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Reproductive Biology |
Department of Biology, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka, Osaka 560-0043, Japan
Received for publication April 12, 2005. Accepted for publication August 26, 2005.
ABSTRACT
Intersexual differences in reproductive investments (RIs) (dry mass of reproductive tissue) at tree and branch levels in Eurya japonica were examined during two successive years. Mean total RIs per tree for males and females (adjusted for the mean trunk diameter in the combined sample trees, 25.7 mm) were 3.47 and 5.67 g dry mass. Females generally allocated about 1.6 times more biomass per tree to reproduction than males. On the other hand, male total RI per terminal branch averaged 51.6 mg dry mass and female averaged 226.6 mg. Females generally allocated about 4.4 times more biomass per terminal branch to reproduction than males. Thus, the magnitude of sexual difference at the tree level was much lower than that at the branch level. There were negative correlations between interyear fluctuation of total RI and stem diameter for both sexes. Interyear fluctuation of RI was greater for females than males in all size categories. This study revealed that conclusions from tree measures of RI differed from branch measures and suggested the importance of evaluating the average RI at the tree level for woody plants. I discussed the importance in adopting an effective sampling strategy for evaluating the RI at the tree level.
Key Words: dioecious plants • module levels • reproductive investment (RI) • sex-related reproduction • size-related reproduction
The concept of trade-offs is based on the scarcity or limited availability of resources and the fact that when more resources are allocated to one function fewer resources are available for other functions (Bazzaz et al., 1987
; Stearns, 1992
; Höglund and Sheldon, 1998
). Much attention has been directed at trade-offs between investments in reproductive and vegetative function because these relationships reflect how organisms balance fecundity against survival probability throughout their lifespans, that is their life history strategies (Bazzaz et al., 1987
). Dioecious plants are thought to be particularly appropriate for the study of the relationships between reproductive and vegetative function because, in these plants, the costs of female functions can be readily separated from those of male functions (Hoffman and Alliende, 1984
; Nicotra, 1999
).
In many dioecious species, males have greater investment in vegetative growth than do females (Putwain and Harper, 1972
; Grant and Mitton, 1979
; Sakai and Burris, 1985
). Many other reports demonstrate that males exceed females in vigor, total size, or vegetative reproduction (Lloyd and Webb, 1977
). Most of those studies concluded that such sexual dimorphism is caused by differential reproductive investment (RI) between the sexes, i.e., females invest more resources in reproduction than do males. Delph (1999)
and Obeso (2002)
reviewed the literature and concluded that RI was consistently higher for females of most dioecious species.
In most woody plants, however, the evidence for differences in RI between the sexes is not based on analyses at the whole plant level, but rather at a finer modular scale (i.e., twig, branch, shoot, or other subunits comprising an individual). From an evolutionary viewpoint, it is the differences among individuals in their reproductive success that is of interest (Herrera, 1991
; but see also Gill et al., 1995
). If the RI at the level of twigs, branches, or shoots is poorly correlated with that of the individual plant, then conclusions of studies based on a finer scale of the plant's modular structure may be misleading (Herrera, 1991
). Because the RI among branches within a tree and among trees can vary greatly, it may be difficult to adequately sample the reproductive branches to reflect reproductive patterns at the tree level. Therefore, measurement of the RI of the plant as a whole is needed.
Plant size is an important factor determining RI (Oyama, 1990
; Worley and Harder, 1996
), and plant-size-dependent effects can be a leading source of variation in reproduction and growth in flowering plants (Herrera, 1991
). In perennials, fecundity per unit plant mass often increases with plant size, with large plants producing more seeds per unit biomass than small ones (Solbrig et al., 1988
; Silvertown and Lovett Doust, 1993
). Therefore, size-dependent effects on RI should be taken into consideration when examining whether sexual dimorphism in RI occurs. If size-dependent variations in RI exist, comparing the average RIs of individuals between sexes if they differ in size will yield a biased result, and plant size should be used as a covariate in the experimental design for improved assessment of RI (Obeso, 2002
).
Interyear variation in RI is also important when comparing RI between the sexes on a lifetime or long-term basis. The RI of an individual plant often fluctuates considerably from year to year (e.g., masting species). For dioecious plants, patterns of annual variation in RI may differ between the sexes. In general, the reproductive behavior between years varies more in females than in males; females flower less frequently than do males (Meagher and Antonovics, 1982
; Bullock and Bawa, 1981
; Bullock, 1982
; Meagher and Antonovics, 1982
; Oyama, 1990
; Cipollini and Stiles, 1991
; Nicotra, 1999
). Such results suggest that single opportunistic censuses frequently lead to biased results (Thomas and LaFrankie, 1993
). Furthermore, females can vary more in intensity of RI among years even if they flower every year. Patterns of interyear variation in RI should be determined in order to compare the average RIs between sexes.
I examined reproductive pattern at the tree level as a function of tree size and sex in Eurya japonica, a temperate dioecious species, during two successive years. The objectives of the study were to answer the following: (1) Do female trees allocate more biomass to reproduction than do males? (2) How do between-year fluctuations in reproductive investment at the tree level vary as a function of tree size and sex? (3) Do conclusions from tree measures of RI differ from branch measures? Furthermore, a potential influence of fruit photosynthesis on estimation of RI is discussed.
MATERIALS AND METHODS
Study species and study area
Eurya japonica (Theaceae) is a broad-leafed evergreen subcanopy tree that attains a height of more than 10 m at maturity. The species is widely distributed in Taiwan, China, Japan (Honshu, Shikoku, Kyushu, and Ryukyu Islands), and the southern parts of the Korean Peninsula. The study was carried out in a natural secondary forest at the Kamigamo Experimental Forest Station of Kyoto University (35°04 N, 135°43' E; altitude, 150 m), about 12 km north of Kyoto. At this location, E. japonica is a common understory and subcanopy tree. From 1991 to 2001, the mean annual precipitation was 1553 mm and the mean monthly temperatures ranged from 2.7°C (January) to 28.0°C (August). Plants flower between late March and early April. Shoot extension growth begins in early May and finishes in autumn. Flowers are borne in the leaf axils of shoots, not only on 1-yr-old shoots but also on older ones. The fruit ripens in autumn and is dispersed by birds. Most flowering trees of the species are either male or female, although a few trees of the species produce flowers similar to hermaphrodite flowers in shape (Manabe, 1996
). The frequency of occurrence of plants that produced hermaphrodite flowers was low (<1%) at the study site, and sex expression of trees was constant for the period of the study.
Sampling procedures
Within the experimental forest, a 20 x 20 m plot was established. All trees of E. japonica within the plot were tagged in early April 1996. In 1999 and 2000, I counted the numbers of flowers (or flower buds) of all trees from early March to early April and the numbers of fruits of all female trees from early October to middle November. Maps of the branching structure of all branches issued directly from the trunk for all the trees were drawn as two-dimensional diagrams. In this paper, the terminal branch was defined as each terminal, unbranched segments of a branch, which is equivalent to the first-order branch in centripetal ordering systems such as the Strahler system (Borchert and Slade, 1981
). The position of each flower and fruit was indicated using a code of symbols. In this way, the numbers of flower and fruit produced at the tree and terminal branch levels were determined. Most flowers and fruits were produced on the terminal branches. I avoided sampling problems by making complete surveys of whole canopies for all the trees. The various parts of the tree crowns were reached by stepladders. In addition, sex expression was noted for all trees for the two consecutive years. I studied 69 male, 60 female, and 95 nonflowering trees. Fresh flowers and fruits were picked from the trees outside the plot and dried separately for mass determinations (five female trees, 10–15 flowers each, 10– 20 fruits each; five male trees, 10–15 flowers each). Stem diameter was measured at ground level in April 2000 as the index of the tree's size.
Data analysis
In this paper, reproductive investment (RI) is defined as the amount of biomass allocated to reproductive tissues. Analysis of covariance (ANCOVA) was used to relate variation in RI to variation in tree size (stem diameter) within each sex (see Sokal and Rohlf, 1995
). The ANCOVA model was constructed with plant sex as a fixed factor and stem diameter as a covariate. The interaction between plant sex and stem diameter was used to test for differences in slopes between the sexes. A significant covariate term indicates that RI and tree size were significantly correlated. A significant main effect (plant sex) term shows that RI differed significantly between sexes when tree sizes are kept comparable.
The significance of differences in RI per terminal branch between the sexes was determined by a Mann-Whitney U test. The reproductive trees were too large and had too many branches to measure the length or diameter of all the terminal branches and branch-size-dependent effects on RI were not considered. However, the size-dependent effects on RI are likely to be minimal because the size-variation of the terminal branches was relatively small (the lengths of most terminal branches seemed to range from 10 to 20 cm; A. Suzuki, personal observation).
Goodness-of-fit tests were used to examine differences between sexes in the probability of flowering in one or both years. Spearman's rank correlation coefficient was used to examine the relationship between RI fluctuation and tree size (stem diameter) for each sex. In order to quantify interyear fluctuation in RI, the ratio of the better to poorer year's RI was used as the index of fluctuation (Bullock and Bawa, 1981
; Suzuki, 2001
). Mann-Whitney U test was used to determine the significance of size- specific differences in interyear fluctuation of RI between the sexes.
RESULTS
Flower and fruit dry mass
Female flowers had a mean dry mass 1.9 times higher than male flowers. The mean dry mass (±SE) per male flower was 2.18 ±0.08 mg, and 1.14 ± 0.03 mg per female flower. Mean dry mass of fruits was 26.06 mg (±2.27 SE).
Annual reproductive investment at flowering
Tree level
The average number of male flowers per tree was 434.2 and that of female flowers was 175.3 (the maximal number of male flowers per tree was 12 381 and that of female flowers was 7082). Slopes of regressions between RI at flowering (in terms of biomass allocated to flowers per tree per year) and plant size did not differ significantly between sexes in each of the two study years (1999 and 2000) and in the 2-year average, indicating that RI at flowering was significantly and positively correlated with plant size for the two sexes (Fig. 1 and Table 1. A significant covariate term indicates that the pooled regression of RI at flowering on plant size is significant in each of the study years and the 2-year average (see Basal diameter term of ANCOVA, Table 1). Furthermore, mean RIs at flowering per tree for males and females (adjusted for the mean trunk diameter in the combined sample trees, 25.7 mm) were 3.13 (95% confidence limits 2.36–4.13) and 0.56 (95% confidence limits 0.42–0.75) g dry mass. Thus, males allocated about 5.6 times more biomass per tree to flowers than females. Mean RI at flowering differed significantly between the sexes when the plant sizes were comparable, as indicated by a highly significant plant-sex term (Table 1).
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Total annual reproductive investment
Tree level
For males, the total RI is the same as the RI at flowering. For females, flower and fruit mass is simply added. Slopes of the regressions between total RI (in terms of biomass allocated to reproductive tissue per tree per year) and plant size were not significantly different between sexes in each of the two study years and the 2-year average (Fig. 2, Table 2). Total RI was also significantly and positively correlated with plant size. A significant covariate term indicates that the pooled regression of total RI on plant size was significant in each of the study years and in the 2-year average (see Basal diameter term of ANCOVA, Table 2). Mean total RIs per tree for males and females (adjusted for the mean trunk diameter in the combined sample trees, 25.7 mm) are 3.47 and 5.67 g dry mass, respectively. Females generally allocated about 1.6 times more biomass per tree to reproduction than males. The differences between the sexes were statistically significant (see plant-sex term of ANCOVA, Table 2). However, the total RI distributions of male and female trees overlapped to a considerable extent, as shown in Fig. 2, and the adjusted means for males and females have a large 95% confidence interval, 2.36–4.23 g and 4.36–8.02 g, respectively.
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Sex ratios and reproductive frequency
The number of flowering male plants exceeded the number of flowering female plants in both years (Table 3). The sex ratios of this stand in 1999 and 2000, however, did not significantly differ from unity (chi-square tests, P = 0.31 and 0.28, respectively). The cumulative sex ratio also did not significantly differ from unity (chi-square test, P = 0.43).
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The differences in total RI fluctuations between males and females were not significant (P > 0.05, Mann-Whitney U test), except in the medium size class category (stem diameter 2–3 cm), although the fluctuations were greater for females than males in all three size categories (Table 5).
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Several authors have suggested the importance of defining the modular level at which costs are assessed (Lovett Doust and Lovett Doust, 1988
; Obeso, 1997
). From an evolutionary viewpoint, it is the differences in RI among individuals that is of interest, and cost-accounting ultimately must be done for the plant as whole (Newell, 1991
). It is therefore surprising that within the field of reproductive ecology the question of differences in RI between the sexes is still open. In most previous studies on dioecious woody species, cost-accounting has been done not for the plant as a whole, but on a finer scale such as twig, branch, or shoot.
At the branch level, many studies have shown clear differences in RI between the sexes. For example, Obeso (1997)
revealed that in Ilex aquifolium, females allocated about eight times more biomass per branch to reproduction than did males. In addition, Armstrong and Irvine (1989)
showed that for Myristica insipida females expended 421% more energy on reproduction per unit length of flowering twig than did males. The present study also supported the trend at the branch level. However, the results of the present study at the tree level indicate that differences in total RI between the sexes tend to be far smaller when plant sizes were comparable.
Furthermore, photosynthesis in fruits may contribute to their carbon requirements, thereby potentially reducing the relative cost of fruit production. Ogawa (2002)
estimated the carbon balance in reproductive organs for 20 woody species over the entire reproductive period. He showed that the relationship between net respiration and dry-mass growth was formulated by a linear function with a negative y-intercept. Therefore, woody plants are divided into three groups, in which CO2 release by dark respiration is less than, equal to, or greater than CO2 refixation by photosynthesis, depending on the size of the reproductive organ. According to the analysis, the net respiration changed from positive to negative at final dry mass (w) = 0.481 g as w decreased (Ogawa, 2002
). The average fruit dry mass for E. japonica at the final stage was 0.072 g, much smaller than the estimated threshold (w = 0.481 g), and developing fruits of E. japonica are green. As commented on by Alpert et al. (1985)
and Cipollini and Levey (1991)
, if allocation implies distribution of a set amount of resources among mutually exclusive uses, then RI of the cost of fruit production must take into account the potential for fruit photosynthesis. Given that fruit photosynthesis in E. japonica accounts for 4% or more of the total carbon requirements of the fruit (i.e., quantity of photosynthates imported from other organs is assumed to be 
96% of the total fruit dry mass), the total RI of females (flower dry mass + 96% of fruit dry mass) does not differ statistically from that of males at the tree level (ANCOVA among intercepts: MS = 0.486, F = 2.556, P = 0.113, data not shown). Although the 1.6 times difference seems to be large at a glance, the variations of RI are also relatively large (see 95% confidential limits in the Results). Then, the difference became not significant, at least statistically, even if only 4% of fruit mass assumed to be from fruit photosynthesis.
Several authors have noted that not only the total investment, but also the timing of reproductive investment is an important consideration (Ågren, 1988
; Delph, 1990
; Antos and Allen, 1994
; Obeso, 2002
). Flowers of E. japonica are produced in early spring. At that time, new leaves of this species and most deciduous species around the site have not expanded because low temperature may prevent their retaining sufficient positive net photosynthesis. Therefore, flowers of E. japonica may be formed largely from stored energy reserves, whereas fruit energy requirements are probably supplied by current photosynthate. Delph (1990)
pointed out that if males invest more in flowering, then females may invest more in photosynthetic tissues early in the season and thereby acquire more resources. The difference in the timing of reproductive investment may decrease the estimate of the negative impact of fruit production on vegetative growth.
Many studies, including the present one, showed large between-year variations in flowering frequency (Hoffmann and Alliende, 1984
; Carlsson and Callaghan, 1990
; Oyama, 1990
; Cipollini and Stiles, 1991
; Herrera et al., 1998
; Antos and Allen, 1999
; Nicotra, 1999
; Obeso, 2002
), suggesting that conclusions reflecting only one year of study may be misleading. Some species invest only those resources in reproduction that are surplus to their requirements of vegetative function and storage (Crawley, 1985
; Crawley and Long, 1995
; Suzuki, 2000
, 2001
). The between-year variations in reproduction of such species likely rely on current total production and/or on the internal resource status of individuals, which in turn depends on environmental factors such as temperature and water conditions. This situation also emphasizes the importance of long-term studies to describe accurately the average RI of long-lived plants such as E. japonica. Furthermore, particularly for dioecious plants, the between-year variation in reproduction must be taken into consideration when determining the average RI because the flowering frequency and fluctuation of male and female plants are likely to differ significantly (Bullock and Bawa, 1981
; Ågren, 1988
; Oyama, 1990
; Cipollini and Stiles, 1991
; Thomas and LaFrankie, 1993
; Antos and Allen, 1999
; Nicotra, 1999
). Eurya japonica females tended to have greater fluctuation in RI between years than males (Table 5). Greater fluctuations in female RI between years suggest that a negative feedback mechanism may act to regulate the costs of reproduction in females (Cipollini and Whigham, 1994
).
RI and between-year fluctuations in reproduction vary with plant size (Silvertown and Lovett Doust, 1993
; Solbrig et al., 1988
). For example, Thomas and LaFrankie (1993)
showed that large individuals of both sexes in three species of Aporusa flowered two years in a row far more often than did small individuals. In E. japonica, larger plants of both sexes were significantly more likely to flower in both 1999 and 2000 than were smaller plants. Perhaps a negative feedback mechanism regulates the costs of reproduction in smaller plants, which suffer from shading if they do not invest relatively more resources to vegetative structure, especially in relation to height growth because competition for light is highly asymmetric.
Based on the results at the branch level, many studies have concluded that the greater costs of reproduction for females is a main cause of male-biased sex ratios, spatial segregation of sexes, and niche differentiation, for example (e.g., Wallace and Rundel, 1979
; Cavigelli et al., 1986
). However, this study revealed that RI at the branch level was not necessarily concordant with that at the tree level. For E. japonica, males and females are not spatially segregated (Manabe, 1993
). This may be because the differences in average RI between the sexes are not substantial at the tree level, as the present study suggested. However, the importance of a more detailed analysis of the long-term consequences should not be undervalued (Bañuelos and Obeso, 2004
), and there may be differential distribution of sexes in relation to habitat (see Allen and Antos, 1993
, and Nicotra, 1998
, for good discussions on spatial distribution).
This study revealed that the conclusions based on tree measures of RI differed from branch measures, mainly because the sexes differed in their number of reproductive branches per tree. Needless to say, it is essential to estimate RI at the tree level in all woody plants, not just in dioecious species. A complete enumeration would be ideal in order to determine RI at the tree level, but this may often be impractical, especially for tall trees. Hirayama et al. (2004)
developed a method to estimate flower and seed production per tree using the seed-trap method and a new method to analyze seed dispersal numerically. Although estimating RI at the tree level for species that are spatially scattered is an adequate approach, this approach may be impractical for species in dense forests. In such cases, an effective sampling strategy should be devised. Because of the problem with estimating RI at the tree level based on RI at the terminal branch level shown by the present study, at the least, large branches should be used as sampling units to avoid problems associated with small twigs (e.g., Allen and Antos, 1988
, 1993
; Antos and Allen, 1999
).
FOOTNOTES
1 The work presented in this paper formed part of a Ph.D. thesis under the supervision of Professor Kihachiro Kikuzawa to whom the author is greatly indebted. The author thanks M. Ishihara for assistance in the field; Dr. T. Manabe for helpful comments; K. P. Sone and T. Hachiya for statistical advice; and Profs. I. Terashima, K. Noguchi, and S. Miyazawa for helpful comments on fruit photosynthesis; and is very grateful to K. Suzuki for encouragement and support throughout this study. This work was financially supported by Yuiko Suzuki Foundation for HIMO students. 
2 Author for correspondence (eurya{at}bio.sci.osaka-u.ac.jp
)
LITERATURE CITED
Ågren J. 1988 Sexual differences in biomass and nutrient allocation in the dioecious Rubus chamaemorus. Ecology 69: 962-973[CrossRef][ISI]
Alpert P. E. A. Newell C. Chu J. Glyphis S. L. Gulmon D. Y. Hollinger N. D. Johnson H. A. Johnson H. A. Mooney G. Puttick 1985 Allocation to reproduction in the chaparral shrub, Diplacus aurantiacus. Oecologia 66: 309-316[CrossRef][ISI]
Allen G. A. J. A. Antos 1988 Relative reproductive effort in males and females of the dioecious shrub Oemleria cerasiformis. Oecologia 76: 111-118[ISI]
Allen G. A. J. A. Antos 1993 Sex ratio variation in the dioecious shrub Oemleria cerasiformis. American Naturalist 141: 537-553[CrossRef][ISI]
Antos J. A. G. A. Allen 1994 Biomass allocation among reproductive structures in the dioecious shrub Oemleria cerasiformis—a functional interpretation. Journal of Ecology 82: 21-29[CrossRef]
Antos J. A. G. A. Allen 1999 Patterns of reproductive effort in male and female shrubs of Oemleria cerasiformis: a 6-year study. Journal of Ecology 87: 77-84
Armstrong J. E. A. K. Irvine 1989 Flowering, sex ratios, pollen-ovule ratios, fruit set, and reproductive effort of a dioecious tree, Myristica insipida (Myristicaceae), in two different rain forest communities. American Journal of Botany 76: 74-85[CrossRef][ISI]
Bañuelos M. J. J. R. Obeso 2004 Resource allocation in the dioecious shrub Rhamnus alpinus: the hidden costs of reproduction. Evolutionary Ecology Research 6: 397-413
Bazzaz F. A. N. R. Chiariello P. D. Coley L. F. Pitelka 1987 Allocating resources to reproduction and defense. BioScience 37: 58-67
Borchert R. N. A. Slade 1981 Bifurcation ratios and the adaptive geometry of trees. Botanical Gazette 142: 394-401[CrossRef]
Bullock S. H. 1982 Population structure and reproduction in the neotropical dioecious tree Compsoneura sprucei. Oecologia 55: 238-242[CrossRef][ISI]
Bullock S. H. K. S. Bawa 1981 Sexual dimorphism and the annual flowering pattern in Jacaratia dolichaula (D. Smith) Woodson (Caricaceae) in a Costa Rican rain forest. Ecology 62: 1494-1504[CrossRef][ISI]
Carlsson B. A. T. V. Callaghan 1990 Effects of flowering on the shoot dynamics of Carex bigelowii along an altitudinal gradient in Swedish Lapland. Journal of Ecology 78: 152-165[CrossRef][ISI]
Cavigelli M. M. Poulos E. P. Lacey G. Mellon 1986 Sexual dimorphism in a temperate dioecious Montana (Aquifoliaceae). American Midland Naturalist 115: 397-406[CrossRef][ISI]
Cipollini M. L. D. J. Levey 1991 Why some fruits are green when they are ripe: carbon balance in fleshy fruits. Oecolgia 88: 371-377[CrossRef][ISI]
Cipollini M. J. E. W. Stiles 1991 Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux. Oecologia 86: 585-593[CrossRef][ISI]
Cipollini M. J. D. F. Whigham 1994 Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae). American Journal of Botany 81: 65-75[CrossRef][ISI]
Crawley M. J. 1985 Reduction of oak fecundity by low-density herbivore populations. Nature 314: 613-614
Crawley M. J. C. R. Long 1995 Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83: 683-696[CrossRef]
Delph L. F. 1990 Sex-differential resource allocation patterns in the subdioecious shrub Hebe subalpina. Ecology 71: 1342-1351[CrossRef][ISI]
Delph L. F. 1999 Sexual dimorphism in life history. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual demorphism in flowering plants, 149–173. Springer-Verlag, Berlin, Germany
Gill D. E. E. L. Chao S. L. Perkings J. B. Wolf 1995 Genetic mosaicism in plants and clonal animals. Annual Review Ecology and Systematics 26: 423-444
Grant M. C. J. B. Mitton 1979 Elevational gradients in adult sex ratios and sexual differentiation in vegetative growth rates of Populus tremuloides Michx. Evolution 33: 914-918[CrossRef][ISI]
Herrera C. M. 1991 Dissecting factors responsible for individual variation in plant fecundity. Ecology 72: 1436-1448[CrossRef][ISI]
Herrera C. M. P. Jorrano J. Guitiàn A. Traveset 1998 Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. American Naturalist 152: 576-594[CrossRef][ISI]
Hirayama D. A. Itoh T. Yamakura 2004 Implications from seed traps for reproductive success, allocation and cost in a tall tree species Lindera erythrocarpa. Plant Species Biology 19: 185-196[CrossRef]
Hoffman A. J. M. C. Alliende 1984 Interaction in the patterns of vegetative growth and reproduction in woody dioecious plants. Oecologia 61: 109-114[CrossRef][ISI]
Höglund J. B. C. Sheldon 1998 The cost of reproduction and sexual selection. Oikos 83: 478-483[CrossRef][ISI]
Lloyd D. G. C. J. Webb 1977 Secondary sex characters in plants. Botanical Review 43: 177-216
Lovett Doust J. L. Lovett Doust 1988 Modules of production and reproduction in a dioecious clonal shrub, Rhus typhina. Ecology 69: 741-750[CrossRef][ISI]
Manabe T. 1993 Population dynamics and reproductive characteristics of understory tree species Eurya japonica in old-growth and secondary forests in warm temperate region, Japan. Ph.D. dissertation, Okayama University, Okayama, Japan (in Japanese)
Manabe T. 1996 Variations in sex expression and the reproductive function of an evergreen broad-leaf understorey species, Eurya japonica Thunb. (Theaceae). Bulletin of the Kitakyushu Museum of Natural History 15: 137-144
Meagher T. R. J. Antonovics 1982 The population biology of Chamaelirium luteum, a dioecious member of the lily family: life history studies. Ecology 63: 1690-1700[CrossRef][ISI]
Newell E. 1991 Direct and delayed costs of reproduction in Aesculus californica. Journal of Ecology 79: 365-378[CrossRef]
Nicotra A. B. 1998 Sex ratio variation and spatial distribution of Siparuna grandiflora, a tropical dioecious shrub. Oecologia 115: 102-113[CrossRef][ISI]
Nicotra A. B. 1999 Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neotropical shrub. Journal of Ecology 87: 138-149[CrossRef]
Obeso J. R. 1997 Costs of reproduction in Ilex aquifolium: effects at tree, branch and leaf levels. Journal of Ecology 85: 159-166[CrossRef]
Obeso J. R. 2002 The costs of reproduction in plants. New Phytologist 155: 321-348[CrossRef][ISI]
Ogawa K. 2002 Quantitative analysis of carbon balance for reproduction in woody species. Journal of Plant Research 115: 449-453[CrossRef][ISI][Medline]
Oyama K. 1990 Variation in growth and reproduction in the neotropical dioecious palm Chamaedorea tepejilote. Journal of Ecology 78: 648-663[CrossRef]
Putwain P. D. J. L. Harper 1972 Studies in the dynamics of plant populations. V. Mechanisms governing sex ratio of Rumex acetosa and Rumex acetosella. Journal of Ecology 60: 113-129[CrossRef]
Sakai A. K. T. A. Burris 1985 Growth in male and female aspen clones: a twenty-five-year longitudinal study. Ecology 66: 1921-1927[CrossRef][ISI]
Silvertown J. W. J. Lovett Doust 1993 Introduction to plant population ecology. Blackwell Science, London, UK
Sokal R. R. F. J. Rohlf 1995 Biometry. W. H. Freeman, New York, New York, USA
Solbrig O. T. W. F. Curtis D. T. Kincaid S. J. Newell 1988 Studies on the population biology of the genus Viola. VI. The demography of V. fimbriatula and V. lanceolata. Journal of Ecology 76: 301-319[CrossRef][ISI]
Stearns S. C. 1992 The evolution of life-histories. Oxford University Press, Oxford, UK
Suzuki A. 2000 Patterns of vegetative growth and reproduction in relation to branch orders: the plant as a spatially structured population. Trees 14: 329-333
Suzuki A. 2001 Resource allocation to vegetative growth and reproduction at shoot level in Eurya japonica (Theaceae): a hierarchical investment?. New Phytologist 152: 307-312[CrossRef][ISI]
Thomas S. C. J. V. Lafrankie 1993 Sex, size, and interyear variation in flowering among dioecious trees of the Malayan rain forest. Ecology 74: 1529-1537[CrossRef][ISI]
Wallace C. S. P. W. Rundel 1979 Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia 44: 34-39[CrossRef][ISI]
Worley A. C. L. D. Harder 1996 Size-dependent resource allocation and costs of reproduction in Pinguicula vulgaris (Lentibulariaceae). Journal of Ecology 84: 195-206[CrossRef]
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