Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux

Summary We examined the influence of differential reproductive frequency between the sexes on tertiary (phenotypic) sex ratios in the the dioecious tree Nyssa sylvatica (Nyssaceae). Reproduction was evaluated in relation to sex, size and canopy exposure using flowering data collected from 1229 marked trees over a four year period. For subsets of each population we used data on flower number, fruit crop size, fruit/flower ratios, and individual flower and fruit mass to compare biomass invested in reproductive structures of males and females. We also examined seasonal changes in stem nitrogen and soluble carbohydrate content in relation to flower and fruit production for trees of each sex. Our results indicate that: 1) Male-biased tertiary sex ratios could be explained by more frequent reproduction by male trees; 2) Estimated secondary sex ratios based on sums of all known males and females were not significantly different from 1:1; 3) Flowering frequency of males and females was significantly related to plant size (DBH) and exposure of the canopy to light; 4) Estimtes of reproductive biomass allocation ranged from 1.36 to 10.8 times greater for females relative to males; 5) Flower production was related to stem nutrient status for both sexes, but nutrient depletion and its effect on subsequent flowering was much more pronounced for female trees. We conclude that less frequent flowering by female trees may result from depletion of stored reserves, and that differential flowering frequency in N. sylvatica may ultimately reduce apparent sexual differences in the costs of reproduction.     

Patterns of reproductive effort in male and female shrubs of Oemleria cerasiformis: a 6-year study

1 We monitored flowering and fruiting of individual male and female plants of Oemleria cerasiformis over a 6-year period in a population in western Canada, and calculated fruit set (percentage of pistils maturing) and reproductive effort (RE) (gram of reproductive tissue per gram of leaf).
2 Over 6 years, male O. cerasiformis had on average much lower total RE, but much higher RE at flowering, than females.
3 In males, strong correlations between RE and light suggested that investment in reproduction was largely determined by light levels. There were strong positive correlations of RE between years, with no evidence of periodic fluctuations.
4 In females, in contrast to males, RE at flowering was not related to light. However, fruit set was strongly correlated with light. Flowering RE and fruit set were uncorrelated in females, indicating that these are affected by different factors.
5 Correlations of RE between years in females, although often significant, were lower than in males, indicating that RE fluctuates more between years in females than in males and may respond to past levels of RE. Flowering may reflect adjustments in response to past reproduction, or may be controlled by resources other than light. Fruit set was not significantly related to previous RE.
6 The greater total RE of females and their limited ability to adjust fruit set are probably major factors contributing to the greater mortality rates of females and the male-biased sex ratios in O. cerasiformis .     

Determinants of biased sex ratios and inter-sex costs of reproduction in dioecious tropical forest trees

Estimates of the sex ratio and cost of reproduction in plant populations have implications for resource use by animals, reserve design, and mechanisms of species coexistence, but may be biased unless all potentially reproductive individuals are censused over several flowering seasons. To investigate mechanisms maintaining dioecy in tropical forest trees, we recorded the flowering activity, sexual expression, and reproductive effort of all 2209 potentially reproductive individuals within 16 species of Myristicaceae over 4 years on a large forest plot in Amazonian Ecuador. Female trees invested >10 times more biomass than males in total reproduction. Flowering sex ratios were male-biased in four species in ≥1 year, and cumulative 4-year sex ratios were male-biased in two species and for the whole family, but different mechanisms were responsible for this in different species. Annual growth rates were equivalent for both sexes, implying that females can compensate for their greater reproductive investment. There was no strict spatial segregation of the sexes, but females were more often associated with specific habitats than males. We conclude that male-biased sex ratios are not manifested uniformly even after exhaustive sampling and that the mechanisms balancing the higher cost of female reproduction are extremely variable.     

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

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.     

Size,gender, and sex change in dwarf ginseng,Panax trifolium (Araliaceae)

Summary Flowering individuals of dwarf ginseng may be either male or hermaphroditic. I recorded the sex expression and size of individuals in three populations for three or four years in order to 1) determine whether this bimodal distribution of sex expression was due to sex changing or genetic dimorphism, and 2) test predictions about a) the relationship between size and gender, and b) the association of size change and sex change. Twenty five to 37% of the flowering individuals in each population changed gender from one year to the next. Of the plants I followed for four years, 83% changed sex and 57% changed more than once. In each of these populations as well as two others, hermaphrodites were significantly larger than males. Gender dynamics of the three populations differed, but hermaphrodites tended to become smaller and were more likely to change gender than remain hermaphroditic the following year, whereas males tended to grow larger and were more likely to remain male than to change gender. Dwarf ginseng is clearly a diphasic (sex changing) species in which sex expression is determined primarily by size. A difference between genders in the immediate resource costs of reproduction appears to be an important determinant of sex change and gender phase ratios in populations.     

Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree

Evolutionary selective forces, like predator satiation and pollination efficiency, are acknowledged to be major causes of masting (the variable, periodic and synchronic production of seeds in a population). However, a number of recent studies indicate that resources might also play an important role on shaping masting patterns. Dioecious masting species offer a privileged framework to study the role of resources on masting variation, since male and female plants often experience different reproductive costs and selective pressures. We followed masting and reproductive investment (RI) of the dioecious tree Juniperus thurifera in two populations along 10 years and studied the different response of males and females to experimentally increased water and nutrient availability in a third population. Juniperus thurifera females invested in reproduction three times more resources than males. Such disparity generated different resource‐use strategies in male and female trees. Tree‐ring growth and water use efficiency (WUE) confirmed that sexes differed in their resource investment temporal pattern, with males using current resources for reproduction and females using resources accumulated during longer periods. Watered and fertilized female trees presented significantly higher flowering reproductive investments than males and experienced an extraordinary mast‐flowering event. However, seeding RI and mast seeding were not affected by the treatment. This suggests that although resource availability affects the reproductive output of this species, there are other major forces regulating masting on J. thurifera. During 10 years, J. thurifera male and female trees presented high and low flowering years more or less synchronously. However, not all mast flowering episodes resulted in mast seeding, leading to masting uncoupling between flowering and seeding. Since flowering costs represent only 1% of females’ total reproductive investments, masting uncoupling could be a beneficial bet‐hedging strategy to maximize reproductive output in spite of unpredictable catastrophic events.     

Pollination biology and seed production of dioeciousCaryodendron orinocense (Euphorbiaceae) in a plantation in coastal Ecuador

Caryodendron orinocense Karst. (Euphorbiaceae) is an important neotropical, dioecious crop tree providing oil—and protein-rich seeds. Increases in size and number of leaves, flowers, and fruits were estimated for 100 trees in a plantation in costal Ecuador. Height increase was one meter per year—female trees grew less than non-flowering and male individuals. Trees matured at about 4 m height, but flowering and production of fruits remained low until tree height exceeded 8 m. Flowering and leaf production started at the beginning of the rainy season, and flowers were pollinated by large flies. Foliage damage did not seriously reduce leaf number nor fruit production. The plantation studied yielded 150 kg seeds per hectare per year. A plantation with 10 m high trees and a sex ratio of nine females per male will produce 500 kg seeds per hectare per year after about 12 years. Production will increase much more in older plantations.     

FLOWERING,SEX RATIOS,POLLEN-OVULE RATIOS,FRUIT SET,AND REPRODUCTIVE EFFORT OF A DIOECIOUS TREE,MYRISTICA INSIPIDA (MYRISTICACEAE), IN TWO DIFFERENT RAIN FOREST COMMUNITIES

The flowering of Myristica insipida R. Br. was studied in two rain forest communities in northern Queensland. This dioecious, subcanopy tree had a male-biased sex ratio at both study sites. In the lowland population the male-bias could be attributed to males (trees producing staminate flowers) starting to flower at a smaller average size than females (trees producing pistillate flowers). There were no intersexual differences in spacing or distribution within the study sites. Males trees flowered earlier, flowered longer, and produced over twice as many flowers as females during the study season. Although the onset of flowering was rather variable, 18–22 days following heavy rains, most trees had a synchronous period of maximum flowering. Pollination manipulations determined that there was no fruit development without pollination, and that increasing pollen loads resulted in increased fruit set with diminishing effect. Taking into account the sex-ratios and intersexual differences in flower production, the pollen-ovule ratio was calculated to be 16,000–19,000. Male trees were found to expend more energy on flowering than female trees. Open-pollination resulted in 1.0% of female flowers setting fruit. The much greater cost of fruit production resulted in females expending 421% more energy on reproduction than males. Fruit and seed production were judged to be pollination-limited. Nonetheless, this species exhibited several characteristics that are predicted if dioecy evolved by means of sexual selection.     

Sex ratios and clonal growth in dioecious Populus euphratica Oliv., Xinjiang Prov., Western China

Using a microsatellite assay, we investigated sex ratios at three levels (apparent, intrinsic, genet) for Populus euphratica stands in Xinjiang, China and possible consequences of sex-specific costs of reproduction in terms of clonal growth and individual growth or mortality. Sex ratios at all levels tended to be male biased (60 % of 3,295 flowering trees were male), although male excess was least pronounced at the genet level (52 % of 850 genets were male). Male clones comprised significantly more (708 vs. 572) trees than female clones. Reproductive investment was measured in terms of carbon (C) and nitrogen (N) contents of male and female reproductive organs: single flowers or fruit capsules, whole inflorescences or infructescences, and whole branches of ca. 2 cm diameter. Male flowers and catkins require less N than female fruits and catkins, but on average only 16 % of female catkins develop into fruits. This changes the measured investment for reproduction at branch level: now male branches spent 3.3 times more N than their female counterparts. This coincides with the annual increment of branches, measured as a possible trade-off for costs of reproduction: female branches needed 2 years less to reach a diameter of 2 cm. We conclude that full fruit set of females would give males a heavy comparative advantage, but frequent abortion of whole infructescences by females seems to be a powerful mechanism to compensate a higher reproductive effort, thus avoiding a pronounced runaway effect by more vigorous clonal growth of male trees over a long time.     

Sex ratio and gender-dependent neighboring effects in <Emphasis Type="Italic">Podocarpus nagi</Emphasis>, a dioecious tree

We analyzed sex ratio, growth rates, and spacing among individuals of Podocarpus nagi, a dioecious tree, on Mt. Mikasa, Nara City, Japan. The sex ratio of reproductive trees ≥ 5 cm in stem diameter at breast height (dbh, 130 cm above ground level) was significantly male-biased. The sex ratio was male-biased in the < 20 cm and ≥ 50 cm size classes, while it did not depart from 1:1 in the 20 ≤ dbh < 50 cm class. Growth rate varied with tree size in males but not in females. The precocity and vigor of males suggests that differences in reproductive costs between sexes induce the biased sex ratio. Random labeling tests on the positions of reproductive trees showed that in the < 30 cm class, males and females were distributed randomly and independently from each other. In the ≥ 30 cm class, males were significantly clumped, whereas females were randomly distributed. Males and females showed significant repulsion, i.e., a spatial segregation of sexes. Both intra- and intersexual effects on the growth rate of crowding by neighbors were significant for females, but not for males. Maximum competitive interference was observed at a distance of 5 m, which corresponded approximately to the radius of clumps of large males and to the significant repulsive distance between large males and females. These results suggest that sexual differences in sensitivity to local crowding are related to the formation of gender-dependent spatial patterns. Formation of female-repulsive male clumps and a male-biased sex ratio may intensify the decreased probability of regeneration near males, as suggested by the limited seed-dispersal range of this species, thereby promoting coexistence with other species.     

Reproductive investment in male and female Eurya japonica (Theaceae) at tree and branch levels

Intersexual differences in reproductive investments (RIs) (dry mass of reproductive tissue) at tree and branch levels in Eurya japonica were examined during two successive years. Mean total RIs per tree for males and females (adjusted for the mean trunk diameter in the combined sample trees, 25.7 mm) were 3.47 and 5.67 g dry mass. Females generally allocated about 1.6 times more biomass per tree to reproduction than males. On the other hand, male total RI per terminal branch averaged 51.6 mg dry mass and female averaged 226.6 mg. Females generally allocated about 4.4 times more biomass per terminal branch to reproduction than males. Thus, the magnitude of sexual difference at the tree level was much lower than that at the branch level. There were negative correlations between interyear fluctuation of total RI and stem diameter for both sexes. Interyear fluctuation of RI was greater for females than males in all size categories. This study revealed that conclusions from tree measures of RI differed from branch measures and suggested the importance of evaluating the average RI at the tree level for woody plants. I discussed the importance in adopting an effective sampling strategy for evaluating the RI at the tree level.     

Population structure and reproduction in the neotropical dioecious tree Compsoneura sprucei

Summary In rain forest study plots, the sexes of Compsoneura sprucei (Myristicaceae) were radomly distributed and similar in vegetative dimensions. The sex ratio among adults was estimated as 1.25 male: female. The population showed two flowering episodes per year, of unequal intensity. Sexual dimorphisms in order of increasing difference included the frequency of flowering, the number of flowers per inflorescence and the number of inflorescences per tree. Most females matured only 0–10 seeds per tree per flowering episode. Tree size was a better indicator of fecundity in males than females. Reproduction in both sexes was dominated by a very few prolific trees.     

Sex change towards female in dying Acer rufinerve trees

BACKGROUND AND AIMS: Sex changes within the genus Acer (Aceraceae) may occur because of associations of sex expression and plant health. In this study, a natural population of Acer rufinerve was monitored to clarify the sex change patterns, the relationship between sex expression and plant health, and the causal environmental conditions that precede sex changes. METHODS: Sex expression, growth rate and mortality of A. rufinerve trees in a natural population were monitored from 1992 to 1997. KEY RESULTS: Three types of sex expression were observed among A. rufinerve: male, female and bisexual. Among the three types of sex expression, sex changes occurred in all directions. In the growing season of 1994, precipitation was reduced. Stem growth rate decreased and mortality was high in 1994. In the spring of 1995, a drastic sex change from male to female or to bisexual occurred. As a result, the sex ratio became female-biased in 1995, although it had been male-biased from 1992 to 1994. In 1996 and 1997, the proportion of males in the population increased, partly as a result of female mortality and partly as a result of female-to-male sex changes. Sex expression of A. rufinerve was associated with their growth rate and mortality. The growth rate decreased for trees whose sex changed from male to female or to bisexual, and increased for trees whose sex changed from female to male or to bisexual. Dead trees reproduced as females before they died, except for those that died as males in 1994. CONCLUSIONS: One explanation for the sex change towards increasing femaleness for this A. rufinerve population in 1995 was the deterioration of plant health in the previous growing season, because of reduced precipitation. Sex changes of unhealthy and dying A. rufinerve towards femaleness may facilitate re-occupancy by offspring in gaps created by the death of A. rufinerve trees.     

Sex ratio of some long-lived dioecious plants in a sand dune area

In dioecious plants the fraction of males among flowering plants in the field (the secondary sex ratio) is the result of the fraction of males in the seeds (the primary sex ratio) and the subsequent survival and age at first reproduction of the two genders. It has been assumed that survival and age at first reproduction are the main determinants of biased secondary sex ratio but, especially for long-lived perennials, few data are available. We address this issue for natural populations of four long-lived perennials in a dune area. In Asparagus officinale and Bryonia dioica, the secondary sex ratio was unbiased. In Salix repens the secondary sex ratio was female-biased (0.337). Hippophae rhamnoides populations were male-biased; the average sex ratio of flowering plants was 0.658, while the fraction of males varied between 0.39 near the sea to 0.84 at the inland side of the dunes. The primary sex ratio was estimated by germinating seeds and growing plants under favourable conditions with minimal mortality. In S. repens the primary sex ratio in seeds was variable among mother plants and was, on average, female-biased (0.289). This is close to the secondary sex ratio, suggesting that the female bias already originates in the seed stage. In Hippophae rhamnoides the primary sex ratio was slightly male-biased (0.564). We argue that in this species, apart from the primary sex ratio, higher mortality and a later age at first reproduction for females contribute to the strong male bias among flowering plants in the field.     

Sex expression,sex change and fruiting habit in anAcer rufinerve population

Three hundred and thirty-eight plants ofAcer rufinerve Sieb. et Zucc. were monitored in a secondary deciduous forest for 5 years in terms of their sex expression and fruiting habit. Two types of flowers, functionally male and female, were recognized. The adult population consisted of constant males, inconstants and constant females. Constant males, plants that bore exclusively male flowers throughout the study period, accounted for 87% of the adult population. Thirty-four inconstant plants (11%) changed their sex in various ways. Constant females which accounted for only 2% of the population, were significantly smaller plants than the other two morphs, and suffered greater mortality. Fruit set was consistent and generally high for plants bearing female flowers. Thirteen juvenile plants out of 17 began reproduction during the 5 years, and all became male. For inconstant plants, fluctuation in sex expression tended to be more frequent and/or greater in magnitude for smaller plants. However, there was no evidence of the directional sex transition predicted by the size advantage hypothesis. Plant health and the successional stage of the stand should be taken into account as well as resource allocation problems to explain the proximate mechanisms of sex expression.     

Male-biased sex ratio and promiscuous pollination in the dioecious island treeLaurus azorica (Lauraceae)

Pollination ofLaurus azorica (Lauraceae), a dioecious Macaronesian tree, was studied. Male and female trees had the same size distribution. The population had 2.5 times as many male trees as females. In addition, males produced more flowers, and their inflorescences lasted longer. Individual flower lifetime and length of flowering season were the same in both sexes. Between the years of observation, one tree changed sex. Pollinators wereHalictinae bees and the flyTachina canariensis. The bees collected pollen and nectar and the fly collected nectar from both sexes. Both species visited other plants as well. The evolution of breeding systems inLauraceae is discussed.     

Effect of sex ratio,habitat factors and neighborhood competition on stem growth in the dioecious tree Fraxinus mandshurica

Growth rates of male and female trees are often different in a dioecious species. In this study, we analyzed sex ratios and the effect of gender, neighborhood competition and habitat factors on the stem growth of dioecious Fraxinus mandshurica trees in a secondary conifer and broad-leaved mixed forest in the Changbai Mountains of northeastern China. The sex ratio in the 5.2-ha study area does not deviate significantly from the expected 1:1 ratio, except for trees in the large diameter classes. For dbh >40 cm, the sex ratio is male-biased. This result suggests that males have a faster rate of stem growth than females, which is usually explained by the higher cost of reproduction in the fruit-bearing females. An analysis of the dbh distributions of two successive measurements showed that the rate of stem growth of the (27) females drops off with increasing dbh and remains below that of the (35) males. A causal model was used to analyze factors affecting the rate of stem growth, showing that these rates are affected significantly and positively by soil moisture and tree size in both genders and that within-gender competition is mainly for nitrogen. Our study suggests that neighborhood competition does not affect stem growth significantly, which is a rather surprising result.     

Effect of growth substances on flowering and sex expression in isolated apical buds of Spinacia oleracea

Apical buds of Spinacia oleracea L. cv. Matador were isolated from 7-day-old vegetative seedlings and grown in sterile culture under inductive long, or non-inductive short photoperiods. Flowering of isolated apices was inducible in long days in approximately 75% of the plants, and in short days by gibberellin treatment (about 40%) or by raising the temperature to 30–32°C (13%). In long days the percentage of flowering was further increased by gibberellin treatment (up to 90%), while it was unaffected by abscisic acid and was strongly decreased by Amo 1618 (55%). In long days the ratio of male to female plants was near 1. The percentage of female plants in long days was increased by gibberellins, and the percentage of male ones decreased by kinetin; as a consequence, the ratio of male to female plants was lowered to about 0.50 in both cases. Abscisic acid and Amo 1618 had the opposite effect, probably because they decreased the flowering in female plants, so that the sex ratio was shifted to 2.6 and 6.8, respectively. Simultaneous treatment with GA₃ reversed the effect of abscisic acid on the sex ratio, but the reversal of the shift to maleness induced by Amo 1618 was only partial. In short days, gibberellins also stimulated the flowering in female plants more than in male. However, when the flowering was induced by higher temperature, most flowering plants were male and kinetin increased their percentage further. The above results have been discussed in terms of different requirements for flowering in male and female plants.     

Do secondary sexual dimorphism and female intolerance to drought influence the sex ratio and extinction risk of <Emphasis Type="Italic">Taxus baccata</Emphasis>?

Sex ratio and sexual dimorphism were studied in the dioecious tree Taxus baccata. We examined five populations of T. baccata in Poland and Ukraine to identify the differences between male and female individuals. The sex of all individuals, height and diameter, needle length and area, specific leaf area (SLA), the number of stomata rows, stomatal density, and content of carbon and nitrogen were measured to identify the differences between male and female individuals. The relationship between sex ratio and climatic conditions, age and population size were analysed using data collected from the field and the literature. Female trees were shorter than males, but needles of females were longer and had larger area. Although there were no differences among sexes in SLA, nitrogen and carbon concentration, we found a positive correlation between nitrogen concentration and SLA among females. The sex ratio changed with tree height within populations, and taller height classes were biased in favour of males. Regardless of population age, the percentage of females within populations was positively correlated with precipitation. Probably high reproductive effort caused female trees to lose in competition with males, and this loss may also be enhanced by lower drought tolerance in females and could contribute to risk of extinction for T. baccata. The continental geographic range of T. baccata may be restricted by limited occurrence of females, which demand higher water resources than males.     

Haploid and diploid survival differences demonstrate selection in scale insect demes

Summary Black pineleaf scale insect populations are subdivided into genetically differentiated demes associated with individual pine trees. A comparison of sex ratios early and late in the life cycle demonstrated differences in the mortality experienced by haploid males and diploid females. Hatching ratios were significantly female-biased, and differential mortality increased this bias in ratios estimated just before adult male eclosion. The relative survival of males and females varied with overall mortality, causing a correlation between local densities and the surviving sex ratio. We suggest (a) that the genetic differentiation of scale demes results in part from selection pressures associated with individual pine trees, (b) that this differentiation entails an accumulation of locally adaptive traits within the scale subpopulation on each tree, (c) that expression of these adaptations in the haploid and diploid sexes may vary with their frequencies, and (d) that the surviving sex ratio thus offers a comparative measure of selection and the local adaptation achieved by the insects in individual demes.