AOBPreview originally published online on October 2, 2002
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Annals of Botany 90: 599-605, 2002
© 2002 Annals of Botany Company
Size Distribution, Growth and Inter-year Variation in Sex Expression of Bischofia javanica, an Invasive Tree
1 Hokkaido Research Centre, Forestry and Forest Products Research Institute (FFPRI), Hitsujigaoka 7, Toyohira, Sapporo 062-8516, Japan and 2 Forestry and Forest Products Research Institute (FFPRI), PO Box 16, Tsukuba Norin Danchi, Ibaraki 305-8687, Japan
* For correspondence. Fax +81 11 851 4167, e-mail naokoy{at}ffpri.affrc.go.jp
Received: 14 March 2002; Returned for revision: 3 July 2002; Accepted: 24 July 2002 Published electronically: 2 October 2002
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Flowering activity and sex expression of Bischofia javanica Blume were investigated for 3 years. B. javanica is an invasive dioecious tree of subtropical forests on the Bonin Islands in the western Pacific of Japan. The sex ratio showed a significant male bias (1·25–2·33). Smaller trees were significantly male biased, whereas larger trees showed no significant difference in sex expression, suggesting that males tend to be more precocious in sexual reproduction. We found evidence for sex changes in B. javanica; these have not been reported previously. Most of the 1653 census trees remained non-flowering (58·1 %); 3·7 % of them showed sex changes, and the percentage of trees repeatedly flowering as males and females was 10·5 and 3·4 %, respectively. Sex changes were observed in both directions but a larger percentage of male trees became female. Flowering frequency and sex expression were significantly related to tree size (i.e. diameter at breast height). Over the 3 years, trees that were consistent females were the largest; inconsistent trees (switching sex between years) were intermediate in size, whereas consistent males were the smallest. There were no significant differences in relative growth rate (RGR) among trees of different sex or flowering frequencies. These results suggest that the maintenance of female reproduction is not related to changes in RGR of diameter but to flowering frequency or the reversal to the male form, dependent upon the internal resource status of individual trees.
Key words: Bischofia javanica (Blume), sex ratio, dioecy, sex change, invasive tree, size distribution, growth rate, subtropical oceanic island.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The invasion of alien tree species has seriously impacted many natural forest ecosystems around the world (Reichard and Hamilton, 1997; Richardson, 1998). Bischofia javanica Blume (Euphorbiaceae), a dioecious tree indigenous to south-east Asia, tropical Australia and Polynesia, has successfully invaded several disparate locations including southern Florida (Morton, 1984; Horvitz et al., 1998), mid-Pacific islands such as Hawaii (Gerrish and Mueller-Dombios, 1980), and the west Pacific Bonin Islands (Shimizu, 1988; Tanimoto and Toyoda, 1996). A detailed description of the invasive nature of this species in the Bonin Islands was given by Yamashita et al. (2000). In these islands, B. javanica has demonstrated a high capacity for seed production as evidenced by the number of seedlings, juveniles and reproductive trees in the natural forest (Shimizu, 1988; Yamashita et al., 2000). The success of this dioecious invasive species may, in part, be attributable to its reproductive behaviour.
Oceanic islands such as the Bonin Islands tend to have higher proportions of dioecious plants than continents despite the fact that it was originally believed that dioecious plants would have more difficulty colonizing islands than monoecious plants because of their self-incompatibility (Carlquist, 1974; Baker, 1984; Baker and Cox, 1984). The establishment of B. javanica on the Bonin Islands is of interest in providing evidence for the invasive success of this dioecious species in oceanic islands.
In general, the sex ratio of a plant population may be affected by prezygotic factors such as the differential success of male- and female-determining gametes of individual plants, or by postzygotic factors such as differential survival of the sexes in different habitats, differences in time of first reproduction, and environmentally determined sex expression (Lloyd and Webb, 1977; Freeman et al., 1980; Waser, 1984). Due to the higher cost of producing fruit, females in many plant species suffer higher mortality than males or begin to reproduce later when they are larger. Environmental sex determination may result in sex change or biased sex ratios such that maleness or femaleness in a heterogeneous environment may depend on the local resource status. In general, harsher locations tend to favour maleness while more resource-rich conditions lead to femaleness (Freeman et al., 1980).
Seed and seedling establishment through dispersal of seed by birds is one of the critical factors for the invasion success of B. javanica (Shimizu, 1988). For a dioecious species, seed production and potential seedling number should be linearly related to the proportion of female plants in the population, to pollination success and to seed predation. Among the attributes of a successful invasive species are a high reproductive capacity, a short juvenile period, production of a large amount of seed and short intervals between mast seeding (Rejmanek and Richardson, 1996). B. javanica exhibits many of these life history attributes. Once seedlings have established, its ability for rapid growth following canopy gap formation (Yamashita et al., 2000) may allow B. javanica to reach maturity more quickly than native species, thus facilitating successful invasion within only a few generations since its introduction a century ago.
Successful reproduction in dioecious plants is regulated by factors such as the spatial structure of adults and the distance between males and females (House, 1992; Gibson and Menges, 1994; Stacy et al., 1996; Mack, 1997; Percy and Cronk, 1997), flowering frequency (Bawa, 1980; de Jong et al., 1992), sex ratio (Bullock and Bawa, 1981; Barrett and Thompson, 1982; Bullock, 1982; Carlsson-Graner et al., 1998), effective population size (Nunney and Elam, 1992; Lande, 1995; Nunney, 1995; Osunkoya, 1999) and pollinator abundance and flight behaviour (House, 1992, 1993; Stacy et al., 1996). Some plant populations exhibit annual variations in sex expression associated with environmental conditions or resource allocation to male and female function (Freeman et al., 1976; Vitale and Freeman, 1986). Annual changes in the proportion of female trees, size at first reproduction, and frequency of flowering could be important features defining the reproductive capacity of B. javanica.
The flowering pattern of B. javanica in a natural mesic forest in the Bonin Islands was studied over three successive years. A large number of individuals (1653) were monitored to address the following questions: (1) does the proportion of female trees of this species vary annually? (2) Is sex expression a stable trait in this population? (3) Are sex expression and flowering frequency related to tree size and growth rate?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A flowering census of B. javanica was conducted in the Mt Kuwanoki Forest Reserve on Hahajima Island of the Bonin Islands, approx. 1000 km south of Tokyo (26°39' N, 142°9' E, 256 m a.s.l.). The reserve covers 5·5 ha; the 2·3 ha study site within the reserve was situated in a natural mesic forest. The climate is subtropical and maritime. The annual mean temperature is 22·9 °C and mean precipitation is 1261 mm (1969–1990; Haha-jima Municipal Office).
Flowering of B. javanica peaks in late-February to mid-May (Shimizu, 1988). All trees in the study site with a diameter at breast height (DBH) greater than 4 cm were numbered (1653 individuals) and their flowering sex determined annually by observing flowers through binoculars in early to mid-March in 1999, 2000 and 2001. B. javanica has small, unspecialized flowers which are visited by small, generalist insects (N. Yamashita, personal observation) DBH was recorded for all 1653 individuals in June 1999 and December 2001. Relative growth rate (RGR) of DBH was calculated following the standard growth analysis method described by Hunt (1982) where RGR was calculated as:
R = (ln Dt2 – ln Dt1)/(t2 – t1) (1)
where R is RGR, D is the DBH of a trunk and t is time in years.
Deviations of sex ratios (number of males/number of females) from 1 : 1 were tested using standard log-likelihood methods (G test for goodness of fit, where expected values are calculated based on the null hypothesis of a sex ratio of 1 : 1). To determine whether there were differences in DBH or RGR between sexes or among annual flowering frequencies, one-way ANOVA was performed using STATISTICA (version 5·1; StatSoft, Inc., Tulsa, OK, USA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sex ratio and size distribution of male and female trees
The number of male plants significantly exceeded the number of female plants in all 3 years of observations (G test, P < 0·05, Table 1). Male-biased sex ratios ranged from 1·25 to 2·30, and ratios were increasingly male biased in years when the total number of flowering individuals was small (Table 1). However, the size distribution of male and female trees broadly overlapped (Fig. 1). There were no flowering trees in the 4–10 cm DBH class in 1999, but in 2000 and 2001 there were both male and female plants in this size class. In 1999 and 2000, male bias was significant in most of the size classes. In 2001, however, male bias was only significant in the 10–16, 16–22 and 22–28 cm DBH classes. Only the largest trees (DBH >52 cm) consistently showed no significant male bias.
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Sex changes between years
In a given year, a high proportion of both male and female trees maintained the same sex as in the previous year (Table 2). In 2000, 5·6 % male trees (12 individuals) and 16·3 % female trees (16 individuals) changed sex from the previous year. In 2001, 7·1 % male trees (23 individuals) and 5·0 % female trees (seven individuals) changed sex from 2000. In all 3 years of observation, there were no trees with both male and female flowers in a given year.
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Relationships between sex expression, tree size and growth rate
Average DBH was consistently higher in females > males > non-flowering trees in all 3 years of observation (P < 0·05, Table 3). Differences in flowering frequency during the study period were significantly size dependent, i.e. DBH of trees that flowered three times > DBH of trees flowering twice > DBH of trees flowering once > DBH of trees that did not flower (P < 0·05, Table 4). RGR of DBH was also smallest in consistently non-flowering trees during the 3-year observation but it did not differ significantly among trees with different flowering frequencies or between trees of different sex. Among the trees that flowered, those that were consistently female in all 3 years (F for 3 years) were significantly larger than trees that were consistently male (M for 3 years), and among trees flowering only once males were smaller (M for 1 year, Non for 2 years). Trees with inconsistent sex expression and trees flowering as females over 2 consecutive years (F for 2 years, Non for 1 year) had a DBH intermediate between that of consistent females and consistent males over 3 years.
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The DBH of trees that remained female for two successive years (FF) was significantly greater than that of trees remaining male (MM) in both 1999–2000, and 2000–2001 (Table 5). During these years, the percentage of the total number of MM in all trees (12·1 % averaged over two successive years) was higher than that of FF (4·8 % averaged over two successive years). The average size of sex-changing trees was significantly greater in MF trees (39·40 cm DBH) than in FM trees (24·39 cm) in 2000–2001, but there was no significant difference in DBH between FM and MF trees in 1999–2000. The DBH of NF trees (non-flowering in 1999 or 2000 but flowered as female in the subsequent year) was significantly greater than that of NM trees (non-flowering in 1999 or 2000 but flowered as male the subsequent year).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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For Bischofia javanica, more male trees were in the smaller size classes than the larger one (Fig. 1). The DBH of NF trees (non-flowering in 1999 or 2000 but flowered as female in the subsequent year) or trees that were F for 1 year Non for 2 years (flowering only once as females) was larger than that of NM trees (non-flowering in 1999 or 2000 but flowered as male in the subsequent year) or M for 1 year Non for 2 years (flowering only once as males) (Tables 4 and 5). Consistent with other findings (Vasiliauskas and Aarssen, 1992; Allen and Anthos, 1993; Marion and Houle, 1996), these results suggest that males tend to be more precocious in sexual reproduction. The DBH distribution of female B. javanica trees was significantly shifted to the right compared with that of males (Table 3). The larger size of female compared with male trees is found in many dioecious species and is explained by females having to accumulate enough resources through vegetative growth to support fruit maturation (Freeman et al., 1976, 1980; Charnov, 1982). In this study, the percentage of repeat flowering males was greater than that of females, and NF trees were larger than NM trees. These results imply a higher cost of reproduction associated with femaleness than maleness.
The observed sex changes in B. javanica appear to be the first reported for this species. Changes in sex expression in other plant taxa (e.g. Lovett Doust and Cavers, 1982; Voeks, 1988; Sakai, 1990; Matsui, 1995) appear to be related to internal conditions of the plant or the availability of resources such as water, nutrients or light (Freeman et al., 1980; Bierzychudek, 1982; Lovett Doust and Cavers, 1982; Kinoshita, 1986). Some tree species begin reproduction as males and later switch to females when sufficient resources have been accumulated to support the greater costs of fruit development (Freeman et al., 1980; Bierzychudek, 1982; Kinoshita, 1986; Sakai, 1990). There is evidence to support this size-dependence in B. javanica since female trees are significantly larger than males, and trees are more likely to switch from male to female (10·6 %, 2-year average) than from female to male (6·3 %, 2-year average). The DBH of trees with inconsistent sex expression was intermediate between consistent female (female for 3 years) and male (male for 3 years) trees. Moreover, in two successive years of observation, the size and number of MF trees (42·8 cm average in two successive years, n = 35 individuals) were greater than those of FM trees (34·8 cm average in two successive years, n = 21 individuals). These results show that the overall larger size of trees with inconsistent sex expression may be mainly due to a greater representation by MF trees, suggesting a higher resource demand for females, and that subsequent to flowering, small females are more prone to reverting back to males or non-flowering.
In many plant species, the high investment to female reproduction is often reflected in differential demographic costs. This is represented by low nutrient reserves in the years following fruiting, expressed as smaller numbers of female flowers per plants or lower growth rate (Rocheleau and Houle, 2001). In flowering trees of B. javanica, however, there was no significant association between RGR and flowering frequency or sex expression (Table 3). These results suggest that meeting the cost of female reproduction may not be related to the variation in RGR of tree diameter but to flowering frequency (FN) or sex reversion to males (FM), depending upon the internal resource status of individual trees. Willson (1986) found similar results in Acer negundo where fruit production had no measurable effect on growth of female relative to male trees. Other studies of the same species also showed similar trends in that males and females had similar growth and physiological responses during dry years, whereas during wet years females exhibited higher growth rates and more profligate water use than males (Dawson and Ehleringer, 1993; Ward et al., 2002).
Males and females of some plant species show a different relationship between plant size and gain in fitness (Freeman et al., 1993, 1997). These authors found that the gain in fitness of males (the number of pollen grains dispersed per unit volume of the donor plant) in Atriplex canescens declined as donor plant size increased, but the total mass of fruit produced per unit plant volume was constant for females. Because no sex-specific difference in growth rate was observed in B. javanica, it is probable that the cost of reproduction is similar in males and females and that sex expression is driven by other size-related factors. Further work on size-dependent changes in male and female fitness is necessary to clarify the factors driving sex expression of this species.
B. javanica was significantly male biased during the 3 years of observation on the Bonin Islands (Table 1). Trees in the family Euphorbiaceae have a similar male-biased sex ratio (Thomas and LaFrankie, 1993). Male-biased sex ratios in the population could lead to increased availability of pollen for female trees. Positive correlations between fecundity and male density have been reported in several tree species (House, 1993). If this is the case, then the male-biased B. javanica population would represent low pollen limitation which favours greater production of viable seeds. Additional data are required to demonstrate the link between higher reproductive success of individual trees and a male-biased sex ratio.
Contrary to the observation on the Bonin Islands, the sex ratio of B. javanica in its native habitat of Okinawa was found to be 1 : 1 (Abe et al., 2002). Available evidence regarding both sex changes and sex ratio variations in Okinawa suggests that the male-biased sex ratio of B. javanica in the Bonin Islands is induced by the local environment. Some dioecious plants exhibiting male-biased reproduction have been found in environments low in nutrients or moisture availability (Freeman et al., 1980; Shea et al., 1993), where plant density is high or the population is young (Lovett Doust and Laporte, 1991; Wheelwright and Bruneau, 1992). Populations of B. javanica in the Bonin Islands are only a few genera tions old (it was introduced only 100 years ago). The large numbers of seedlings, saplings and small canopy trees suggest a young population in a phase of expansion growth. Wheelwright and Bruneau (1992) also reported that a population of Ocotea tenera (a rainforest tree) was male-biased in a young experimental plot but that the sex ratio was 1 : 1 in a natural mature population. Extrapolating from the current higher frequency of sex change from male to female in B. javanica, we speculate that this population will eventually reach an even sex ratio over time. Long-term monitoring of the environment, population age structure and sex ratio is needed to resolve the regulation of sex expression in this species in this recently invaded habitat.
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ACKNOWLEDGEMENTS |
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We thank Dr T. T. Lei for critical reading of the manuscript and stimulating discussions. Thanks are also due to Drs K. Niiyama and H. Tanaka for their various comments. We are grateful to N. Koike, Y. Hoshi, K. Kamo, A. Ishida and N. Tanaka for their support during this study. Kind and detailed comments were received from Dr D. C. Freeman. This study was supported by grants funded by the Environmental Agency, and by the Ministry of Education, Culture, Sports, Science and Technology (B-14360091).
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