Annals of Botany 89: 205-211, 2002
© 2002 Annals of Botany Company
Sex Ratio and Reproductive Effort in the Dioecious Juniperus communis subsp. alpina (Suter) 
elak. (Cupressaceae) Along an Altitudinal Gradient
1Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo. 1095, 41080 Sevilla, Spain
* For correspondence. Fax (+) 954557059, e-mail plortiz{at}us.es
Received: 24 July 2001; Returned for revision: 18 September 2001; Accepted: 29 October 2001.
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ABSTRACT |
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The hypothesis that reproductive cost differs between sexes was tested in Juniperus communis subsp. alpina along an altitudinal gradient. Sex ratio (male : female) increased significantly with elevation, and above 2600 m it was significantly male-biased. The reproductive effort was markedly greater for females than for males at all elevations. However, over 3 years of study, the growth of the females, measured as elongation of the main axes, was similar to that of the males. In both sexes, growth decreased with increasing elevation. Neither size of the ripe seed cones, nor the number of developed seeds per cone varied with elevation. The percentage of filled seeds was significantly greater at higher elevations indicating more favourable conditions for wind pollination in these stands. However, cone production decreased with elevation and so, reproductive success of J. communis subsp. alpina in Sierra Nevada decreases towards both upper and lower altitudinal distribution limits. The results do not support the hypothesis of differential reproductive cost between sexes; thus, alternative arguments to explain the altitudinal variation of sex ratio are discussed.
Key words: Juniperus communis, Cupressaceae, altitudinal gradient, cone crop, growth rate, reproductive effort, sex ratio.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In dioecious species, the resource investment in reproductive effort is usually greater for females than for males (Lloyd and Webb, 1977; Meagher and Antonovics, 1982; Lovett-Doust et al., 1987; Allen and Antos, 1988; Cipollini and Stiles, 1991; Korpelainen, 1992). Sexual differences in resource efforts may lead to greater physiological stress in the sex with greater reproductive investment (Dawson and Ehleringer, 1993; see Geber et al., 1999). This reproductive investment can affect growth rate, making it lower in the females than in the males (Lloyd and Webb, 1977; Allen and Antos, 1993). In extreme cases, the greater reproductive effort can lead to a higher mortality rate in females, and thus to populations with male-biased sex ratios (Meagher, 1981; Waser, 1984; Bierzychudek and Eckhart, 1988; Allen and Antos, 1993).
However, physiological and morphological mechanisms by which resource uptake is increased in females have been reported (see Geber et al., 1999). Sometimes the females predominate in habitats of high quality, increasing resource gain (Dawson and Ehleringer, 1993; Ramadan et al., 1994). Such a situation is frequent in anemophilous dioecious plants, with the females being situated in the deepest and best-drained soils, and the males in the more marginal zones or in more unfavourable environments with faster air currents; the latter would enhance male function, increasing opportunities for mating (Freeman et al., 1976; Bierzychudek and Eckart, 1988; Freeman et al., 1993).
Despite numerous studies on the possible consequences of reproduction differences depending on sex, the results obtained have been contradictory (e.g. in favour: Lovett-Doust et al., 1987; Cipollini and Stiles, 1991; Korpelainen, 1992; and against: Sakai and Burris, 1985; Gehring and Linhart, 1993). Likewise, disparate results have been found in the dioecious junipers. In Juniperus virginiana, the general sex ratio was male-biased, and males showed a greater representation among the larger diameter and taller trees suggesting that females have a greater reproductive cost; however, no differences in growth between the sexes were found (Vasiliauskas and Aarssen, 1992). In different populations of J. communis var. depressa, both male-biased and female-biased sex ratios have been found, but neither differences in growth, nor spatial segregation between the sexes have been reported (Marion and Houle, 1996; Houle and Duchesne, 1999). In six populations of Juniperus oxycedrus, the sex ratio scarcely deviated from unity, and segregation of the sexes by niche was seen only in one population (Ortiz et al., 1998).
The aim of the present work was to analyse consequences of differences in reproduction by sex in Juniperus communis subsp. alpina (Suter) 
elak., along an altitudinal gradient. In southern Spain, J. communis subsp. alpina populations tend to be dominated by adult individuals, non-reproductive individuals being very scarce (García et al., 1999). These populations occur between 1900 and 2900 m in elevation. At these altitudes, the environmental conditions are severe, and snowfalls are frequent; moreover, environmental severity and the period of snow cover increase considerably with elevation. If females allocate more resources to reproduction than do the males, in zones where the environmental conditions are more unfavourable, secondary differences between the sexes can be expected to be more marked.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study species and study site
Juniperus communis subsp. alpina is frequent in low zones of northern Europe and in the high mountains of central and southern Europe. It is a prostrate dioecious plant, less than 50 cm tall and up to 3 m in diameter. Branches in contact with the soil can root, and very often the oldest parts of the plants die, making its real age difficult to determine. The floral buds are formed at the end of summer, when shoot elongation finishes. Pollination takes place at the end of spring or beginning of summer of the following year. Fertilization takes place during spring of the second year, and the cones are ripe in the summer of the third year (Singh, 1978). Thus, females may bear up to three crops of female cones, in various stages of development.
The study was carried out in the Sierra Nevada (south-east Spain), where J. communis subsp. alpina grows on acid soils between 1900 and 2900 m in elevation. In the lowest zones, the juniper co-occurs with shrub taxa; above 2400 m, these thorny species become increasingly scarce, and disappear above 2600 m; in the highest zones, the juniper coexists with perennial herbaceous species or small chamaephytes (see Table 1).
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Methods
The sex ratio (number of male genets/number of female genets) was determined in six stands of J. communis subsp. alpina distributed along an altitudinal gradient (2100, 2150, 2350, 2500, 2700 and 2850 m; Fig. 1, Table 1). The sex ratio was determined during the pollination period by the presence of female or male cones. Although the branches of the individuals usually do not overlap, we were careful to sample only once from each individual, moving to the next clearly distinct individual before sampling again. At least 50 individuals were sampled in each stand. Non-reproductive individuals were also counted.
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Reproductive and vegetative characters were studied in three of the stands: at low elevation (2100 m), medium (2350 m) and high (2700 m). Hereafter, stands will be denoted by these elevations. In each of these stands, ten individuals (five females and five males) were chosen at random. The growth of each was estimated as the annual elongation of 30 randomly selected main branches during the years 1996, 1997 and 1998.
The production of pollen and seed cones was studied in five branches chosen at random on each individual. Cone production on these branches was counted directly in 1997 and 1998 (male cones were counted only in 1998). Ripe seed cones were collected from females and their length and width measured. The developed seeds were extracted from each ripe cone, counted and cut transversely, noting how many contained an embryo (filled seeds).
To ascertain if female individuals had greater reproductive effort (RE) than males, in 1998 RE was estimated following Bazzaz and Ackerly (1992). In five branches of each of the 30 plants, we measured resources allocated to vegetative function as the dry mass of shoot elongated in the current year, and those allocated to reproductive function as the dry mass of developing cones. In female individuals, all developing cones were considered; but given that females can bear up to three cone crops simultaneously, to avoid overestimating female reproductive allocation, the mass of 3-year-old cones and that of 2-year-old cones was divided by 3 and 2, respectively. Possibly, this still overestimates the cost of 2- and 3-year-old cones because cone growth is higher during the first year of development. The final dry masses of twigs and cones were determined after drying to constant mass at 70 °C. Rates of RE (g cone/g twig) of each sex were calculated.
Statistical analyses
Deviations from unity for the sex ratio of the six stands were verified using G-tests (Sokal and Rohlf, 1981). The relationship between sex ratio and elevation was determined by linear regression analysis. Differences in elongation were tested using an ANOVA for repeated measures; in this analysis sex, year and elevation were considered as fixed effects, and plant as a random effect nested in elevation. Differences in RE were tested using ANOVA tests of fixed effects. Differences in female cone production were tested using an ANOVA test for repeated measures considering year and elevation as fixed effects and plant as a random effect nested in elevation. A one-way ANOVA was used to determine the effect of the elevation on male cone production and female cone characters. When significant differences between elevations were shown (P < 0·05), these were located with Tukey LSD tests. Prior to any statistical analysis, variables with non-normal distributions were transformed to logarithms (base 10), and percentage values were arcsin transformed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sex ratios were strongly affected by elevation, with number of males increasing with elevation (R2 = 0·9366, n = 6, F1,4 = 59·19, P = 0·0015; Fig. 2). Sex ratios in stands situated at lower elevations did not differ significantly from unity (P > 0·05); however, the two stands above 2600 m showed a significantly male-biased sex ratio (P < 0·01). Non-reproductive individuals were very scarce; only four non-bearing cone plants were found during any of the annual samples: two at 2150 m, one at 2350 m and one at 2700 m.
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Growth of the individuals, measured as the mean annual elongation of the main axes, differed markedly between elevations (ANOVA, F2,6 = 242·85, P = 0·000002). The mean annual elongation decreased with elevation: at 2100 m all individuals had a mean annual elongation of 25·49 ± 1·4 mm, which decreased to 14·22 ± 0·7 mm in individuals of the stand situated at 2350 m, and to 9·88 ± 0·4 mm in the stand at 2700 m. Elongation was also markedly different between years (ANOVA, F2,12 = 60·62, P = 0·000001); growth in 1998 was greater than in 1997 and 1996, and this difference was much more marked at lower elevations (Fig. 3). In all the stands the growth of males was greater than that of females, but these differences were not significant (ANOVA, F1,6 = 1·75, P = 0·23). Elevation affected mean growth of females and males equally: in the stand situated at 2350 m, females and males grew 42 % and 46 % less than at 2100 m, respectively, and at 2700 m, the decrease in growth compared with that in the lowest stand was 58 % in females and 64 % in males (elevation x sex interaction was not significant, ANOVA, F2,6 = 0·66, P = 0·55; Table 2).
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Production of female and male cones was strongly influenced by the elevation at which the individuals were growing, and decreased with increasing elevation (Table 3). The median production of male cones in 1998 was 321·8 cones per branch at 2100 m, 112·4 at 2350 m, and 116·8 at 2700 m, but only at 2100 m was male cone production significantly higher than the others (Tukey LSD test, P < 0·05). The production of female cones differed significantly between years (ANOVA, F1,6 = 25·97, P = 0·0022) and elevations (ANOVA, F2,6 = 7·57, P = 0·0228). Fewer female cones were produced as elevation increased (Table 3), but only at 2100 m was cone production significantly higher than at the others (Tukey LSD test, P < 0·001 in 1997 and P = 0·0001 in 1998). The year x elevation interaction was also significant (ANOVA, F2,6 = 15·41, P = 0·0043) indicating that the crop of female cones in 1998 was larger than in 1997 in the stands at 2100 m and 2350 m, but not in the highest stand.
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The length and width of ripe female cones showed no clear patterns of variation with elevation (Table 4). Thus, cones from 2100 m were the longest, while those from 2350 m were the widest. Nor did seed production per cone vary with elevation: the median of the distributions was 1 in all the stands, and the mean ranged between 1·22 and 1·44 seeds per cone. However, the number of filled seeds per cone in the stand situated at the lowest elevation was significantly lower than in those situated at higher elevations (Table 4): in the lowest stand, only 2·51 % of seeds contained an embryo, against 59 % and 37·5 % in the medium and high stands, respectively. Taking into account both female cone production per branch and number of viable seeds per cone, the total number of viable seeds produced per branch was statistically different between elevations (F2,12 = 9·39, P = 0·00034). At 2350 m the total number of viable seeds produced per branch was five times higher (34·9 ± 8·9 seeds) than at 2100 m and 2700 m (6·34 ± 1·4 and 7·54 ± 1·6 seeds, respectively).
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Reproductive effort was higher in female individuals than in male individuals at every elevation, but no differences between elevations were found (Fig. 4). In 1998, females allocated a mean of 29·5 % of their current resources to reproduction, while males allocated only 5·8 %. ANOVA showed significant differences only between sexes (F1,6 = 8·20, P = 0·0286); moreover, none of the interactions were significant.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Our results support the notion of spatial segregation of the sexes in Juniperus communis subsp. alpina along an altitudinal gradient. Many dioecious plant species show spatial segregation by gender along a gradient of habitat quality, and it has been reported that most segregated species are wind-pollinated plants (see Shea et al., 1993), as are the junipers. The sex ratio in J. communis subsp. alpina ranged from unity to male-biased, increasing markedly with elevation and, therefore, with the presence of more adverse environmental conditions. A similar situation has been found in J. communis var. depressa along a latitudinal gradient, but in this case the southernmost population had a female-biased sex ratio (Marion and Houle, 1996). Likewise, spatial segregation of the sexes along a gradient of habitat quality has been reported in a population of J. oxycedrus with males being more abundant in drier places (Ortiz et al., 1998).
The predominance of males in perennial dioecious species can be explained by differences in age at the first reproduction (see Geber et al., 1999); the males often reach reproductive maturity before the females (Falinski, 1980; Allen and Antos, 1993). However, in J. communis subsp. alpina, only the stands situated at greatest elevation deviated significantly from unity, so that the difference in reproductive age cannot be taken as general in this taxon.
A difference in the mortality rates of females and males may be associated with differential reproductive cost between the sexes, which gives rise to considerable secondary differences between them, including demographic differences, which lead to biased sex ratios (Meagher, 1981; Waser, 1984; Bierzychudek and Eckhart, 1988). Several authors have shown that males allocate a higher proportion of resources to vegetative growth and suggested that this would give them higher tolerance to environmental extremes. Thus, it might be expected that a higher proportion of males would be found at the extremes of a species range (Grant and Mitton, 1979; Hoffman and Alliende, 1984). This agrees with our results in J. communis subsp. alpina, where a greater proportion of males occurs in the higher zone of its range. In this juniper, the reproductive effort of the females was always greater than that of the males. However, this greater effort did not imply a higher cost, given that vegetative growth was similar between the sexes. These results would indicate that females do not suffer a greater cost associated with the higher reproductive effort. Similar results have been reported in J. communis var. depressa where no consequence of a greater investment of females in reproduction was apparent (Marion and Houle, 1996). Nevertheless, differential efforts for reproduction between the sexes may also be expressed through other traits such as radial growth, number of branches, number of leaves per stem or root growth (Escarré et al., 1987, 1990; Tiedemann et al., 1987; Lovett-Doust and Lovett-Doust, 1988; Ramp and Stephenson, 1988; Jing and Coley, 1990; Korpelainen, 1992). Studies made in other junipers also failed to reveal differences between the sexes in some of these traits (Vasiliauskas and Aarssen, 1992; Marion and Houle, 1996). Alternatively, higher reproductive investment by females might be compensated for by exhibiting greater physiological abilities than males (see Geber et al., 1999).
The female reproductive cycle in J. communis subsp. alpina is extremely long, as the time taken for the receptive cones to ripen is at least 3 years (Singh, 1978). For approx. 1·5 years, the unripe cones are green and so may partially mitigate their energy cost via photosynthesis (Marion and Houle, 1996). However, the crops are accumulative, with each reproductive female plant maintaining simultaneously three crops of developing cones, and the cost could be high. Reproductive effort of the females could decrease if they did not produce cones every year. In dioecious species, the females commonly reproduce less often than the males (Bullock, 1982; Hoffman and Alliende, 1984). In J. communis subsp. alpina the female individuals in all the stands bore three concurrent cone crops, and even on the oldest branches, cones of previous crops could easily be observed (serotine cones, as in many cases they presented seeds with an embryo). However, the fact that there are significant differences among years in the crops of female cones at low and medium elevations suggests an alternation between good and poor crops, as is common in other conifers (Powell, 1977; Jordano, 1991; Arista et al., 1997). Such crop alternation could also alleviate the reproductive effort of females.
A decrease in the fruit-set could equalize the reproductive effort of males and females (Verdú and García-Fayos, 1998). In J. communis subsp. alpina, the number of female cones decreased with elevation but, even so, the reproductive effort of females was higher than that of the males. Under unfavourable environmental conditions, the reproductive effort of the females could be mitigated by producing low quality cones as well (Houle and Babeux, 1994). In Juniperus communis subsp. alpina, neither the size of the ripe cones nor the number of seeds differed among stands. The proportion of viable seeds was even greater in the higher stands. Some studies have shown a decrease in seed set or in seed mass in high elevations (Cruden, 1972; Hilligardt, 1993). Such studies were carried out in zoophilous species, and it has been argued that the unfavourable conditions on high mountains (e.g. low temperatures) reduce the abundance of pollinators (Heinrich, 1993). J. communis subsp. alpina is an anemophilous plant, so its pollination is favoured when the vegetation is open and the winds are strong (Dafni, 1992; Dawson and Ehleringer, 1993). In the lowest zones of Sierra Nevada, the juniper coexists with a stratum of dense shrubs consisting of larger plants that are a barrier to anemophily. With increasing elevation, the bush stratum accompanying the juniper disappears, and is replaced by small herbaceous and chamaephyte species. The more open structure of these communities and the strong winds typical of the high mountain favour anemophilous pollination. In conifers, one cause of reduced crops of viable seeds is pollination limitation (Owens et al., 1991; Arista and Talavera, 1996; Ortiz et al., 1998). In J. communis subsp. alpina, the number of male individuals is higher than that of females as elevation increases, and can duplicate in the highest stands. This increase in the proportion of male individuals means an increase in the pollen : ovule ratio, which will also favour the success of anemophilous pollination. Thus, as fruit set decreases with elevation and seed viability increases, the reproductive success of J. communis subsp. alpina in Sierra Nevada is higher at medium elevations and decreases towards both upper and lower altitudinal distribution limits. García et al. (2000) reported a similar situation in J. communis along a latitudinal range, the production of filled seeds declining gradually towards both northern and southern distribution limits, although cone production was not reported in that study.
In sexually dimorphic plant species, gender may be determined genetically, environmentally or by a genotype–environment interaction (Charnov, 1982; Lloyd and Bawa, 1984; Meagher, 1988; Pannell, 1997; Ainsworth, 1999). In J. communis, the system of gender determination is still unknown, but lability in sex expression has been reported in other juniper species (Freeman et al., 1981; Jordano, 1991; Vasiliauskas and Aarssen, 1992). In some populations of J. communis, monoecious individuals have been found (Ortiz et al., pers. obs.), which suggests some degree of sexual plasticity in this species. Thus, environmental influences on sex expression could also be involved in the elevational differences in sex ratio observed in J. communis subsp. alpina. Alternatively, differential ‘birth rate’ (Taylor, 1996) could also account for the biased sex ratio.
In conclusion, in Juniperus communis subsp. alpina, reproductive effort of females was always higher than that of males, but differences between sexes in shoot elongation were not found. The general sex ratio was male-biased, and this pattern was more evident as the elevation increased, indicating a higher tolerance of males to environmental extremes. The results do not support the hypothesis of differential reproductive cost between sexes. Further investigation on the system of sex determination and ecological aspects of the sex ratio are needed to understand the biased sex ratio in this taxon.
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ACKNOWLEDGEMENTS |
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The authors thank Drs T. E. Dawson, C. Freeman, K. Vrieling, M. Ronsheim and J. Lovett-Doust for their useful comments, which have improved the manuscript. This research was supported by a grant 4086 (Ayuda a los grupos de Investigación) from Junta de Andalucía and by the Spanish DGICYT (PB91–0070-C03–03) of the ‘Flora Iberica’ programme.
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  M. Onate and S. Munne-Bosch Influence of plant maturity, shoot reproduction and sex on vegetative growth in the dioecious plant Urtica dioica Ann. Bot., October 1, 2009; 104(5): 945 - 956. [Abstract] [Full Text] [PDF]
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 I. Bisang, J. Ehrlen, and L. Hedenas Reproductive effort and costs of reproduction do not explain female-biased sex ratios in the moss Pseudocalliergon trifarium (Amblystegiaceae) Am. J. Botany, September 1, 2006; 93(9): 1313 - 1319. [Abstract] [Full Text] [PDF]
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A. Sakai, A. Sasa, and S. Sakai Do sexual dimorphisms in reproductive allocation and new shoot biomass increase with an increase of altitude? A case of the shrub willow Salix reinii (Salicaceae) Am. J. Botany, July 1, 2006; 93(7): 988 - 992. [Abstract] [Full Text] [PDF]
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S. NANAMI, H. KAWAGUCHI, and T. YAMAKURA Sex Change Towards Female in Dying Acer rufinerve Trees Ann. Bot., June 1, 2004; 93(6): 733 - 740. [Abstract] [Full Text] [PDF]
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