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Annals of Botany 91: 13-19, 2003
© 2003 Annals of Botany Company
Sexual Differences in Reproductive Phenology and their Consequences for the Demography of Baccharis dracunculifolia (Asteraceae), a Dioecious Tropical Shrub
1 Ecologia Evolutiva de Herbívoros Tropicais/DBG, CP 486, ICB/Universidade Federal de Minas Gerais, 30161-970, Belo Horizonte-MG, Brazil
* For correspondence. Fax 55 31 34992569, e-mail esanto{at}icb.ufmg.br
Received: 29 May 2002; Returned for revision: 19 July 2002; Accepted: 24 September 2002 Published electronically: 31 October 2002
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Patterns of phenological variation and reproductive investment were studied in the dioecious shrub Baccharis dracunculifolia DC (Asteraceae), and possible consequences on survivorship were evaluated. The sex ratio was determined in a natural field population (n = 921) of B. dracunculifolia in Belo Horizonte, Brazil. Fifty-two males and 56 females were sampled at random from this population. During the reproductive season of 1999, inflorescence production, shoot growth and mortality, and xylem water potential were recorded for each individual. The population sex ratio was male-biased (1·27 : 1, P < 0·05), and was associated with a higher mortality of female shoots (38·4 vs. 23·1 %, P < 0·05), and individuals (17·8 vs. 11·5 %, P < 0·1), despite lower water stress in female plants. Flowering phenology also differed between the sexes, with males producing more inflorescences, and earlier, than females. Owing to fruit maturation, the number of inflorescences supported by females was higher than that supported by males later in the reproductive season. This occurred during the dry season, and drought stress may have been responsible for the greater female mortality. Thus, the male-biased sex ratio in this population of B. dracunculifolia is probably due to different reproductive functions of males and females. Intersexual differences in reproductive phenology had consequences for plant demography.
Key words: Baccharis dracunculifolia, Asteraceae, dioecy, plant phenology, sexual dimorphism, plant reproduction, sex ratio, demography, Brazil.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sex-related differences in secondary traits of dioecious plant species have been reported in many studies (e.g. Ågren, 1988; Lovett Doust and Lovett Doust, 1988; Krischik and Denno, 1990a, b; Elmqvist et al., 1991; Dawson and Ehleringer, 1993; Delph et al., 1993; Cipollini and Whigham, 1994; Renner and Ricklefs, 1995; Purrington and Schmitt, 1998; Nicotra, 1999). In general, dimorphisms in plant height and biomass, shoot length, leaf shape, and number and size of flowers are seen as products of divergent allocation to reproductive and vegetative processes in males and females (Freeman et al., 1976; Lloyd and Webb, 1977; Ågren, 1988; Krischik and Denno, 1990a, b). In theory, females should allocate more resources to reproduction, due to seed and fruit production, which may reduce their vegetative growth (Krischik and Denno, 1990a, b; Elmqvist et al., 1991; but see Delph et al., 1993), flowering frequency (Meagher, 1984; Cipollini and Stiles, 1991) and long-term survivorship (Krischik and Denno, 1990a; Éscarre and Houssard, 1991) compared with that of males.
Fruit and seed production are metabolically costly for females (Stanton et al., 1986; Ågren, 1988) and, to build and support these structures, female demand for nutrients and water may be greater than that of males. Such a dimorphic resource requirement may generate differential mortality between the sexes, often resulting in sex ratios that are skewed to maleness in natural populations of perennial dioecious species (Lloyd and Webb, 1977; Lovett-Doust et al., 1987; Krischik and Denno, 1990a; but see Eppley, 2001).
Plant phenology is related to development and sex expression in dioecious species. Studies concerning temporal variations of resource allocation to reproduction in dioecious plants usually report greater reproductive investment by males at the beginning of the reproductive season, through early flower production, whereas females tend to divert a greater amount of resources to reproduction later in the season to sustain fruit maturation (Ågren, 1988; Delph et al., 1993; Gehring, 1993; Purrington and Schmitt, 1998). Trade-offs in biomass allocation between reproduction and growth can also lead to temporal variation in vegetative investment (Ågren, 1988; Krischik and Denno, 1990a; Elmqvist et al., 1991; Cipollini and Whigham, 1994). In this way, male growth becomes reduced early in the reproductive season, whereas female costs are borne later in the season (Delph et al., 1993). Thus, studies of intersexual differences in dioecious plants should consider resource investment across the entire reproductive season due to the contrasting phenologies of male and female individuals.
Patterns of resource investment were studied in male and female individuals in a natural population of the Neotropical dioecious shrub Baccharis dracunculifolia DC (Asteraceae) throughout one reproductive season. Possible consequences of reproduction on survivorship in both sexes were also investigated. Specifically, the following questions were addressed: (1) what is the sex ratio in a representative natural population of B. dracunculifolia; (2) are there temporal differences in reproduction and growth between males and females in B. dracunculifolia; and (3) are there intersexual differences in water status and shoot mortality of B. dracunculifolia?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study area
The study was conducted at the Campus of the Universidade Federal de Minas Gerais, Belo Horizonte, southeastern Brazil (19°30'S, 44°00'W), at 805 m a.s.l. The average annual temperature at the study site varies from 18 to 20 °C, and the average annual precipitation is 1500 mm. Most precipitation is concentrated in the rainy season, lasting from early November to late March; the dry season usually lasts from May to September. Vegetation on the campus is very heterogeneous and disturbed, being composed of natural, introduced, ornamental and fruit-bearing species. The adjacent native vegetation is composed of dry forest and cerrado (savanna) species (Ferrari, 1977). The study plants were all located in a 2 ha area at an early successional stage, with a predominance of B. dracunculifolia, grasses, and herbaceous and shrubby leguminous species (Araújo et al., 1995). Studies in this natural population have been conducted since 1991 (Lara and Fernandes, 1994; Araújo et al., 1995; Espírito-Santo and Fernandes, 1998, 2002; Espírito-Santo et al., 1999). Data on total monthly precipitation during the study period were obtained from the Pampulha Airport Weather Station, located approx. 1 km from the study site.
Study organism
Baccharis dracunculifolia is a widespread, perennial and woody dioecious shrub, 2–3 m in height, native to southeastern and southern Brazil, Argentina, Uruguay, Paraguay and Bolivia (Barroso, 1976). Flowering typically occurs twice a year: from late March to early June, and from late November to mid-December (Espírito-Santo and Fernandes, 1998). Flowers are tiny and densely aggregated into inflorescences (a capitulum), which are distributed throughout the shoots. Male flowers are pale yellow, whereas female flowers are white; inflorescences of both sexes are similar in size. Male and female capitula may last 3–5 d, and flowers usually open for 12 h, being visited by several different insect species, predominantly hymenopterans and dipterans (Silva, 1997b). Native social bees visit only male inflorescences in search of pollen and nectar. Nectar is not found in female flowers. Flies, solitary bees and wasps effectively pollinate female flowers (Silva, 1997b). After fertilization, several achenes are produced per capitulum, and seeds are wind-dispersed. Seeds are not produced without fertilization (absence of agamospermy; Silva, 1997b). There are no records of any species of Baccharis switching sexes.
Sex ratio
The sex ratio of this B. dracunculifolia population was determined using a single quadrat, 40 x 40 m, randomly located in the study area. Two perpendicular transects (x- and y-axis) of 100 x 100 m were demarcated to comprise the entire plant population. A unique number (from 40 to 60, to avoid the quadrat being located outside the population) was assigned at random for each axis. From this coordinate, the positions (north/south and east/west) of each quadrat side were randomly assigned. All individuals encountered inside this quadrat were marked in May 1997, during the peak of the reproductive season. Plant sex was determined through analyses of flower morphology. The proportion of male to female individuals was compared using a 
2 goodness-of-fit test (Zar, 1996).
Plant growth and reproduction
Sexual differences in reproduction and growth were analysed in 56 female and 52 male individuals, randomly selected in the field in February 1999. On each individual, all terminal shoots were numbered and two of these were selected at random and marked. The length of these two shoots was recorded every other week from March to August. Shoot relative growth rate was calculated as: (final length – initial length)/initial length, for each measurement date. This variable was log-transformed to meet the requirements of normality and homoscedasticity, and compared between males and females using a repeated measures ANOVA, with sex as grouping factor and date as repeated factor (Zar, 1996). Total numbers of immature (closed) and mature (open) inflorescences supported by each marked shoot were recorded weekly during the same period. As there was no relationship between the number of capitula and shoot length (P > 0·05 at all eight intervals, Spearman rank correlation test), the absolute number of inflorescences per shoot was used as a measure of reproductive investment instead of the number of inflorescences per unit of shoot length. This procedure allowed the use of data on reproductive investment obtained at dates when shoot length was not measured. The number of inflorescences was compared between sexes at each measurement date using a Mann–Whitney U-test, as the data were not normally distributed (Zar, 1996). To verify a possible trade-off between plant investment in reproduction and in current growth, the relationship between the total number of inflorescences and shoot relative growth rate was obtained at each time interval, for each plant sex, using a Spearman rank correlation test (Zar, 1996). The percentage of males and females that were flowering was calculated weekly.
Plant water stress and mortality
To verify the existence of intersexual differences in plant physiological responses to environmental conditions, the water status of each plant was measured four times during the study (February, April, June and August). Plant water potential represents the tension (negative pressure) in xylem vessels caused by leaf transpiration, and is the force driving water uptake from the soil (Scholander et al., 1965; Canny, 1995). Thus, plants under high water deficit have low water potentials, and vice versa. In this study, plant water deficit was assessed through pre-dawn measurements (between 0500 and 0600 h) of the xylem water potential. During this period, xylem water potential is usually at its daily minimum and is considered to be in equilibrium with soil water status (Choné et al., 2001). One fourth-level shoot, approx. 10 cm in length, was collected at random from each plant, and its water deficit measured. Individuals of B. dracunculifolia may have almost 150 such shoots during the dry season (146·8 ± 14·8, n = 30, M. M. Espírito-Santo, unpubl. res.), and sampling one shoot each month will have a minimal impact on plant water stress and future survival. Measurements were conducted using a Scholander Pressure Chamber (model 1003/603; PMS Instrument Co., Corvallis, OR, USA). This variable was compared between male and female plants using a repeated measures ANOVA with sex as grouping factor and date as repeated factor (Zar, 1996).
Shoot and plant mortalities were recorded every other week from March to August. At the end of study, the total number of dead shoots was compared between sexes using a 2 goodness-of-fit test (Zar, 1996). The expected number of dead shoots was calculated from the overall proportion of dead shoots in this population at the end of the study, regardless of plant sex. The same procedure was used to compare the mortality of male and female plants. All data are given as mean ± s.e.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sex ratio
The 40 x 40 m quadrat contained 921 individuals of which 391 were male, 307 female and 223 were juvenile or vegetative plants. The sex ratio was male-biased among the flowering individuals of this sample (1·27 : 1), and this difference was statistically significant (
2 = 5·05, d.f. = 1, P < 0·025).
Plant growth and reproduction
Variation in plant growth rate was similar for both sexes during the study period. Growth rates started to decline in late March, at the end of the rainy season, decreasing markedly during April and May, and reaching almost zero at the beginning of the dry season (June–July). However, growth rates tended to increase again at the end of the study period (late August) (Fig. 1). Plant growth varied significantly during the study period for both sexes (repeated measures ANOVA, within subjects, Time: F12,2568 = 33·1, P < 0·05), but the growth pattern did not differ between males and females (repeated measures ANOVA, within subjects, Time x Sex: F12,2568 = 0·86, P > 0·05). Overall, there was no significant difference in growth rate between male and female plants (repeated measures ANOVA, between subjects, Sex: F1,103 = 0·15, P > 0·05). There were no significant correlations between shoot growth rate and inflorescence number at each time interval for either male or female individuals (P > 0·05 at all intervals, Spearman rank correlation test).
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The population of B. dracunculifolia began flowering in early March. On average, males produced inflorescences earlier than females, with a greater proportion of male plants flowering throughout March (Fig. 2). The total number of inflorescences supported by males was significantly greater than that supported by females during the first month of flowering (Fig. 2). At the beginning of April the percentage of males flowering fell, resulting in a similar proportion of males and females flowering in the population. By late April, inflorescence production increased considerably, peaking in mid-May. During the period of high reproductive investment, almost all individuals of both sexes were flowering, and there were no intersexual differences in the total number of inflorescences supported (except on 7 May, see Fig. 2). At the end of the reproductive season (June), the percentage of flowering females was higher than that of males, and the total number of inflorescences supported by female plants was significantly greater than that supported by males. The gradual decrease in the total number of inflorescences sustained by females at the end of May indicates the process of fruit maturation, and contrasts with the abrupt decline in male reproductive effort in early June (Fig. 2).
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Plant water stress and mortality
Xylem water potentials remained constant from February until April, and increased in June. In August, at the end of the dry season, plant water potential reached its lowest value (Fig. 3). Xylem water potentials varied significantly during the study period (repeated measures ANOVA, within subjects, Time: F3,318 = 155·1, P < 0·05). There was no difference in the pattern of water deficit variation between plants of different sexes (repeated measures ANOVA, within subjects, Time x Sex: F3,318 = 0·51, P > 0·05), but males showed a significant lower overall xylem water potential than females during the whole study (Fig. 3) (repeated measures ANOVA, between subjects, Sex: F1,106 = 7·95, P < 0·01).
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Shoot mortality was low in March, showing a marked increase thereafter, mainly during July, in the middle of the dry season (Fig. 4). Shoot death was higher for female than male plants (
2 = 4·15, d.f. = 1, P < 0·05). By the end of the study, 43 female shoots had died (38·4 % of the total marked initially), whereas only 24 male shoots had died during the same period (23·1 % of the total marked initially). Mortality of female individuals (ten plants, 17·8 % of the initial number) was also higher than that of males (six plants, 11·5 % of the initial number) during the study period, but this difference was not statistically significant (2 = 0·83, d.f. = 1, P > 0·05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Phenological differences in reproduction between male and female individuals observed for B. dracunculifolia constitute a common pattern among dioecious plants (Lloyd and Webb, 1977; Ågren, 1988; Delph et al., 1993; Gehring, 1993; Purrington and Schmitt, 1998). Earlier production of flowers by males (compared with females) has been shown to be related to various factors, such as time of seed emergence (Purrington and Schmitt, 1998), competition among males for pollination opportunities (Stephenson and Bertin, 1983) and growth rates (Krischik and Denno, 1990a; Elmqvist et al., 1991). In this study, there were no differences in growth rates between males and females, a trend also observed in other studies of this species (Araújo et al., 1995; Espírito-Santo et al., 1999). Sexual differences in flowering phenology of B. dracunculifolia appear (at least in the past) to be the result of contrasting reproductive functions of males and females (pollen vs. seed production; and see Willson, 1979). Female costs are higher at the end of a reproductive session, when seed production is greater. Under resource limitation, an increased investment in attractive structures may decrease subsequent seed production (Vaughton and Ramsey, 1998). Since fruit maturation in B. dracunculifolia occurs during the dry season, a relatively high investment in inflorescences at the beginning of the reproduction season could have a negative effect the number of seeds produced later, reducing female fitness. At the same time, pollen donation may exert a strong selection pressure on male flowering time, since pollinators may preferentially visit early-flowering males throughout the season (pollinator assemblage phenomenon: Webb, 1976; Stephenson and Bertin, 1983), increasing the overall reproductive success of males that produce their flowers earliest.
Generally, a trade-off between reproductive and vegetative activities is observed for resource-limited plants (Krischik and Denno, 1990a; Herms and Mattson, 1992; Hemborg and Karlsson, 1999). Most studies into resource investment in dioecious plants have reported a reduced vegetative growth in female plants compared with that of males, as a consequence of a greater reproductive investment by pistillate individuals (Ågren, 1988; Bertin, 1989; Cipollini and Whigham, 1994). In this study, there was no relationship between inflorescence support and shoot growth rates in either sex. However, measurements of resource allocation that are more precise than shoot elongation and inflorescence number, such as reproductive and vegetative biomass, should be conducted to confirm the absence of a trade-off between growth and reproduction in this species. Nevertheless, a marked decrease in shoot growth was observed after the start of reproduction. This result suggests that individuals in this population cannot sustain the same levels of vegetative growth during flowering. As the plants supported inflorescences until June, this trade-off may be intensified by the onset of the dry season, in May, and by the resulting water limitation. In fact, shoot growth almost stopped between late May and early July (Fig. 1). During this period, female reproductive investment was higher than that of males, due to fruit maturation and seed production. This greater energy expenditure of females in periods of resource limitation did not lead to intersexual differences in current shoot growth rates. However, it may be reflected in the higher mortality of female shoots and plants compared with that of males, which had already ceased reproduction during the period of intense drought.
The greater mortality of female compared with male shoots (38·4 vs. 23·1 %) and female individuals (17·8 vs. 11·5 %) probably accounts for the male-biased sex ratio observed in this population. Several studies have addressed sex ratios in dioecious plants, and the majority has reported male-dominated populations to be more common (Lloyd, 1973; Lloyd and Webb, 1977; Opler and Bawa, 1978; Meagher, 1980; Ågren, 1987; Krischik and Denno, 1990a; Thomas and La Frankie, 1993; but see Freeman et al., 1976; Lovett Doust et al., 1987; Taylor et al., 1999). Biased sex ratios have previously been reported for B. dracunculifolia: Silva (1997a) reported that staminate plants dominated ten out of 11 populations of this species studied in areas experiencing different environmental conditions. This author did not observe any influence of population density or habitat quality (xeric and mesic sites) on sex ratios. Thus, it is likely that the skewed sex ratio observed in the present population is a consequence of sexual differences on plant phenology. Females invested more resources in reproduction than did males during the dry season, suffering from higher overall mortality than males despite having lower water stress during the entire study period. These results corroborate those of other studies which indicate a lower water requirement and higher survivorship under water limitation by males of dioecious species (Freeman et al., 1976, 1997; Waser, 1984; Ågren, 1987; Krischik and Denno, 1990a). Gender-specific differences in plant physiological traits, such as water-use efficiency and stomatal sensitivity to declining soil and air water content, have already been reported for dioecious species (Dawson and Bliss, 1989; Dawson and Ehleringer, 1993), and may be involved in the higher susceptibility of females of B. dracunculifolia to the effects of drought.
The sexually dimorphic patterns of resource allocation of B. dracunculifolia reported here probably constitute an indirect outcome of the distinct functions of each plant sex (pollen donation vs. seed production). Male reproductive effort was greater than that of females in the rainy season. In contrast, fruit production occurred during the dry season. This different flowering phenology did not lead to intersexual differences in plant growth (shoot elongation), but may have demographic consequences for this plant species, expressed as higher female mortality and male-biased sex ratios in natural populations. Other demographic parameters, such as seed germination and sapling survivorship, should be investigated to unravel the selection forces determining the timing of plant reproduction, which exposes females of B. dracunculifolia to higher reproductive investment during periods of resource scarcity.
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ACKNOWLEDGEMENTS |
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This manuscript was substantially improved by comments from Cláudia M. Jacobi and Jon Lovett Doust. We thank Carlos A. K. Miranda and Bernardo D. Ranieri for help during field work. This research was supported by Fapemig CRA 2519/97, IFS C/2487-1, CNPq 52·1772/95–8, and by the Postgraduate Program in Ecologia, Conservação e Manejo da Vida Silvestre of the Universidade Federal de Minas Gerais. We gratefully acknowledge a scholarship from the Conselho Nacional de Pesquisa e Desenvolvimento (CNPq) to M.M.E.S. This study was in partial fulfilment of requirements for the MSc degree at Universidade Federal de Minas Gerais.
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