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Reproductive Biology |
2Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland; 3Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014 Oulu, Finland
Received for publication October 13, 2003. Accepted for publication October 22, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Geraniaceae • Geranium sylvaticum • gynodioecy • pollen limitation • resource limitation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Stephenson, 1981
; Sutherland and Delph, 1984
). Several hypotheses have been presented to explain this common phenomenon, including resource and pollen limitation (Sutherland, 1986
, 1987
; Burd, 1995
, 1998
; and references therein). A plant is considered pollen limited if additional pollen increases fruit or seed production (Schemske, 1980
; Willson and Schemske, 1980
; Bierzychudek, 1981
; Burd, 1994
; Larson and Barrett, 2000
), whereas a plant receiving sufficient pollen is considered resource limited if the addition of resources increases fruit or seed production (Zimmerman and Aide, 1989
). However, pollen and resource limitation are not necessarily mutually exclusive phenomena and both may lead to low reproductive output.
In gynodioecious plant populations where females and hermaphrodites coexist, hermaphrodites function as pollen donors, and thus the reproductive output of females depends on pollen production by the hermaphrodites. In general, in species with gender polymorphism pollen limitation can be caused by at least three factors. First, the amount of pollen produced is affected by the proportion of pollen-producing plants in the population (Lewis, 1941
; Levin and Kerster, 1974
; Widén and Widén, 1990
). In natural populations, most of the pollen flow occurs between very close neighbors (Levin and Kerster, 1974
). When hermaphrodites are locally rare, the reproductive success of both genders decreases as a response to changes in neighborhood sex ratio, indicating that both females and hermaphrodites are sensitive to low pollen availability (Graff, 1999
). Consequently, pollen limitation is expected to become more likely when the frequency of females increases in gynodioecious populations (Lewis, 1941
). Such frequency-dependent female reproductive output has indeed been observed in experimental studies of the gynodioecious Silene vulgaris (McCauley and Brock, 1998
) and gynodioecious Fragaria virginiana (Ashman and Diefenderfer, 2001
). Second, selective foraging of pollinators on either of the morphs may limit reproductive success in sexually dimorphic plant species (Bell, 1985
; Ashman and Stanton, 1991
; Eckhart, 1991
; Delph and Lively, 1992
; Ashman, 2000
; Ashman et al., 2000
). Plant size, flower size, and the number of flowers influence the frequency of pollinator visits and hence reproductive output (Willson and Rathcke, 1974
; Willson and Price, 1977
). In gynodioecious populations, reproductive success of female plants may be reduced compared to hermaphrodites if the generally larger flowers of hermaphrodites are more attractive to pollinators (e.g., Darwin, 1877
; Baker, 1948
; Delph, 1996
). Third, an overall shortage of pollinators limits reproductive success of both females and hermaphrodites. For example, yearly variation in temperature and precipitation during a flowering season may affect pollinator abundance and activity and lead to variation in plant reproductive success (Dudash and Fenster, 1997
).
If reproductive output of an individual plant does not increase after supplemental hand-pollination, the plant is assumed to be limited by resource availability. Several studies have obtained evidence for resource limitation of seed production in wild plants (e.g., Willson and Price, 1980
; Whigham, 1984
; Delph, 1986
; Zimmerman and Aide, 1989
). In many gynodioecious species, hermaphrodites produce significantly more and larger flowers, and both seeds and pollen, while females save resources at the time of flowering by producing fewer and smaller flowers without pollen (e.g., Darwin, 1877
; Baker, 1948
; Delph, 1996
; Ashman, 2000
), although females may overall allocate more resources to reproduction if their seed set is higher than that of hermaphrodites. Thus, reproductive output should be more resource limited in the sex morph that allocates relatively more resources to reproduction. Eckhart and Chapin (1997)
compared resource limitation of seed production between female and hermaphroditic plants in the gynodioecious species Phacelia linearis; they did not find significant differences in fruit or seed production between females and hermaphrodites in response to addition of nutrients. However, they found substantial evidence of sex-differential nutrient sensitivity of plant allocation, with females being superior to hermaphrodites in low-nutrient conditions. Poot (1997)
also found a similar trend of sex-differential nitrogen use: in Plantago lanceolata, female plants grew better and had higher reproductive output than hermaphrodites in nitrogen-limited conditions. Correspondingly, we have found a negative correlation between population female frequency and soil nitrogen concentration in Geranium sylvaticum (Asikainen and Mutikainen, unpublished data).
The sex ratio of gynodioecious plant populations is affected by genetic and ecological factors (Lloyd, 1976
; Charlesworth, 1981
; Frank, 1989
; Delph, 2003
). Genetic control of sex theoretically sets the limits for variation in population female frequency (Lewis, 1941
; Lloyd, 1976
; Charlesworth, 1981
), and the sex ratio of a particular population is affected by the seed production of females relative to that of hermaphrodites (e.g., Charlesworth, 1981
; McCauley and Taylor, 1997
; Delph and Carroll, 2001
; Asikainen and Mutikainen, 2003
). Any ecological factor that affects the relative fitness of females and hermaphrodites may influence population sex ratio and further the maintenance of females in gynodioecious populations (Lewis, 1941
; Lloyd, 1974
; Maurice and Fleming, 1995
). The availability of pollen and resources is likely to have differential effects on the reproductive output of females and hermaphrodites (Maurice and Fleming, 1995
). If hermaphrodites of a gynodioecious species are self-compatible and if self-pollination does not require a pollinator, females are predicted to be more susceptible to pollen limitation because they must outcross (Maurice and Fleming, 1995
). In three species fulfilling these conditions and in accordance with this prediction, females were more pollen limited than hermaphrodites (Widén, 1992
; Fleming et al., 1994
; Ramsey and Vaughton, 2002
). On the other hand, the fruit set of female plants of gynodioecious Hebe stricta was not significantly limited by pollen availability (Delph and Lively, 1992
).
In our study species, gynodioecious Geranium sylvaticum, female frequency varies from almost zero to 27% among populations (Vaarama and Jääskeläinen, 1967
; Asikainen and Mutikainen, 2003
). In most of the populations, females produced more seeds per flower than hermaphrodites; however, the relative seed fitness differed significantly among the populations (Asikainen and Mutikainen, 2003
). Here, we examined if part of the among-population variation in relative female fitness is caused by variation in pollen or resource limitation among the populations and between the sexes and if pollen limitation does affect population female frequency (Maurice and Fleming, 1995
). First, we experimentally examined the effects of supplemental hand-pollination on the reproductive output of both females and hermaphrodites in three natural populations of G. sylvaticum for two successive years. Since the perfect flowers of G. sylvaticum are self-compatible (personal observation) and since hermaphrodites have slightly more flowers and larger petals than females (Vaarama and Jääskeläinen, 1967
; Asikainen and Mutikainen, 2003
and unpublished data), we expected females to be more pollen limited than hermaphrodites. Second, to examine the interaction between population sex ratio and the level of pollen limitation, we estimated pollen limitation in five populations that differ by their sex ratio. If female plants are pollen limited and if pollen limitation depends on the frequency of the pollen-producing hermaphrodites, pollen limitation may limit female frequency within population. Finally, we studied the effects of pollen and fertilizer addition on the reproductive output of females and hermaphrodites in three populations.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Intermediate sexual forms and individuals bearing both perfect and pistillate flowers have also been found in several populations at low frequency (Vaarama and Jääskeläinen, 1967
; Asikainen and Mutikainen, 2003
). Geranium sylvaticum flowers in the beginning of June in southern Finland. Flowering lasts more than 3 wk in our study populations (Asikainen and Mutikainen, unpublished data). An individual plant bears from a few to several hundred flowers (Asikainen and Mutikainen, 2003
). However, only a few flowers are open simultaneously. The perfect flowers are protandrous and pollen is produced before the stigmas are receptive to pollen. The primary pollinators are bumblebees, syrphid flies, and other dipterans. There are 10 ovules in each flower (personal observation). The fruit of G. sylvaticum has five parts. Each fruit contains usually less than five seeds, but as many as seven seeds have been found within a fruit (personal observation). The fruits mature in July in southern Finland.
We selected five populations that differ by their habitat and sex ratio for the experimental manipulations (Table 1). The female frequencies in particular populations have remained quite stable both in the short term (1–2 yr; Asikainen and Mutikainen, unpublished data) and in the long term (40 yr; Vaarama and Jääskeläinen, 1967
; Asikainen and Mutikainen, 2003
).
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In 2002, we extended the pollen limitation experiment into two new populations (Ruissalo and Seili II). These two new populations were experimentally manipulated as described. The addition of these two new populations allowed us to more reliably examine the variation in the degree of pollen limitation among the populations in the second study year. The data on fruit set, seed set, and the number of seeds produced in this experiment were analyzed as described before, excluding the effect of year.
Population sex ratio and pollen limitation
Using the five populations, we examined if the level of pollen limitation is related to female frequency by calculating Spearman's correlation coefficients between population female frequency and level of pollen limitation of females. We calculated the level of pollen limitation as L = 1 – (Po/Ps), where Po is the number of seeds produced by open-pollinated female plants, and Ps is the number seeds produced by the hand-pollinated female plants in each population (Larson and Barrett, 2000
). Thus, the higher the value of L, the more pollen limited the female plants are.
Resource and pollen limitation
To examine whether seed production of G. sylvaticum is resource and/or pollen limited, we marked 60 haphazardly chosen females and 60 hermaphrodites in each of three study populations (Katariinanlaakso, Paimio, and Seili I). Our factorial design had two fixed factors, pollination and fertilization, each with two levels. Fertilization was chosen as a resource because seed production is generally limited by soil nutrients (e.g., Ayre and Whelan, 1989
). Furthermore, we expected that the study plants were not limited by water because the study populations are located in moist meadows or in moist deciduous forest habitats. In each population, we started the fertilization treatment just after the first flowers had opened. In each population, plants assigned to the fertilization treatment received a combination of 16 : 4 : 25 NPK and 0 : 18 : 25 NPK fertilizers (NutriSI) every sixth day at the manufacturer's recommended dosage (both 2 mL/L) in 250 mL of water per plant. We continued the fertilization treatment throughout the flowering period until the fruits started to mature. Hand-pollination and seed collection were carried out as described. Twenty randomly selected seeds per plant were weighed to the nearest 0.01 mg. The data on fruit set, seed set, the number of seeds produced per plant, and seed mass were analyzed using ANOVA with plant sex, pollination treatment (hand-pollination/open-pollination), fertilization treatment (fertilized/nonfertilized), and population as fixed factors.
Fruit set, seed set, and the number of seeds produced were log-normally transformed to meet the assumptions of ANOVA. The means and standard errors presented in the figures are back-transformed values. Because the sex of each plant was determined from a few first-to-open flowers, we excluded those plants that turned out to be intermediate or had both perfect and pistillate flowers. Further, we had to exclude some plants because they were lost or partly eaten. Overall, 44–50 plants from the analysis of pollen limitation experiment and 39–45 plants from the analysis of resource and pollen limitation experiment were excluded for these reasons.
Note that the same individual plants were used in both 2001 and 2002 as the control plants (i.e., open-pollination treatment). Hand-pollinated plants used in 2002 were different from those used in 2001 to avoid the effect of hand-pollination on the reproductive output in 2002. The fact that the control plants were the same in the two study years could be corrected by dividing the P values by two, i.e., the critical P value at the P = 0.05 significance level would be 0.025. Note that this correction would not change the interpretation of our results; P values that are significant at the P < 0.05 level (except those for the interactions between population and pollination for fruit set, between sex and year, and between population, pollination, and year for seed set; see Table 2) are also significant at the P < 0.025 level. All statistical tests were performed with SPSS statistical software (Norusis, 1990
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Population sex ratio and pollen limitation
The degree of pollen limitation for fruit set, seed set, and the number of seeds produced differed among the five study populations (fruit set: population x pollination: F4,283 = 3.233, P = 0.013; seed set: population x pollination: F4,278 = 3.388, P = 0.010; the number of seeds produced: population x pollination: F4,277 = 2.501, P = 0.043). Population female frequency and relative pollen limitation (L) in females did not correlate significantly (Spearman's r = –0.60, P = 0.285, N = 5, two-tailed test). Note that the direction of the correlation is even opposite to our expectation. Thus, even though the number of populations was rather low, this result suggests that the level of pollen limitation in females does not depend on the proportion of the pollen-producing hermaphrodites.
Resource and pollen limitation
On average, both supplemental hand-pollination and fertilization during the flowering season increased fruit set (by 28 and 32%, respectively) in G. sylvaticum (Table 3, Fig. 2). Seed set (by 29%) and the number of seeds produced (by 72%) increased only with fertilization (Table 3, Fig. 2). The differences between sexes and among populations were also significant for all these traits (Table 3). Interestingly, the effect of fertilization on the number of seeds produced varied among the study populations (Table 3). Overall, these results suggest that G. sylvaticum is generally more resource limited than pollen limited.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), the trioecious cactus Pachycereus pringlei (Fleming et al., 1994
), and the gynodioecious geophyte Wurmbea biglandulosa (Ramsey and Vaughton, 2002
), females were more pollen limited than hermaphrodites. In a trioecious population of Silene acaulis, differences between females and hermaphrodites in pollen limitation were not found (Mutikainen and Asikainen, unpublished data). The increased reproductive success of hermaphrodites after supplemental pollination observed here indicates that insect visits are necessary for high reproductive output in hermaphrodites as well as in females. Because we did not observe a higher degree of pollen limitation in females compared to hermaphrodites, our results suggest that limited pollen availability does not reduce the chances of coexistence of females with hermaphrodites in G. sylvaticum. In fact, equal or even lower pollen limitation of females compared to hermaphrodites together with the presumed lower expenditure on pollinator attraction in females through production of smaller flowers may even be beneficial for the maintenance of female plants because they may allocate resources more efficiently for reproduction and survival. Similarly to pollen limitation, resource availability did not limit the reproductive output of females and hermaphrodites significantly differently and thus it is unlikely to contribute significantly to the maintenance of gynodioecy in G. sylvaticum. In contrast to our results, the effect of resource limitation on reproductive output of females and hermaphrodites differs in some gynodioecious species (Eckhart and Chapin, 1997
; Poot, 1997
). Female plants grow more and have higher reproductive output compared to hermaphrodites in nitrogen-limited conditions, for example, in Plantago lanceolata (Poot, 1997
).
In gynodioecious species, the fitness of the two sexes is expected to be frequency dependent partly because only the hermaphrodites are able to produce pollen (McCauley and Taylor, 1997
). Such frequency dependency has indeed been found in a study of the gynodioecious Silene vulgaris (McCauley and Brock, 1998
). However, we found no significant correlation between population female frequency and pollen limitation of females in the present study. Thus, our results suggest that pollen limitation of females is not frequency dependent, at least given the variation in sex ratio seen in this species. McCauley and Brock (1998)
studied pollen limitation among 12 artificial populations that vary from 0 to 100% (in 10% intervals) in their female frequency. If we compare the study of S. vulgaris to the present study, there are at least two major differences. First, female frequency of natural populations differs considerable between these two plant species. In G. sylvaticum, female frequency varies from almost zero to 27.2% among natural populations (Asikainen and Mutikainen, 2003
), whereas in S. vulgaris female frequency varies from 0 to 75% (McCauley and Brock, 1998
). Second, the study of pollen limitation in S. vulgaris was conducted in artificial populations, whereas here we examined pollen limitation in G. sylvaticum in natural populations. Note that female frequency was rather low and varied within a narrow range (4.4–23%) among our study populations. It is possible that these facts explain the lack of a significant correlation between the level of pollen limitation and population female frequency observed in G. sylvaticum. However, with respect to the maintenance and dynamics of gynodioecy, it is important to examine the frequency dependence in populations that are within the range of natural variation in female frequency. For example, we have not found any natural populations with more than 30% females. Note also that because we only had five study populations, the power in the analysis of the relationship between female frequency and pollen limitation is rather low.
In conclusion, pollen limitation of females did not increase with an increase in female frequency, and thus, it should not constrain female frequencies in gynodioecious populations in G. sylvaticum. Because the observed female population frequencies are rather low (less than 30%), the fitness and frequency of female plants must be limited by other ecological or genetic factors.
Variation in pollen limitation
The extent of pollen limitation varied among populations, but was not related to the frequency of pollen producers in G. sylvaticum. Thus, the observed variation in pollen limitation among populations is more likely to be caused by variation in habitat characteristics than by variation in female frequency. Habitat characteristics may influence the species composition of the pollinator fauna as well as the amount and activity of pollinators (e.g., Delph, 1990
). Population size, the location per se and differences in habitat types are likely to cause variation in pollen limitation among the study populations. Varying weather conditions, such as temperature and precipitation, during the flowering season are also likely to cause variation in pollination success through variation in pollinator abundance and activity in space and time (Dudash and Fenster, 1997
; Baker et al., 2000
). The highest level of pollen limitation was observed in the Katariinanlaakso, Seili II, and Ruissalo populations (L = 0.28, 0.17, and 0.13, respectively). We found no pollen limitation in the Paimio and Seili I populations (L < 0). Three of our study populations are located on the mainland of southern Finland and two on an island. Furthermore, habitat type varies from open meadows to deciduous forest. However, the differences in habitat characteristics between the mainland and island populations do not explain the difference in pollen limitation. In fact, the two island populations that are located quite close to each other (less than 1 km), Seili I and Seili II, both in a meadow habitat, experienced considerably different levels of pollen limitation. Thus, to find out whether variation in pollen limitation is explained by habitat type, we need to include populations from other habitats than meadows.
Resource and pollen limitation
To our knowledge, the effects of pollen and resource supplementation have been simultaneously examined only in a few other studies (e.g., Delph, 1986
; McCall and Primack, 1987
; Campbell and Halama, 1993
). Simultaneous addition of resources may more reliably reveal the level of pollen limitation if hand-pollinated plants are not able to increase seed or fruit production due to resource limitation and vice versa. In our study, simultaneous addition of pollen and resource suggest the existence of significant but low pollen limitation. The results on fertilized plants strengthen the conclusion that there is no difference in pollen limitation between females and hermaphrodites in G. sylvaticum. Further, our results suggest that G. sylvaticum is more limited by resource availability than by pollen availability. This results from the fact that the main effect of fertilization was stronger than that of supplemental pollination and only slightly weaker than the combined effect of fertilization and supplemental pollination.
Previously, we did not find significant differences in individual seed mass between females and hermaphrodites of G. sylvaticum, whereas seed mass varied among populations (Asikainen and Mutikainen, 2003
). Thus, we expected the seed mass of G. sylvaticum to be quite stable. In this study, we measured seed mass to examine if fruit set or seed set of hand-pollinated or fertilized plants increased at the expense of seed mass. We found no difference in seed mass between hand-pollinated and open-pollinated plants. However, the seeds of fertilized plants were slightly heavier (6.6%) than the seeds of nonfertilized plants. This result suggests that resource availability affects not only the quantity of seeds produced but seed quality as well.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ashman T.-L C Diefenderfer 2001 Sex ratio represents a unique context for selection on attractive traits: consequences for the evolution of sexual dimorphism. American Naturalist 157: 334-347[CrossRef][ISI]
Ashman T.-L M. L Stanton 1991 Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72: 993-1003[CrossRef][ISI]
Ashman T.-L J Swetz S Shivitz 2000 Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana. Oikos 90: 347-356[CrossRef][ISI]
Asikainen E P Mutikainen 2003 Female frequency and relative fitness of females and hermaphrodites in gynodioecious Geranium sylvaticum (Geraniaceae). American Journal of Botany 90: 226-234
Ayre D. J R. J Whelan 1989 Factors controlling fruit set in hermaphroditic plants: studies with the Australian Proteaceae. Trends in Ecology and Evolution 4: 267-272[CrossRef]
Baker H. G 1948 Corolla size in gynodioecious and gynomonoecious species of flowering plants. Proceedings of the Leeds Philosophical Society 5: 136-139
Baker A. M J. D Thompson S. C. H Barrett 2000 Evolution and maintenance of stigma-height dimorphism in Narcissus. II. Fitness comparisons between style morphs. Heredity 84: 514-524
Bell G 1985 On the function of flowers. Proceedings of the Royal Society of London, B 224: 223-265
Bierzychudek P 1981 Pollinator limitation of plant reproductive effort. American Naturalist 117: 838-840[CrossRef][ISI]
Burd M 1994 Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60: 83-139[CrossRef][ISI]
Burd M 1995 Ovule packaging in stochastic pollination and fertilization environments. Evolution 49: 100-109[CrossRef][ISI]
Burd M 1998 "Excess" flower production and selective fruit abortion: a model of potential benefits. Ecology 79: 2123-2132[ISI]
Campbell D. R K. J Halama 1993 Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74: 1043-1051[CrossRef][ISI]
Charlesworth D 1981 A further study of the problem of the maintenance of females in a gynodioecious species. Heredity 46: 27-39
Darwin C. R 1877 The different forms of flowers on plants of the same species. Murray, London, UK
Delph L. F 1986 Factors regulating fruit and seed production in the desert annual Lesquerella gordonii. Oecologia 69: 471-476[CrossRef][ISI]
Delph L. F 1990 The evolution of gender dimorphism in New-Zealand Hebe (Scrophulariaceae) species. Evolutionary Trends in Plants 4: 85-97
Delph L. F 1996 Flower size dimorphism in plants with unisexual flowers. In D. G. Lloyd and S. C. H. Barrett [eds.], Floral biology: studies on floral evolution in animal pollinated plants, 217–237. Chapman and Hall, New York, New York, USA
Delph L. F 2003 Sexual dimorphism in gender plasticity and its consequences for breeding system evolution. Evolution and Development 5: 34-39
Delph L. F S. B Carroll 2001 Factors affecting relative seed fitness and female frequency in a gynodioecious species, Silene acaulis. Evolutionary Ecology Research 3: 487-505[ISI]
Delph L. F C. M Lively 1992 Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynoecious shrub. Oikos 63: 161-170[CrossRef][ISI]
Dudash M. R C. B Fenster 1997 Multiyear study of pollen limitation and cost of reproduction in the iteroparous Silene virginica. Ecology 78: 484-493[CrossRef][ISI]
Eckhart V. M 1991 The effects of floral display on pollinator visitation vary among populations of Phacelia linearis (Hydrophyllaceae). Evolutionary Ecology 5: 370-384[CrossRef][ISI]
Eckhart V. M F. S Chapin 1997 Nutrient sensitivity of the cost of male function in gynodioecious Phacelia linearis (Hydrophyllaceae). American Journal of Botany 84: 1092-1098[Abstract]
Fleming T. H S Maurice S. L Buchmann M. D Tuttle 1994 Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae). American Journal of Botany 81: 858-867[CrossRef][ISI]
Frank S. A 1989 The evolutionary dynamics of cytoplasmic male sterility. American Naturalist 133: 345-376[CrossRef][ISI]
Graff A 1999 Population sex structure and reproductive fitness in gynodioecious Sidalcea malviflora malviflora (Malvaceae). Evolution 53: 1714-1722[CrossRef][ISI]
Larson B. M. H S. C. H Barrett 2000 A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69: 503-520[CrossRef]
Levin D. A H. W Kerster 1974 Gene flow in seed plants. Evolutionary Biology 7: 139-220
Lewis D 1941 Male sterility in natural populations of hermaphrodite plants. New Phytologist 40: 56-63[CrossRef]
Lloyd D. G 1974 Theoretical sex ratios of dioecious and gynodioecious angiosperms. Heredity 32: 11-34[ISI]
Lloyd D. G 1976 The transmission of genes via pollen and ovules in gynodioecious angiosperms. Theoretical Population Biology 9: 299-316[CrossRef][ISI][Medline]
Lloyd D. G 1980 Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytologist 86: 69-79[CrossRef][ISI]
Maurice S T. H Fleming 1995 The effect of pollen limitation on plant reproductive systems and the maintenance of sexual polymorphisms. Oikos 74: 55-60[CrossRef][ISI]
McCall C R. B Primack 1987 Resources limit the fecundity of three woodland herbs. Oecologia 71: 431-435[CrossRef][ISI]
McCauley D. E M. T Brock 1998 Frequency-dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution 52: 30-36
McCauley D. E D. R Taylor 1997 Local population structure and sex ratio: evolution in gynodioecious plants. American Naturalist 150: 406-419[CrossRef][ISI]
Norusis M. J 1990 SPSS, Advanced statistics user's guide. SPSS, Chicago, Illinois, USA
Poot P 1997 Reproductive allocation and resource compensation in male-sterile and hermaphroditic plants of Plantago lanceolata (Plantaginaceae). American Journal of Botany 84: 1256-1265[Abstract]
Ramsey M G Vaughton 2002 Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success. Plant Systematics and Evolution 232: 189-200[CrossRef][ISI]
Schemske D. W 1980 Evolution of floral display in the orchid Brassavola nodosa. Evolution 34: 489-493[CrossRef][ISI]
Stephenson A. G 1981 Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 253-279
Sutherland S 1986 Patterns of fruit-set: what controls fruit-flower ratios in plants?. Evolution 40: 117-128[CrossRef][ISI]
Sutherland S 1987 Why hermaphroditic plants produce many more flowers than fruits: an experimental test with Agave mckelveyana. Evolution 41: 750-759[CrossRef][ISI]
Sutherland S L. F Delph 1984 On the importance of male fitness in plants: patterns of fruit-set. Ecology 65: 1093-1104[CrossRef][ISI]
Vaarama A O Jääskeläinen 1967 Studies in gynodioecism in the Finnish populations of Geranium sylvaticum L. Annales Academiae Scientiarum Fennicae, series A, IV, Biologica 108: 1-37
Whigham D 1984 The effect of competition and nutrient availability on the growth and reproduction of Ipomoea hederacea in an abandoned old field. Journal of Ecology 72: 721-730
Widén M 1992 Sexual reproduction in a clonal, gynodioecious herb Glechoma hederacea. Oikos 63: 430-438[CrossRef][ISI]
Widén B M Widén 1990 Pollen limitation and distance-dependent fecundity in females of the clonal gynodioecious herb Glechoma hederacea (Lamiaceae). Oecologia 83: 191-196
Willson M. F P. W Price 1977 The evolution of inflorescence size in Asclepias (Asclepiadaceae). Evolution 31: 495-511[CrossRef][ISI]
Willson M. F P. W Price 1980 Resource limitation of fruit and seed production in some Asclepias species. Canadian Journal of Botany 58: 2229-2233
Willson M. F B. J Rathcke 1974 Adaptive design of the floral display in Asclepias syriaca. American Midland Naturalist 92: 47-57[CrossRef][ISI]
Willson M. F D Schemske 1980 Pollinator limitation, fruit production, and floral display in pawpaw (Asimina triloba). Bulletin of the Torrey Botanical Club 107: 401-408[CrossRef][ISI]
Zimmerman J. K T. M Aide 1989 Patterns of fruit production in a neotropical orchid: pollinator vs. resource limitation. American Journal of Botany 76: 67-73[CrossRef][ISI]
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M. Lopez-Villavicencio, B. J. Genton, E. Porcher, and J. A. Shykoff The role of pollination level on the reproduction of females and hermaphrodites in the gynodioecious plant Gypsophila repens (Caryophyllaceae) Am. J. Botany, December 1, 2005; 92(12): 1995 - 2002. [Abstract] [Full Text] [PDF]
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