology63:1740–1750.Google Scholar
  86. Haig, D. &M. Westoby. 1988. On limits to seed production. Amer. Naturalist131:757–759.Google Scholar
  87. Hainsworth, F. R., L. L. Wolf &T. Mercier. 1985. Pollen limitation in a monocarpic species,Ipomopsis aggregata. J. Ecol.73:263–270.Google Scholar
  88. Hannan, G. L. 1981. Flower color polymorphism and pollination biology ofPlatystemon californicus Benth. (Papaveraceae). Amer. J. Bot.68:233–243.Google Scholar
  89. Harder, L. D. &J. D. Thomson. 1989. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Amer. Naturalist133:323–344.Google Scholar
  90. —,M. B. Cruzan &R. S. Unnasch. 1985. Sexual reproduction and variation in floral morphology in an ephemeral vernal lily,Erythronium americanum. Oecologia67:286–291.Google Scholar
  91. Heithaus, E. R., P. A. Opler &H. G. Baker. 1974. Bat activity and pollination of Bauhiniapauletia: plant-pollinator coevolution. Ecology55:412–419.Google Scholar
  92. Herrera, J. 1991. The reproductive biology of a riparian Mediterranean shrub,Nerium oleander L. (Apocynaceae). Bot. J. Linn. Soc.106:147–172.Google Scholar
  93. Hiirsalmi, H. 1969.Trientalis europaea L. A study of the reproductive biology, ecology and variation in Finland. Ann. Bot. Fennici6:119–173.Google Scholar
  94. Hoffman, M. T. 1992. Functional dioecy inEchinocereus coccineus (Cactaceae): breeding system, sex ratios, and geographic range of floral dimorphism. Amer. J. Bot.79:1382–1388.Google Scholar
  95. Hogan, K. P. 1983. The pollination biology and breeding system ofAplectrum hyemale (Orchidaceae). Canad. J. Bot.61:1906–1910.Google Scholar
  96. Holtsford, T. P. 1985. Nonfruiting hermaphroditic flowers ofCalochortus leichtlinii (Liliaceae): potential reproductive functions. Amer. J. Bot.72:1687–1694.Google Scholar
  97. Honig, M. A., H. P. Linder &W. J. Bond. 1992. Efficacy of wind pollination: pollen load size and natural microgametophyte populations in wind-pollinatedStaberoha banksii (Restionaceae). Amer. J. Bot.79:443–448.Google Scholar
  98. Horvitz, C. C. &D. W. Schemske. 1988. A test of the pollinator limitation hypothesis for a neotropical herb. Ecology69:200–206.Google Scholar
  99. Jain, S. K. 1976. The evolution of inbreeding in plants. Ann. Rev. Ecol. Syst.7:469–495.Google Scholar
  100. Janzen, D. H., P. de Vries, D. E. Gladstone, M. L. Higgins &T. M. Lewishon. 1980. Self and cross-pollination ofEncyclia cordigera (Orchidaceae) in Santa Rosa National Park, Costa Rica. Biotropica12:72–74.Google Scholar
  101. Jennersten, O. 1988. Pollination inDianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conservation Biol.2:359–366.Google Scholar
  102. —,L. Berg &C. Lehman. 1988. Physiological differences in pollinator visitation, pollen deposition and seed set in the sticky catchfly,Viscarla vulgaris. J. Ecol.76:1111–1132.Google Scholar
  103. Johnson, R. A. 1992. Pollination and reproductive ecology of acuña cactus,Echinomastus erectrocentrus var.acunensis (Cactaceae). Int. J. Plant Sci.153:400–408.Google Scholar
  104. Johnston, M. O. 1991. Pollen limitation of female reproduction inLobelia cardinalis andL. siphilitica. Ecology72:1500–1503.Google Scholar
  105. Karoly, K. 1992. Pollinator limitation in the facultatively autogamous annual,Lupinus nanus (Leguminosae). Amer. J. Bot.79:49–56.Google Scholar
  106. Kevan, P. G. 1972. Insect pollination of high arctic flowers. J. of Ecol.60:831–847.Google Scholar
  107. Kikuzawa, K. 1989. Floral biology and evolution of gynodioecism inDaphne kamtchatica var.jezoensis. Oikos56:196–202.Google Scholar
  108. — &N. Mizui. 1990. Flowering and fruiting phenology ofMagnolia hypoleuca. Pl. Spec. Biol.5:255–261.Google Scholar
  109. Kimata, M. 1978. Comparative studies on the reproductive systems ofMazus japonicus andM. miquelii (Scrophulariaceae). Pl. Syst. Evol.129:243–253.Google Scholar
  110. Koptur, S. 1984. Outcrossing and pollinator limitation of fruit set: breeding systems of neotropicalInga trees (Fabaceae: Mimosoideae). Evolution38:1130–1143.Google Scholar
  111. Kunin, W. E. 1992. Density and reproductive success in wild populations ofDiplotaxis erucoides (Brassicaceae). Oecologia91:129–133.Google Scholar
  112. Kwak, M. M. &O. Jennersten. 1986. The significance of pollination time and frequency and of purity of pollen loads for seed set inRhinanthus angustifolius (Scrophulariaceae) andViscaria vulgaris (Caryophyllaceae). Oecologia70:502–507.Google Scholar
  113. —. 1991. Bumblebee visitation and seed set inMelampyrum pratense andViscaria vulgaris: heterospecific pollen and pollen limitation. Oecologia86:99–104.Google Scholar
  114. Lawrence, W. S. 1993. Resource and pollen limitation: plant size-dependent reproductive patterns inPhysalis longifolia. Amer. Naturalist141:296–313.Google Scholar
  115. Lee, T. D. 1984. Effects of seed number per fruit on seed dispersal inCassia fasciculata (Caesalpinaceae). Bot. Gaz.145:136–139.Google Scholar
  116. —. 1989. Patterns of fruit and seed production in a Vermont population ofCassia nictitans L. (Caesalpinaceae). Bull. Torrey Bot. Club116:15–21.Google Scholar
  117. — &F. A. Bazzaz. 1982. Regulation of fruit and seed production in an annual legume,Cassia fasciculata. Ecology63:1363–1373.Google Scholar
  118. Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. Amer. Naturalist141:517–536.Google Scholar
  119. Lloyd, D. G. 1987. Allocations to pollen, seeds, and pollination mechanisms in self-fertilizing plants. Func. Ecol.1:83–89.Google Scholar
  120. — &D. L. Venable. 1992. Some properties of natural selection with single and multiple constraints. Theor. Populat. Biol.41:90–110.Google Scholar
  121. — &M. S. Wells. 1992. Reproductive biology of a primitive angiosperm,Pseudowintera colorata (Winteraceae), and the evolution of pollination systems in the Anthophyta. Pl. Syst. Evol.181:77–95.Google Scholar
  122. Lubbers, A. E. &N. L. Christensen. 1986. Intraseasonal variation in seed production among flowers and plants ofThalictrum thalictroides (Ranunculaceae). Amer. J. Bot.73:190–203.Google Scholar
  123. Manasse, R. S. &K. Pinney. 1991. Limits to reproductive success in a partially self-incompatible herb: fecundity depression at serial life-cycle stages. Evolution45:712–720.Google Scholar
  124. Mann, H. B. &D. R. Whitney. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat.18:50–60.Google Scholar
  125. Marshall, D. L. &N. C. Ellstrand. 1988. Effective mate choice in wild radish: evidence for selective seed abortion and its mechanism. Amer. Naturalist131:739–756.Google Scholar
  126. Maynard Smith, J. 1982. Evolution and the Theory of Games. Cambridge Univ. Press, Cambridge.Google Scholar
  127. Mazer, S. J., A. A. Snow &M. L. Stanton. 1986. Fertilization dynamics and parental effects upon fruit development inRaphanus raphanistrum: consequences for seed size variation. Amer. J. Bot.73:500–511.Google Scholar
  128. McCall, C. &R. B. Primack 1985. Effects of pollen and nitrogen availability on reproduction in a woodland herb,Lysimachiaquadrifolia. Oecologia67:403–410.Google Scholar
  129. —. 1987. Resources limit the fecundity of three woodland herbs. Oecologia71:431–435.Google Scholar
  130. McDade, L. A. 1983. Pollination intensity and seed set inTrichanthera gigantea (Acanthaceae). Biotropica15:122–124.Google Scholar
  131. — &P. Davidar. 1984. Determinants of frait and seed set inPavonia dasypetala (Malvaceae). Oecologia64:61–67.Google Scholar
  132. Mizui, N. &K. Kikuzawa. 1991. Proximate limitations to fruit and seed set inPhellodendron amurense var.sachalinense. Pl. Spec. Biol.6:39–46.Google Scholar
  133. Montalvo, A. M. &J. D. Ackerman. 1987. Limitations to fruit production inIonopsisutricularioides (Orchidaceae). Biotropica19:24–31.Google Scholar
  134. Morse, D. H. &R. S. Fritz. 1983. Contributions of diurnal and nocturnal insects to the pollination of common milkweed (Asclepias syriaca L.) in a pollen-limited system. Oecologia60:190–197.Google Scholar
  135. Motten, A. F. 1983. Reproduction ofErythronium umbilicatum (Liliaceae): pollination success and pollinator effectiveness. Oecologia59:351–359.Google Scholar
  136. —. 1986. Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol. Monogr.56:21–42.Google Scholar
  137. Murakami, N. &M. Maki. 1992. Sex allocation ratio in a wind-pollinated self-incompatible monoecious tree,Alnus firma Sieb. et Zucc. (Betulaceae). Pl. Spec. Biol.7:97–101.Google Scholar
  138. Murawski, D. A. 1987. Floral resource variation, pollinator response, and potential pollen flow inPsiguria warscewiczii. Ecology68:1273–1282.Google Scholar
  139. Murcia, C. 1990. Effect of floral morphology and temperature on pollen receipt and removal inIpomea trichocarpa. Ecology71:1098–1109.Google Scholar
  140. Nault A. &D. Gagnon. 1987. Some aspects of the pollination ecology of wild leek,Allium tricoccum Ait. Pl. Spec. Biol.2:127–132.Google Scholar
  141. Norman, E. M. &D. Clayton. 1986. Reproductive biology of two Florida pawpaws:Asimina obovata andA. pygmaea (Annonaceae). Bull. Torrey Bot. Club113:16–22.Google Scholar
  142. —,K. Rice &S. Cochran. 1992. Reproductive biology ofAsimina parviflora (Annonaceae). Bull. Torrey Bot. Club119:1–5.Google Scholar
  143. Ockendon, D. J. &L. Currah. 1977. Self-pollen reduces the number of cross-pollen tubes in the styles ofBrassica olemceae L. New Phytol.78:675–680.Google Scholar
  144. Ohara, M., S. Kawamo &F. H. Utech. 1990. Differentiation patterns of reproduction systems in the genusTrillium. Pl. Spec. Biol.5:73–81.Google Scholar
  145. Oliviera, P. E., P. E. Gibbs, A. A. Barbosa &S. Talavera. 1992. Contrasting breeding systems in twoEriotheca (Bombacaceae) species of the Brazilian cerrados. Pl. Syst. Evol.179:207–219.Google Scholar
  146. O’Neill, R. V. 1989. Perspectives in hierarchy and scale. Pages 140–156in J. Roughgarden, R. M. May, and S. A. Levin (eds.) Perspectives in Ecological Theory. Princeton Univ. Press, Princeton.Google Scholar
  147. Opler, P. A., H. G. Baker &G. W. Frankie. 1975. Reproductive biology of some Costa RicanCardia species (Boraginaceae). Biotropica7:234–247.Google Scholar
  148. Ornduff, R. 1971. The reproductive system ofJepsonia heterandra. Evolution25:300–311.Google Scholar
  149. Osborn, M. M., P. G. Kevan &M. A. Lane. 1988. Pollination biology ofOpuntia polyacantha andOpuntia phaeacantha (Cactaceae) in southern Colorado. Pl. Syst. Evol.159:85–94.Google Scholar
  150. Part, J. M., M. W. Merchant, D. R. E. Williams &B. J. D. Meeuse. 1989. Pollination biology ofPlatanthera stricta (Orchidaceae) in Olympic National Park, Washington. Amer. J. Bot.76:1097–1106.Google Scholar
  151. Petersen, C., J. H. Brown &A. Kodric-Brown. 1982. An experimental study of floral display and fruit set inChilopsis linearis (Bignoniaceae). Oecologia55:7–11.Google Scholar
  152. Pettersson, M. W. 1991. Pollination by a guild of fluctuating moth populations: option for unspecialization inSilene vulgaris. J. Ecol.79:591–604.Google Scholar
  153. Pleasants, J. M. &S. J. Chaplin. 1983. Nectar production rates ofAsclepias quadrifolia: causes and consequences of individual variation. Oecologia59:232–238.Google Scholar
  154. Primack, R. B. &P. Hall. 1990. Costs of reproduction in the Pink Lady’s Slipper orchid: a four-year experimental study. Amer. Naturalist136:638–656.Google Scholar
  155. — &D. G. Lloyd. 1980. Andromonoecy in the New Zealand shrub,Leptospermum scoparium (Myrtaceae). Amer. J. Bot.67:361–368.Google Scholar
  156. Queller, D. C. 1983 Sexual selection in a hermaphroditic plant. Nature305:706–707Google Scholar
  157. —. 1987. Sexual selection in flowering plants. Pages 165–179in J. W. Bradbury and M. B. Andersson, (eds.), Sexual Selection: Testing the Alternatives. John Wiley & Sons, Chichester.Google Scholar
  158. Ramirez, N. &Y. Brito. 1990. Reproductive biology of a tropical palm swamp community in the Venezuelan llanos. Amer. J. Bot.77:1260–1271.Google Scholar
  159. Ramsey, M., N. Prakash &S. Cairns. 1993. Breeding systems of disjunct populations of Christmas Bells (Blandfordia grandiflora R.Br., Liliaceae): variation in self-fertility and an ovular mechanism regulating self-fertilisation. Austral. J. Bot.41:35–47.Google Scholar
  160. Rathcke, B. 1988. Interactions for pollinations among coflowering shrubs. Ecology69:446–457.Google Scholar
  161. Real, L. A. &B. J. Rathcke. 1991. Individual variation in nectar production and its effects on fitness inKalmia latifolia. Ecology72:149–155.Google Scholar
  162. Robertson, J. L. &R. Wyatt. 1990. Reproductive biology of the yellow finged orchid,Platanthera ciliaris. Amer. J. Bot.77:388–398.Google Scholar
  163. Rocha, O. J. &A. G. Stephenson. 1991. Effects of nonrandom seed abortion on progeny performance inPhaseolus coccineus L. Evolution45:1198–1208.Google Scholar
  164. Rodríguez-Robles, J. A., E. J. Meléndez &J. D. Ackerman. 1992. Effects of display size, flowering phenology, and nectar availability on effective visitation frequency inComparattia falcata (Orchidaceae). Amer. J. Bot.79:1009–1017.Google Scholar
  165. Rust, R. W. 1977. Pollinator service in sympatric species of jewel weed (Impatiens: Balsaminaceae). J. New York Ent. Soc.85:234–239.Google Scholar
  166. Schemske, D. W. 1980. Evolution of floral display in the orchidBrassavola nodosa. Evolution34:489–493.Google Scholar
  167. —. 1983. Breeding system and habitat effects on fitness components in three neotropicalCostus (Zingiberaceae). Evolution37:523–539.Google Scholar
  168. Schlessman, M. A. 1985. Floral biology of American ginseng (Panax quinquefolium). Bull. Torrey Bot. Club112:129–133.Google Scholar
  169. Schlising, R. A. 1976. Reproductive proficiency inPaennia californica (Paeoniaceae). Amer. J. Bot.63:1095–1103.Google Scholar
  170. Schneider, E. L. &D. M. Nichols. 1984. Floral biology ofArgemone aurantiaca (Papaveraceae). Bull. Torrey Bot. Club111:1–7.Google Scholar
  171. Schoen, D. J. 1977. Floral biology ofDiervilla lonicera (Caprifoliaceae). Bull. Torrey Bot. Club104:234–240.Google Scholar
  172. Shore, J. S. &S. C. H. Barrett. 1984. The effect of pollination intensity and incompatible pollen on seed set inTumera ulmifolia (Turneraceae). Canad. J. Bot.62:1298–1303.Google Scholar
  173. Sih, A. &M.-S. Baltus. 1987. Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology68:1679–1690.Google Scholar
  174. Simpson, B. B., J. L. Neff &G. Dieringer. 1986. Reproductive biology ofTinantia anomala (Commelinaceae). Bull. Torrey Bot. Club113:149–158.Google Scholar
  175. Snow, A. A. 1982. Pollination intensity and potential seed set inPassiflora vitifolia. Oecologia55:231–237.Google Scholar
  176. —. 1986. Pollination dynamics inEpilobium canum (Onagraceae): consequences for gametophytic selection. Amer. J. Bot.73:139–151.Google Scholar
  177. — &S. J. Mazer. 1988. Gameophytic selection inRaphanus raphanistrum: a test for heritable variation in pollen competitive ability. Evolution42:1065–1075.Google Scholar
  178. — &D. W. Roubik. 1987. Pollen deposition and removal by bees visiting two tree species in Panama. Biotropica19:57–63.Google Scholar
  179. — &T. P. Spira. 1991. Differential pollen-tube growth rates and nonrandom fertilization inHibiscus moscheutos (Malvaceae). Amer. J. Bot.78:1419–1426.Google Scholar
  180. — &D. F. Whigham. 1989. Costs of flower and fruit production inTipularia discolor (Orchidaceae). Ecology70:1286–1293.Google Scholar
  181. Sork, V. L. &D. W. Schemske. 1992. Fitness consequences of mixed-donor pollen loads in the annual legumeChamaecrista fasciculata. Amer. J. Bot.79:508–515.Google Scholar
  182. Southwick, E. E. 1984. Photosynthate allocation to floral nectar: a neglected energy investment. Ecology65:1775–1779.Google Scholar
  183. Spears, E. E. 1987. Island and mainland pollination ecology ofCentrosema virginianum andOpuntia stricla. J.Ecol.75:351–362.Google Scholar
  184. Stanton, M. L. 1987. Reproductive biology of petal color variants in wild populations ofRaphanus sativus. 2. Factors limiting seed production. Amer. J. Bot.74:188–196.Google Scholar
  185. — &R. E. Preston. 1988a. Ecological consequences and phenotypic correlates of petal size variation in wild radish,Raphanus sativus (Brassicaceae). Amer. J. Bot.75:528–539.Google Scholar
  186. —. 1988b. A qualitative model for evaluating the effects of flower attractiveness on male and female fitness in plants. Amer. J. Bot.75:540–544.Google Scholar
  187. Stanton, M. L., A. A. Snow &S. N. Handel. 1986. Floral evolution: attractiveness to pollinators increases male fitness. Science232:1625–1627.PubMedGoogle Scholar
  188. Stebbins, G. L. 1957. Self-fertilization and population variability in the higher plants. Amer. Naturalist91:337–354.Google Scholar
  189. Steel, R. G. D. &J. H. Torrie. 1960. Principles and Procedures of Statistics. McGraw Hill, New York.Google Scholar
  190. Stephenson, A. G. 1979. An evolutionary examination of the floral display ofCatalpa speciosa (Bignoniaceae). Evolution33:1200–1209.Google Scholar
  191. —. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Ann. Rev. Ecol. Syst.12:253–279.Google Scholar
  192. — &J. A. Winsor. 1986.Lotus corniculatus regulates offspring quality through selective fruit abortion. Evolution40:453–458.Google Scholar
  193. Stevens, D. P. 1988. On the gynodioecious polymorphism inSaxifraga granulata L. (Saxifragaceae). Biol. J. Linn. Soc.35:15–28.Google Scholar
  194. Sugawara, T. 1988. Floral biology ofHeterotropa tamaensis (Aristolochiaceae) in Japan. Pl. Spec. Biol.3:7–12.Google Scholar
  195. Sutherland, S. 1987. Why hermaphroditic plants produce many more flowers than fruits: an experimental test withAgave mckelveyana. Evolution41:750–759.Google Scholar
  196. — &L. F. Delph. 1984. On the importance of male fitness in plants: patterns of fruit-set. Ecology65:1093–1104.Google Scholar
  197. Swanson, S. D. &S. H. Sohmer. 1976. The biology ofPodophyllum peltatum L. (Berberidaceae), the may apple. II. The transfer of pollen and success of sexual reproduction. Bull. Torrey Bot. Club103:223–226.Google Scholar
  198. Takahashi, H. 1984. The floral biology ofTricyrtis latifolia Maxim. (Liliaceae). Bot. Mag. (Tokyo)97:207–217.Google Scholar
  199. —. 1987. A comparative floral and pollination biology ofTricyrtis flava Maxim.,T. nana Yatabe andT. ohsumiensis Masamune (Liliaceae). Bot. Mag. (Tokyo)100:185–203.Google Scholar
  200. —. 1989. The floral biology ofTricyrtis affinis Makimo (Liliaceae). Pl. Spec. Biol.4:61–68.Google Scholar
  201. Threadgill, P. F., J. M. Baskin &C. C. Baskin. 1981. The floral ecology ofFrasera caroliniensis (Gentianaceae). Bull. Torrey Bot. Club108:25–33.Google Scholar
  202. Travis, J. 1984. Breeding system, pollination, and pollinator limitation in a perennial herb,Amianthum muscaetoxicum (Lilliaceae). Amer. J. Bot.71:941–947.Google Scholar
  203. Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136–179in B. Campbell (ed.), Sexual Selection and the Descent of Man 1871–1971. Aldine, Chicago.Google Scholar
  204. Vogel, S. &I. C. Machado. 1991. Pollination of four sympatric species ofAngelonia (Scrophulariaceae) by oil-collecting bees in NE. Brazil. Pl. Syst. Evol.178:153–178.Google Scholar
  205. Walsh, N. E. &D. Charlesworth. 1992. Evolutionary interpretations of differences in pollen tube growth rates. Quart. Rev. Biol.67:19–37.Google Scholar
  206. Waser, N. M. 1983. The adaptive nature of floral traits: ideas and evidence. Pages 241–285in L. Real (ed.), Pollination Biology. Academic Press, N.Y.Google Scholar
  207. Weiler, S. G. 1980. Pollen flow and fecundity in populations ofLithospermum caroliniense. Amer. J. Bot.67:1334–1341.Google Scholar
  208. Whelan, R. J. &R. L. Goldingay. 1989. Factors affecting fruit-set inTelopea speciosissima (Proteaceae): the importance of pollen limitation. J. Ecol.77:1123–1134.Google Scholar
  209. Whisler, S. L. &A. A. Snow. 1992. Potential for the loss of self-incompatibility in pollen-limited populations of mayapple (Podophyllum peltatum). Amer. J. Bot.79:1273–1278.Google Scholar
  210. Wiens, D. 1984. Ovule survivorship, broodsize, life history, breeding systems, and reproductive success in plants. Oecologia64:47–53.Google Scholar
  211. —,C. L. Calvin, C. A. Wilson, C. I. Davern, D. Frank &S. R. Seavey. 1987. Reproductive success, spontaneous embryo abortion, and genetic load in flowering plants. Oecologia71:501–509.Google Scholar
  212. —,D. L. Nickrent, C. I. Davern, C. L. Calvin &N. J. Vivrette. 1989. Developmental failure and loss of reproductive capacity in the rare paleoendemic shrubDedeckera eurekensis. Nature338:65–67.Google Scholar
  213. Willson, M. F. 1979. Sexual selection in plants. Amer. Naturalist113:777–790.Google Scholar
  214. —. 1990. Sexual selection in plants and animals. Trends Ecol. Evol.5:210–214.Google Scholar
  215. — &N. Burley. 1983. Mate Choice in Plants. Princeton Univ. Press, Princeton.Google Scholar
  216. — &P. W. Price. 1977. The evolution of inflorescence size inAsclepias (Asclepiadaceae). Evolution31:495–511Google Scholar
  217. — &D. W. Schemske. 1980. Pollinator limitation, fruit production, and floral display in pawpaw (Asimina triloba). Bull. Torrey Bot. Club107:401–408.Google Scholar
  218. Wilson, P., J. D. Thomson, M. L. Stanton & L. P. Rigney. 1994. Beyond floral Batemania: gender biases in selection for pollination sucess. Amer. Naturalist (in press).Google Scholar
  219. Worthen, W. B. &E. W. Stiles. 1988. Pollen-limited fruit set in isolated patches ofMaianthemum canadense Desf. in New Jersey. Bull. Torrey Bot. Club115:299–305.Google Scholar
  220. Wyatt, R. 1982. Inflorescence architecture: how flower number, arrangement, and phenology affect pollination and fruit set. Amer. J. Bot.69:585–594.Google Scholar
  221. — &R. L. Hellwig. 1979. Factors determining fruit set in heterostylous bluets,Houstonia caerulea (Rubiaceae). Syst. Bot.4:103–114.Google Scholar
  222. Young, H. J. 1986. Beetle pollination ofDiffenbachia longispatha (Araceae). Amer. J. Bot.73:931–994.Google Scholar
  223. — &M. L. Stanton. 1990. Influences of floral variation on pollen removal and seed production in wild radish. Ecology71:536–547.Google Scholar
  224. — &T. P. Young 1992. Alternative outcomes of natural and experimental high pollen loads. Ecology73:639–647.Google Scholar
  225. Young, T. P. 1982. Bird visitation, seed-set, and germination rates in two species ofLobelia on Mount Kenya. Ecology63:1983–1986.Google Scholar
  226. Zimmerman, J. K. &T. M. Aide. 1989. Patterns of fruit production in a neotropical orchid: pollinator vs. resource limitation. Amer. J. Bot.76:67–73.Google Scholar
  227. Zimmerman, M. &G. H. Pyke. 1988. Reproduction inPolemonium: assessing the factors limiting seed set. Amer. Naturalist131:723–738.Google Scholar

Copyright information

© The New York Botanical Garden 1994

Authors and Affiliations

  • Martin Burd
    • 1
  1. 1.Department of BotanyUniversity of WisconsinMadisonUSA

Personalised recommendations