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2 Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810, Japan; and 3 Uryu Experimental Forest, Faculty of Agriculture, Hokkaido University, Nayoro 096-0071, Japan
Received for publication October 1, 1998. Accepted for publication January 4, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Araceae • flowering performance • gender change • heat production • protogyny • size-dependency • Symplocarpus renifolius.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Galen, Gregory, and Galloway, 1989
; Bertin, 1993
; Imbert and Richards, 1993
). During the flowering season, the number of flowers with staminate (male) and pistillate (female) phases in a population is expected to change from male biased to female biased in a protandrous population and from female biased to male biased in a protogynous population (Thomson and Barrett, 1981
; Devlin and Stephenson, 1987
; Pellmyr, 1987
). Under such conditions, the timing of flowering and gender shift greatly affect the reproductive success (hereafter, RS) of individual plants through the male and female functions (Campbell, 1989
; Molau, 1991
). In some cases, the coexistence of various sex-expression types occurs within a population (Pellmyr, 1987
; Schlessman, Underwood, and Graceffa, 1996
; Ramirez and Berry, 1997
). For example, Cimicifuga simplex usually produces protandrous hermaphroditic flowers, but some plants having purely male or female flowers exist within a population. The female individuals bloom in the early season when the functional sex ratio of the dominant hermaphroditic plants is male biased, while the male individuals bloom in the late season when the sex ratio is female biased (Pellmyr, 1987
).
Even when variations in sex-expression types do not occur, the floral sex allocation of sequential hermaphrodites is expected to change. In the case of protandry, early-blooming hermaphroditic flowers are expected to invest more resources in female function, while late-blooming flowers should favor male function, according to the prediction of the Evolutionary Stable Strategy model presented by Brunet and Charlesworth (1995)
. Switching the time of the sex phase may influence the RS of sequential hermaphrodites when the functional sex ratio within a population varies during the flowering season. In a protogynous population, early flowering and rapid change in sex expression from female to male may increase paternal success through pollen donation because the sex ratio of the population is extremely female biased at the beginning of the flowering season. In contrast, plants with delayed flowering phenology may reduce their paternal success due to low proportion of female-phase flowers within a population. If competition among pollen donors promotes the differentiation in temporal gender allocation via paternal RS (e.g., Stephenson and Bertin, 1983
; Sutherland and Delph, 1984
; Schlessman, Underwood, and Graceffa, 1996
), there could be directional selection for precocious males to take advantage of the female-biased sex ratio of the population.
Symplocarpus renifolius Schott ex. Miq. is a hermaphroditic perennial herb blooming in early spring under the humid broad-leaved deciduous forests of northeastern Asia. Each plant produces one or two exothermic spadices (succulent spike) bearing 
100 protogynous flowers. The flowering progresses basipetally for each spadix, resulting in an expression of different sexual phases over time. The female phase and the male phase take 6.8 ± 5.8 d (SD) and 16.7 ± 5.7 d, respectively, with a short transitional bisexual phase of 2.1 ± 0.9 d (Uemura et al., 1993
). The spadices do not produce nectar, but they produce heat. Heat production is also well known in S. foetidus, an allied species in North America, and it is considered to relate to pollinator attraction as a reward itself, as well as enhancing the emission of carbon dioxide or a fetid odor, which is thought to mimic that of mammalian feces or carrion (Moodie, 1976
). The other evolutionary significance of heat production in thermoregulating plants is that the flower itself may require a constant temperature for the proper development of its own reproductive structures (Seymour, 1997
). Heat production of the spadix in S. renifolius is conspicuous only in the female and bisexual phases and abruptly decreases in the male phase when the elongation of stamens and the dehiscence of anthers mostly finish (Uemura et al., 1993
). This suggests that the heat production of the spadix may influence the phenological development of pistils and stamens. If early flowering and rapid sex change are costly, the ability to produce heat, the timing of flowering and sex change, and the RS through male and female functions should correlate with plant size, i.e., the amount of resources stored. Especially in early spring, the development of floral organs is restricted by cool temperature, and plants may require considerable energy (= resources) for the quick growth of flowers by means of some enzyme- and/or temperature-dependent physiological processes (cf. Seymour, 1997
). It would, therefore, be expected that larger plants can bloom earlier and change their gender from female to male more rapidly than smaller ones; thus larger plants can improve their RS as pollen donors change. In this paper, we discuss the importance of flowering behavior on RS through male and female functions and the relationship among plant size, ability to produce heat, and phenotypic performance of the two sexes in S. renifolius.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In a natural population of S. renifolius, low temperature during the flowering season (mid-April to late May) may result in very low fruit set (10%) and seed production (1%), probably due to low activity of pollinating insects (Uemura et al., 1993
; Wada and Uemura, 1994
). This study was conducted on a natural population of S. renifolius within a deciduous forest near Sapporo, northern Japan (43°03' N, 141°31' E). The mean annual temperature of the study site is 8.0°C, with the maximum of the mean monthly temperature, 20°–21°C, occurring in July or August, and the minimum, -5°C, in January (data from the records of Japan Meteorological Agency). The floor of this forest is thickly covered with snow from December to April and then flooded with melt water in spring.
Estimation of biomass and ovule number
The basal diameter of the vegetative stems and the biomass were measured on 38 plants in the population in the summer 1992 (at a time of full growth of aboveground parts) in order to estimate total plant size. We dug out whole individuals, oven-dried them, and measured the dry mass. The relationship between the basal diameter of stem and dry mass was: lny = 2.76lnx + 4.80, r2 = 0.890, and P < 0.001, where x and y are the basal diameter (mm) and dry mass (g) of a plant, respectively. We counted the number of flowers for other 48 fertile plants and obtained the following allometric relationship: lnz = 0.031lnx + 3.605, r2 = 0.760, and P < 0.001, where x and z are the basal diameter (mm) and the number of flowers, respectively. These measurements indicate that the basal stem diameter can be used with high confidence as a nondestructive estimator of the biomass and the number of ovules.
Flowering phenology, gender expression, and sex ratio
At the beginning of April 1993, we arbitrarily selected 112 plants of S. renifolius, on which we labeled 145 spadices (33 plants had two spadices). The flowering phenology was observed every 2–3 d from the beginning of April until the end of the flowering season, late May 1993. During each observation, the sexual phase (immature, female, bisexual, male, and post flowering) of each labeled spadix was recorded. For the plants with two spadices, we defined the female phase of the individual as the period with only female-phase spadices, the male phase as a period with only male-phase spadices, and the bisexual phase as any combination involving at least pre-male phase spadices. The daily sex ratios of the spadices within the population were determined from 500 randomly chosen spadices. The sex ratio was defined as [M(t) + B(t)]/[F(t) + 2B(t) + M(t)], where M(t), B(t), and F(t) are the number of spadices as male, bisexual, and female phases at time t, respectively.
Measurement of the heat production of the spadix
We randomly selected 19 plants with inflorescences in the population and measured the temperature of the spadices. The measurement was conducted at 1-h intervals throughout the flowering season by using automatic recording thermometers (KADEC-U, Kona System Co., Ltd., Sapporo, Japan) with thermistor sensors placed on the distal surface of spadices, where the heat production is most active (Uemura et al., 1993
). We also measured the air temperature (40 cm above ground) in the same way. For an index of daily heat production per spadix, we used the cumulative difference of hourly temperature between spadix and air (°C), which was given by 
(STi-ATi), where STi and ATi were the temperatures of the spadix and air at the hour i, respectively. In this calculation, only nighttime data obtained from 1800 to 0600 were used in order to remove the effect of warming within a spathe by directional solar radiation. Then, the value of daily heat production per spadix was given by 2 (STi-ATi). In these 19 plants, the correlation between the basal diameter and the maximum value of the cumulative daily heat production per spadix was examined to investigate the effect of plant size on heat production.
Measurement of paternal and maternal RS
We covered each labeled spadix with a wire cage of 1 x 1 cm mesh size after flowering to avoid fruit predation by small rodents or foxes until the maturation of seeds. After seed maturation, we measured the basal diameter of each labeled individual, collected all fruit, and counted the number of seeds per fruit. The maternal RS of a spadix is directly expressed as the number of seeds. Following Devlin and Stephenson (1987)
, we estimated the daily paternal and maternal RS both from the number of fertilized ovules at a given time that finally matured into seeds and from the number of staminate (male and bisexual) and pistillate (female and bisexual) phase spadices at that time within the population. First, we assumed that the 112 sampled S. renifolius individuals reflected the dynamics of the breeding population. In this study, we defined the number of seeds produced on a plant as the maternal RS of that plant and the number of seeds sired as paternal RS, disregarding seed size or quality. Next, we calculated the total number of seeds set in the population as a function of time in the flowering period. We calculated the seed set of a spadix on each day during the female and bisexual phases as n/(dF + dB), where n is the number of seeds produced by a spadix and dF and dB are the duration of female and bisexual phases, respectively. At the population level, the expected total number of fertilized ovules that mature into seeds at time t, N(t), can be presented by the sum of seed set per spadix, n/(dF + dB), for all female- and bisexual-phased spadices at time t. Therefore, we calculated the mean daily RS of a spadix as N(t)/[F(t) + B(t)] in terms of female function and as N(t)/[M(t) + B(t)] in terms of male function. We derived the estimated number of seeds sired by a given spadix, or the paternal RS of the spadix, over the reproductive season as
We analyzed the correlations between flowering phenology (e.g., onset of flowering and duration of female and male phases) and plant size or the number of seeds produced by using Pearson's r (n = 112 individuals). Regression lines and correlation coefficients (r) between cumulative heat production and plant size or duration of female phase and between plant size and the number of seeds produced or the estimated number of seeds sired were calculated by the least-square regression method.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The number of seeds produced was significantly positively correlated with the duration of female and bisexual phases (Table 1). This indicates that their flowering phenology influenced maternal RS.
Heat production was high during the female and bisexual phases, in which the temperature of the spadices was sometimes 10°C or more above the air temperature. As demonstrated in a previous study by Uemura et al. (1993)
, thermogenesis was abruptly diminished at the male phase and disappeared after the flowering season. Values of cumulative daily heat production ranged from 27.2° to 242.1°C and were significantly correlated with the basal diameter (r = 0.633, P = 0.003; Fig. 3A). A negative correlation was detected between the maximum value of cumulative heat production and the duration of the female phase (r = -0.632, P = 0.004; Fig. 3B). These results indicate that larger plants can provide warmer spathes than smaller plants during the female and bisexual phases and that heat production is correlated with the rapid gender change of each spadix after a short period of pistillate phase.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; de Jong and Klinkhamer, 1989
; Nakamura, Stanton, and Mazer, 1989
; Kudo, 1993
). It has been assumed that because reproduction through female function requires more energy than that through male function, small-sized plants often function primarily as males, i.e., pollen donors (Bierzychudek, 1982
; Willson and Burley, 1983
; Schlessman, 1988
). In S. renifolius, however, larger plants indicated greater ability to produce heat, rapid gender change from female to male (shorter female phase), and a longer period of pollen presentation than those of smaller plants. As a result, larger plants functioned more as males than as females.
Seed production in the observed population was highly restricted not by resource but by pollinator limitation, because there was no significant correlation between plant size and seed number produced per plant (Fig. 5A). Under such conditions, competition for pollinator acquisition among individuals is important to promote both paternal and maternal RS (Thomson and Brunet, 1990
; Dafni, 1992
; Stanton, 1994
). Therefore, both the paternal and the maternal RS of each plant strongly depend on their attractiveness to pollinators and on the flowering schedules within a population (Stanton, 1994
). Early flowering may enhance male RS by preempting the receptive stigmas, as mentioned before. Moreover, longer pollen presentation seems to increase male RS under pollinator limitation. Then, is there a trade-off between maternal and paternal RS in this species? Although larger plants tended to have a shorter pistillate phase than smaller plants, the number of seeds produced per spadix was statistically independent of plant size, as shown in Fig. 5A. If the heat production of spadices during the female phase is related to pollinator attraction (Uemura et al., 1993
), higher heat production by large plants may compensate for the short pistillate phase under female-biased sex ratios during the early flowering season. Thus, large plants can increase their paternal RS without a decrease in maternal RS through early flowering and rapid sex change.
Some problems still remain in our estimation of paternal RS. We estimated RS from the seed set of each plant divided by the duration of the pistillate phase and the total seed set within the population on each day divided by the number of pistillate and staminate spadices. Because the seed production in this population is recognized to be strongly limited by infrequent pollinator visitation (Uemura et al., 1993
), RS in nature may greatly vary among spadices and/or individuals. Thus, we may have underestimated the variation of RS through male function. Besides, we did not confirm the relationship between the size of spadix and spathe and the number of pollinator visits, because pollinator visitation was rare throughout our observation period. A high value of daily paternal RS at the beginning of the flowering season would be expected to result in larger, warmer, and early-flowering individuals with high attractiveness for pollinators. Moreover, our results demonstrated that paternal RS linearly increased with size, while maternal RS did not (Fig. 5). This suggests that a substantial sexual separation in terms of plant size occurred in the breeding system and strongly supports the existence of size advantage in the male function (Devlin, 1989
; Broyles and Wyatt, 1990
) but not in the female function in this species.
The size-dependent flowering phenology in S. renifolius may provide a unique breeding system with irreversible pollen flow from larger plants to smaller plants at low pollinator activity levels. If plant size is correlated with the frequency of pollinator visits, it will result in great variation of paternal and maternal RS among plants, where a small portion of individuals in the population attracts pollinators and achieves greater success (Stanton, 1994
). Although protogynous flowering in this species is a mechanism to reduce pollen–stigma interference (i.e., ovule clogging by self-pollen because of self-incompatibility), such dichogamous flowering creates a large variation of functional sex ratio within a population through the flowering season. Under such a predictable transition of sex ratio, the size-dependent flowering behavior observed in this study (regulation of onset and gender-shift timing within flowers) is considered as a reproductive strategy to reduce male-male competition among plants. In this strategy, heat production might play an important role in enabling S. renifolius not only to attract pollinators but also to flower earlier and to change gender rapidly by promoting temperature-dependent physiological activities for flower development in a cool environment. However, size advantage in the female function would be expected to increase when pollinators are more abundant; larger plants have more flowers (ovules) and resources than smaller ones. Therefore, a long-term study is necessary to estimate the lifetime reproductive success of S. renifolius in consideration of yearly variations among pollinator abundance and RS both in the male and the female function in the population.
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FOOTNOTES |
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4 Author for reprint requests, current address: Department of Biosphere Science, Faculty of Science, Toyama University, Toyama 930-8555, Japan.
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LITERATURE CITED |
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, 1.0 = 
)
0.05) ; *, P < 0.05; **, P < 0.01 (Student's t test)
