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Sex ratios, size distributions, and sexual dimorphism in the dioecious tree Ilex aquifolium (Aquifoliaceae)¹

^a Dpto Biología Organismos y Sistemas,Unidad de Ecología, Universidad de Oviedo, E33071 Oviedo, Spain; and ^b Area de Ecología, Facultad de Biologia, Universidad de Santiago de Compostela, E15071 Santiago, Spain

	ABSTRACT

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Sex ratio and sexual dimorphism in physiology and growth were studied in the dioecious tree Ilex aquifolium at two localities in northern Spain. Genet sex ratio was significantly male biased in one locality but not in the other. However, ramet and flowering ramet sex ratios were male biased at both study sites. Males had significantly thicker main trunks than females in one locality and produced more ramets in the other. Growth rate, estimated from mean width of annual rings, did not differ between localities, but males produced wider rings than females at both sites. Mean annual growth rates over the last 10, 20, and 30 yr were significantly higher for males. Measurements of chlorophyll fluorescence indicated that the efficiency of photosynthesis of leaves on nonfruiting branches of females was higher than for leaves on branches of male plants under low-light conditions, though not under saturating-light conditions. Efficiency of photosynthesis was significantly lower on fruiting branches of female plants than on nonfruiting branches. We discuss whether the observed between-sex differences are attributable to the higher cost of reproduction in females and/or to pollen competition.

Key Words: Aquifoliaceae • chlorophyll fluorescence • dioecy • Ilex • physiological differentiation • sex ratio • sexual dimorphism • tree growth

	INTRODUCTION

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Females of woody dioecious plants usually expend proportionally more of their resources on reproduction and less on maintenance and growth compared to males (Lloyd and Webb, 1977; Willson, 1983). Specifically, males have been observed to be larger (Hoffman and Alliende, 1984; Vasiliauskas and Aarssen, 1992; Allen and Antos, 1993), to grow faster (Luken, 1987; Jing and Coley, 1990; Cipollini and Whigham, 1994), to survive for a longer period (Opler and Bawa, 1978; Lovett-Doust and Lovett-Doust, 1988; Allen and Antos, 1993), to exhibit a higher degree of clonal propagation, and to reproduce earlier and more frequently than females (Opler and Bawa, 1978; Bullock and Bawa, 1981; Bullock, 1982; Cavigelli et al., 1986; Lovett-Doust and Lovett-Doust, 1988; Thomas and LaFrankie, 1993). However, some studies have observed equivalent or even higher expenditure on reproduction in males and higher expenditure on growth in females (Grant and Mitton, 1979; Sakai and Burris, 1985; Willson, 1986; Sakai and Sharik, 1988; Davidson and Remphrey, 1990).

Little is known about gender specialization in physiology (Dawson and Ehleringer, 1993); however, sex-specific physiology (Freeman and McArthur, 1982; Dawson and Bliss, 1989; Dawson and Ehleringer, 1993) may lead to differences in carbon balance, which may result in sexual differentiation in growth and reproductive allocation. These differences may affect gender-specific size distributions and sex-ratio biases (Crawford and Balfour, 1983).

Following Allen and Antos (1993), three different sex ratios may be considered in populations of adult dioecious plants: (1) genet sex ratio (i.e., "secondary" genet sex ratio, the "primary" ratio being that at conception), (2) ramet sex ratio, and (3) flowering ramet sex ratio ("tertiary" or "phenotypic" sex ratio). A higher reproductive allocation by females may lead to increased mortality among female plants, and thus to male-biased genet sex ratios (Lloyd, 1973; Lovett-Doust and Lovett-Doust, 1988; Allen and Antos, 1993). Similarly, differences between males and females in ramet production or frequency of flowering as a consequence of higher reproductive allocation by females may lead to male-biased ramet or flowering ramet sex ratios.

The present study was designed to evaluate whether there is sexual dimorphism in physiological and growth traits in the dioecious tree Ilex aquifolium and, if so, to assess its possible consequences for size distributions. Intersexual differences in size distributions may be due to differences in the performance of each sex in different microhabitats (Bierzychudek and Eckhart, 1988; Dawson and Bliss, 1989, Dawson and Ehleringer, 1993). We therefore tested for spatial separation of the sexes and explored the extent to which there is between-sex physiological differentiation. In addition, we estimated genet, ramet, and flowering ramet sex ratios in the study population.

We selected this species because its allocation to fruit production is higher than its allocation to pollen production, which may result in a somatic cost of reproduction (Obeso, 1997). The cost associated with reproduction could be most easily met showing physiological specialization of both sexes (Dawson and Bliss, 1989) and a higher investment by females might be compensated for by exhibiting greater physiological abilities than males. Contrarily, it is also possible that a higher somatic cost (reduced growth) of females might result in a demographic cost of reproduction (lower ramet production and/ or higher mortality of females relative to males).

We specifically addressed the following questions. First, do sex ratios deviate significantly from 1:1? Second, are the sexes spatially segregated? Third, do males and females differ in vegetative growth rates, size distributions, and efficiency of photosynthesis? Fourth, do leaves on fruiting and nonfruiting branches of female plants differ in efficiency of photosynthesis?

	METHODS

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Study species
Holly, Ilex aquifolium L. (Aquifoliaceae), is a dioecious broad-leaved evergreen tree. It occurs in Europe and North Africa and is also commonly cultivated (Peterken and Lloyd, 1967).

The genus Ilex is entirely dioecious (Carr, 1991), though occasional hermaphrodite trees and male-to-female sex changes have been observed (Peterken and Lloyd, 1967). The flowers are clumped in axillary positions on shoots produced the previous year. The fruit, which ripens in autumn, is a drupe containing four pyrenes, which are typically bird dispersed.

Vegetative spread by suckers arising from shallow lateral roots and producing clonal clumps of trees is also common. Under heavy browsing, plants remain as low shrubs. Reproductive allocation (the ratio of mass of sexual structures to branch mass) at our study sites was 56 ± 87% (mean ± 1 SD) of branch dry mass for females at fruiting (N = 60 branches from ten trees) and 7 ± 3% for males at flowering (N = 30 branches from ten trees; Obeso, 1997).

Study sites
The study was conducted at two localities (Pome Forest and Grandiella) in the Cantabrian Range (Asturias, northern Spain), where holly is a common understory tree. Pome Forest is located in the Picos de Europa National Park (950 m a.s.l., 43°16'N, 4°59'W). It is a beech forest with Ilex aquifolium and Crataegus monogyna in the undergrowth. Grandiella (Sierra del Aramo, 1050 m a.s.l., 43°14'N, 5°55'W) is an area of pastures with second-growth forest dominated by Ilex aquifolium, Crataegus monogyna, Sorbus aria and S. aucuparia are also present.

Despite high seedling production, seedling recruitment of shrubs and trees is rare at both sites, because browsing ungulates (mainly cattle and horses) are abundant and consume most of the saplings. At Grandiella, small shrubs are rare but most trees show a dense mass of branches on their heavily browsed lower part. In Pome Forest, holly shrubs are heavily browsed, but the taller holly trees are scarcely affected because of the height of their canopy. Suckering is frequent in the clumps of stems at Grandiella, but rare in Pome Forest, where browsing herbivores consume the suckers because they are not protected by a dense mass of branches.

Sampling procedures
Each clump of trunks was considered a genet, and each individual trunk a ramet. Assigning trunks to genets was not difficult because trunks from the same genet normally grow in a circle and genets are far from each other. We selected all the trees included in a previously delimited area. Trees selected at Pome were tagged to examine for mortality and damage. The diameter-at-breast-height (dbh) and sex of each trunk were recorded for at least 200 genets at each study site. Within each genet, the widest trunk was considered the main trunk. Non flowering trunks were rare at Pome but common at Grandiella, where they were assigned to the same sex as the flowering trunks of that genet. A total of 630 trunks were sexed (388 males and 242 females) and measured. Only one tree was monoecious; it was included as a male because ovulate flowers were confined to one branch.

To test for spatial segregation of sexes, distances to the nearest male and female were measured for a randomly selected subset of 53 male and 53 female genets in the Pome forest. This locality was selected because most of the trunks were isolated (vegetative propagation was rare), and there were no small non reproductive trees.

Growth rates were estimated by measuring annual tree-ring widths. At each locality, one or two cores were taken from each of 15 healthy trees of each sex using a Pressler bore. The cores were mounted on wooden strips and sanded, and annual-tree ring widths were measured to the nearest 0.01 mm with a sliding-stage micrometer for as many years as possible. Heart rot made the ring widths for the earlier years in some cores from Pome difficult to decipher, so age was underestimated for some trees. For each sex and locality, growth-rate estimates were based on ten trees in which annual rings for the last 30 yr were clearly identifiable.

To examine tree mortality, 204 trees in Pome, sexed in May 1995, were examined for damage in September 1996. We recorded the sex of the trees that sustained major damage or were dead. We included standing broken stems, fallen trees, and dead trees (Matelson, Nadkrni, and Solano, 1995).

Efficiency of photosynthesis
The plant material consisted of 30 3rd-yr plants (15 of each sex), growing with optimal fertilization and water supply in 7-L pots containing a 3:1 mixture of seedling substrate (Pindstrup Plus-Blue, based on 70% blond peat, 30% black peat, and added nutrients) and perlite (Silvaperl Products Ltd., Harrogate, Yorkshire, UK). Plants were grown from randomly selected seeds, from stock from the Cantabrian Range, at the field station of the University of Santiago (42°53'N, 8°32'W, 260 m a.s.l.), under natural light and temperature conditions. At the time of the experiment female basal diameter averaged 10.33 ± 1.07 mm [N = 15] and male basal diameter 10.37 ± 1.13 mm [N = 15]. There was a mean of 113.60 ± 38.28 leaves for female plants and 105.27 ± 39.79 leaves for male plants. All but two of the female plants produced mature fruits at the time of the experiment (mean number of fruits per plant = 8.1, SD = 10.6, N = 13).

Efficiency of photosynthesis was evaluated on the basis of measurements of chlorophyll fluorescence. In vivo chlorophyll a fluorescence measurements were taken in the afternoon (from 1450 to 1610) on two different days in December 1996, using a portable pulse-amplitude-modulated fluorometer (PAM 2000, Walz, Effeltrich, Germany) which works by the saturation pulse method. On 4 December, a completely cloudy day, photosynthetically active radiation (PAR; measured with a LI-COR 190 SA Quantum Sensor, LI-COR, Lincoln, Nebraska, USA) reaching the leaf ranged from 5 to 9 µmol photons · m· s, as compared with a maximum of 54 µmol photons · m · s above the canopy during the period of measurement. On 9 December, a clear day without clouds, PAR at the leaf surface ranged from 501 to 674 µmol photons · m · s, as compared with a maximum of 1441 µmol photons · m · s overhead. On both occasions, we performed standardized chlorophyll fluorescence measurements on the upper surface of intact current-year leaves. On each female plant we measured fluorescence on six leaves (three on fruiting branches and three on non fruiting branches); on male plants we took measurements on each of three leaves per plant. The fluorescence parameters recorded were as follows. The effective quantum yield of photochemical energy conversion, or energy capture efficiency of the photosystem II open centers, was assessed by the yield parameter Fv'/Fm' (Genty, Briantais, and Baker, 1989), where Fv' = Fm' - Ft, Ft is the measured fluorescence under the natural light obtaining, and Fm' is the maximal fluorescence reached in a pulse of saturating light with an illuminated sample (i.e., fluorescence reached when the pool of primary quinone electron acceptor, QA, of the photosystem II reaction centers is fully reduced, and hence photochemistry impeded. For nonstressed, dark-adapted plants from widely diverse taxa, habitats, and with diverse leaf structures, the ratio Fv'/Fm' is typically in the range 0.75-0.85 (Björkman and Demmig, 1987; Bolhár-Nordenkampf et al., 1989). Stress factors, affecting mainly PSII function, reduce the value of this ratio (Krause and Weis, 1991). The quantum efficiency of the photosystem II photochemistry (PSII) in leaves operating at steady-state photosynthesis under the PAR obtaining was determined as the product (Fv'/Fm') qP (Genty, Briantais, and Baker, 1989), where qP is the photochemical quenching coefficient of fluorescence, representing the proportion of photosystem II reaction centers that are open.

Statistical analyses
To determine whether there were differences in growth rate between sexes and/or between localities, a series of two-way mixed-model (random factor locality, fixed factor sex) analyses of variance (ANOVA) were performed, the response variable being tree-ring width year by year (1–10) before 1994, or mean tree-ring width over the 10, 20, or 30 yr before 1994. The tree-ring width data were subjected to logarithmic or reciprocal square-root transformations to obtain homogeneity of variances and maximum fit to normal distributions.

Between-sex differences in chlorophyll fluorescence parameters were evaluated using one-way analysis of variance (ANOVA). To investigate possible effects of reproductive status of female branches (flowering or nonflowering) on fluorescence parameters, we used ANOVA with two factors (plant and branch reproductive status). To obtain independent data we used only one branch per tree. Tests for homoscedasticity indicated that no transformations were needed for these data.

Means are cited ± 1 SD, with sample size in parentheses.

	RESULTS

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Sex ratios and size distributions
The genet sex ratio was significantly male biased in Pome but did not differ significantly from 1:1 in Grandiella (Table 1). Ramet sex ratios were male biased at both sites. The proportion of male ramets was higher in Grandiella than in Pome, where vegetative propagation was scarce. At both sites, the ramet sex ratio differed little or not at all from the flowering ramet sex ratio (Table 1).

View larger version (30K): [in this window] [in a new window]   Fig. 1. Size distributions (diameter at breast height, dbh, in cm) for main trunks of male and female plants (genets) in the Pome (N = 200) and Grandiella (N = 200) populations.

Nearest-neighbor distances
In Pome, the sex of the nearest-neighbor genet was independent of genet sex (Table 2), i.e., there was no significant spatial association of the sexes. The average distances to the nearest male and the nearest female neighbors were likewise not significantly different, regardless of whether males or females are considered (Table 2).

Plant growth rate
The trees used for measures of annual tree-ring width showed a mean dbh (diameter at breast height) of 26.3 ± 4.8 cm (20) in Pome and 23.9 ± 10.7 cm (20) in Grandiella; the two means do not differ significantly at the 5% level. Mean estimated age was 162 ± 45 yr at Pome and 75 ± 12 yr at Grandiella. Neither dbh nor age differed significantly between sexes (results not shown). We found no significant relationship between dbh and tree age.

Investigation of the influence of sex and locality on tree-ring width (TRW), by a series of two-way ANOVAs each considering the data for a single year from the period 1985–1994, did not reveal any significant effects (results not shown). However, significant effects of sex were detected when the response variable in ANOVA was 10-yr mean (1985–1994), 20-yr mean, or 30-yr mean TRW (Table 3, Fig. 2); this indicates that there is a cumulative effect that is not detected when only single years are considered. Females had slower growth than males but we did not detect any significant effects of locality (Table 3, Fig. 2).

View larger version (15K): [in this window] [in a new window]   Fig. 2. Mean ring width (+ 1 SE, N = 10) over the last 10, 20, and 30 yr, for main trunks of male and female plants (genets) from the two localities. White bars: Pome. Black bars: Grandiella.

	DISCUSSION

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This study shows that there is sexual dimorphism in some physiological traits and growth parameters in Ilex aquifolium. Male trees grew faster, and the leaves of nonfruiting branches of female plants showed better photosynthetic efficiency than leaves of fruiting branches and of male plants.

The slower growth of females might be attributed to the higher outlay on reproduction, i.e., the greater allocation of resources to reproduction relative to the males (Obeso, 1997). However, such effects usually need periods of time >10 yr to be detected at tree level; this may be attributable to pronounced interindividual variation in growth rate and/or the fact that the costs of reproduction are often deferred. Deferred costs have been reported for a number of woody and herbaceous perennials (Primack and Hall, 1990; Newell, 1991). However, Jing and Coley (1990) found between-sex differences in ring width in Acer negundo in 7 of 10 yr studied.

In species like Ilex aquifolium, in which resource allocation to reproduction is considerably higher among females than among males, it seems likely that there will be strong selection in favor of females who are able to minimize the negative effects of this greater outlay (Jönsson and Tuomi, 1994), whether (a) by deferring the negative effects to subsequent years, or (b) by using their remaining resources more efficiently (see, for example, Dawson and Ehleringer, 1993; Kohorn, 1994; Delph and Meagher, 1995). As a result of responses of this type, it may be rather difficult to detect the "costs" (i.e., negative effects) of the greater outlay of females on reproduction. The results of the present study suggest that females of Ilex aquifolium counter the greater outlay on reproduction in at least three ways. First, females in the Grandiella population show less vegetative propagation than males. Second, under low light, photosynthesis (as measured by Fv'/Fm' and PSII ) was more efficient in leaves of nonfruiting branches of females than in leaves of male branches. Third, green fruits themselves show photosynthetic activity (R. Retuerto, personal observation), thus presumably contributing at least a small proportion of the resources required for their production (Bazzaz, Carlson, and Harper, 1979).

Chlorophyll fluorescence analysis has been offered as a convenient alternative to gas exchange measurements for determination of photosynthetic performance of plants and their stress limitations (Schreiber, Bilger, and Neubauer, 1994). It has been extensively demonstrated that changes in fluorescence emissions correlated with the quantum efficiency of O₂ evolution (Schreiber, Neubauer, and Klughammer, 1988; Lovelock, Jebb, and Osmond, 1994) and CO₂ assimilation (Genty, Briantais, and Baker, 1989; Demmig-Adams et al., 1990; Andrews, Fryer, and Baker, 1995; Edwards and Baker, 1993). As far as we know, this is the first study to demonstrate between-sex differences in physiology through the analysis of chlorophyll fluorescence emissions. As indicated by other reports, physiological specialization may aid each sex in meeting different resource demands associated with reproduction (Bourdeau, 1958; Crawford and Balfour, 1983; Dawson and Bliss, 1989, 1993; Dawson and Ehleringer, 1993).

In species in which the reproductive activity induces an increase in rates of photosynthesis, the magnitude of the increase may be dependent on the size of the sink (Neales and Incoll, 1968; Gifford and Evans, 1981). The source–sink hypothesis states that the cost of mobilization and active transport favors local sinks over more distant ones. Unexpectedly, we observed that leaves on nonfruiting branches of female plants exhibited significantly better photosynthetic efficiency than leaves on fruiting branches. Similarly, Karlsson (1994) has observed a cost of reproduction in terms of CO₂-assimilation capacity of the branch, suggesting that reproduction affects nutrient utilization by nearby leaves, causing a decrease in photosynthetic capacity by lowering the leaf nitrogen content. This variation between branches confirms that plant canopies may not be completely integrated, but consist of subunits that differ physiologically (Watson and Casper, 1984; Sprugel, Hinckley, and Schaap, 1991). Dawson and Bliss (1993) have pointed out some consequences of these observations with regard to our ability to generalize about a plant's responses within or across environments, and on within-canopy and whole-canopy fitness.

Under high-light intensities, above those reported by Peterken and Lloyd (1967) as saturating for 1st-yr leaves of holly, both sexes performed equally badly, with abrupt decreases in PSII and Fv'/Fm'. Abrupt decreases in Fv'/Fm' under high-light intensities have been interpreted as a symptom of photoinhibition (Andrews, Fryer, and Baker, 1995). Our results indicate that the environmental context is crucial to understanding between-sex differences in physiology; specifically, between-sex physiological differences may exist only under certain conditions. Our results are also consistent with the reported better performance of females in less stress-prone habitats (Freeman, Klikoff, and Harper, 1976; Dawson and Ehleringer, 1993). However, we failed to detect any evidence of spatial separation of the sexes in Pome.

In previous studies of holly, Peterken and Lloyd (1967) and Kay and Stevens (1986) reported no significant departure from a 1:1 sex ratio. However, the results of Richards (1988) and the present study indicate the genet sex ratio (GSR) is male biased in some localities. In the present study, the GSR in the Pome population (1.4:1) was significantly male biased, while that in the Grandiella population (1.27:1) approached significance (P < 0.09); despite these results, however, we did not detect any significant between-sex difference in genet mortality rate. Ramet and flowering ramet sex ratios were significantly male-biased in both of our study populations, though the bias was particularly pronounced in the Grandiella. Male-biased ramet sex ratios are attributable to greater production of ramets by male trees and/or higher ramet mortality among females. Greater production of ramets by male trees may largely explain the male-biased ramet sex ratio in Grandiella, where vegetative propagation is much more frequent than at Pome (because trees have a dense mass of branches with spiny leaves at their base, which protects suckers from browsing herbivores).

Flowering ramet sex ratio was coincident with ramet sex ratio because most ramets flowered; however, there were huge differences among ramets in flower density, with some flowering female ramets producing only a few flowers. Flower density tends to be higher in males (Obeso, 1997).

Many cases of male-biased sex ratio in plants have been attributed to the higher cost of reproduction in females (Ornduff ,1985; Allen and Antos, 1988, 1993; Cipollini and Stiles, 1991; Vasiliauskas and Aarssen, 1992; Dawson and Ehleringer, 1993). However, insufficient data are presently available to establish whether this is a general phenomenon in woody dioecious plants.

The fact that male trunks at Grandiella were no larger than female trunks despite faster growth by males may be attributable to the age of the trees: specifically, the trees at this site have low mean dbh and are probably too young to reflect the effect of the higher cost of reproduction in females. Trees in Pome are old enough to show sexual dimorphism in size, though it should be stressed that between-sex differences in size may be due not only to slower growth of females but also to higher female mortality; indeed, the higher mortality among females may be at least partially a consequence of slower growth. In addition, female mortality may be higher under stress conditions or in particular microhabitats (Bierzychudek and Eckhart, 1988; Allen and Antos, 1993). Our data from Pome do not support the possibility that females suffered higher mortality than males. Therefore, the male-biased sex ratio and sexual dimorphism in size observed in Pome should not be attributed to higher female mortality, at least at the adult stage. However, data presented here might not be enough to test this issue.

Slower growth of female plants of Ilex aquifolium (a putative "somatic cost" of reproduction) has been demonstrated recently by Obeso (1997); in the present study, however, a "demographic cost" of reproduction was not clearly demonstrated (i.e., higher mortality and/or lower ramet production among females). In fact, the larger size of males may be due to between-sex differences in resource allocation patterns, or to sexual selection, rather than to differences in cost of reproduction. For example, a male that is larger than neighboring males may produce more flowers and thus have greater success as a pollen donor (Willson, 1994). In this connection, Carr (1991) found that increasing investment in reproduction by males of Ilex opaca clearly conferred competitive advantage. In Ilex aquifolium, the pollen competition hypothesis is supported by the fact that flowering period is longer and flower production higher in males than in females (Obeso, 1996, 1997). However, it is very difficult to design a experiment to discriminate between these different hypotheses, since they are not mutually exclusive.

	FOOTNOTES

 
¹ The authors thank Esteban Cabal, Nacho Fernández-Calvo, and Puerto Menéndez for continuous help in field work. Guy Norman corrected the English. The staff of the Picos de Europa National Park kindly granted permission to conduct field studies in the Pome Forest. This research was supported by a C.I.C.Y.T. grant (PB94-1538).

⁴ Author for correspondence.

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