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Flowering phenology, display size, and fruit set in an understory dioecious shrub, Aucuba japonica (Cornaceae)¹

Forest Environment Division, Forestry and Forest Products Research Institute, Ibaraki 305-8687, Japan

Received for publication August 19, 1999. Accepted for publication May 11, 2000.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
I investigated the effects of display size and flowering phenology on fruit set in Aucuba japonica, an understory dioecious shrub pollinated by opportunistic insects. Natural variations in display size, flowering phenology, and fruit set were monitored in 1997. A hand-pollination experiment was also conducted to check whether pollen limitation was a factor in fruit set in the field. Increases in floral display size did not affect fruit set; the proportion of flowers that set fruit was almost constant irrespective of the total number of flowers per inflorescence, the total number of inflorescences per plant, and the total number of flowers per plant. The hand-pollination experiment showed that fruit set was not pollen limited despite the low mating probability that resulted from the combination of dioecism and the species' dependence on opportunistic pollinators. This was due, in part, to the fact that female flowers did not have a predetermined period of receptivity, but instead remained receptive until they received pollen. In contrast, flowering phenology did affect fruit set. Fruit set was most abundant when male and female flowering was most abundant. This suggests there was some degree of pollen limitation during the part of the flowering season when male flowers were scarce.

Key Words: Aucuba japonica • Cornaceae • dioecy • flowering phenology • fruit set • resource limitation

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Some plant mating systems are associated with particular life-history characters or habitats (Bawa, 1980 ; Sutherland and Delph, 1984 ; Arroyo and Squeo, 1990 ; Barrett, Harder, and Worley, 1997 ; Sakai and Weller, 1999 ). Dioecious shrubs that live in the forest understory show such patterns (Thomson and Brunet, 1990 ). Most, for example, have small, inconspicuous, and numerous flowers (Bawa, 1980 ; Fox, 1985 ; Muenchow, 1987 ; Sakai and Weller, 1999 ) and are pollinated by unspecialized pollinators such as small bees, flies, and other diptera (Opler, Baker, and Frankie, 1980 ; Muenchow, 1987 ). In general, these insects do not specialize on a given plant species as strongly as do bumble bees or honey bees, for example, nor do they carry pollen as effectively (Thomson, Maddison, and Plowright, 1982 ; Dukas, 1987 ; Herrera, 1989 ). How does an understory dioecious shrub achieve reproductive success despite reliance on such opportunistic and inefficient pollinators?

In order for dioecy to evolve, at least one fitness gain function must have an accelerating shape (Charnov, 1979 ). The small, numerous flowers associated with dioecy have been explained as a reflection of this approach, wherein increased floral display greatly increases attractiveness to pollinators (Bawa and Opler, 1975 ; Bawa, 1980 ). But this display hypothesis appears to conflict with the strategies adopted by understory dioecious shrubs to some extent. First, because opportunistic pollinators do not discriminate among display sizes as well as specialist insects do (Thomson, Maddison, and Plowright, 1982 ; Vaughton and Ramsey, 1998 ), display should not have a strong effect on the fitness gain function. Second, dioecious plants almost always have some sexual differences in the number or size of flowers, with male plants being more conspicuous (Lloyd and Webb, 1977 ; Carr, 1991 ; Cipollini and Whigham, 1994 ; Vaughton and Ramsey, 1998 ); this would leave the less conspicuous females with less visitation (Charlesworth, 1993 ). Such male bias in visitation has been reported for several dioecious species (Bawa, 1977 ; Kay et al., 1984 ; Ågren, Elmqvist, and Tunlid, 1986 ; Bierzychudek, 1987 ; Elmqvist, Ågren, and Tunlid, 1988 ; Thomson, 1988 ; Eckhart, 1991 ; Shykoff and Bucheli, 1995 ).

On the other hand, some studies have shown that display size did not increase the visitation rate per flower (Muenchow and Delesalle, 1994 ). In a theoretical model by Harder and Thomson (1989) , from the view of pollen presentation, the optimal number of flowers was determined by pollen removal per visit. They found that pollen packaging would evolve if insect visitations were frequent enough, and decreasing pollen loss from each flower would increase the adaptive value of producing a large number of flowers, even if visitation rates did not increase strongly with increasing display size.

In addition, flowering phenology is an important fitness factor (de Jong and Klinkhamer, 1991 ; Ashman and Schoen, 1996 ; Sabat and Ackerman, 1996 ). Especially in dioecious plants, mating is impossible unless pollinators move from a male plant with dehiscent anthers to a female plant with receptive stigmata. Not every plant-to-plant movement will be from male to female, so the probability that an inter-plant movement results in pollination is lower for a dioecious species than for a hermaphrodite one. Pollinator movement is also restricted by microclimatic conditions such as the irradiance regime in the forest understory (Herrera, 1995, 1997 ). There are few empirical data that focus on the apparent conflict between dioecism and reproduction by means of opportunistic pollinators.

The goal of this study was to understand the female strategy for successful reproduction using opportunistic pollinators in a forest understory. I addressed the following questions: (1) Does the size of the female inflorescence or the number of inflorescences per female affect fruit set? (2) Does fruit set depend on flowering phenology? (3) Is fruit set pollen limited?

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Natural history of species
Aucuba japonica (Cornaceae) is an evergreen dioecious shrub common in the understory of temperate old-growth forest and cedar plantations in Japan. The shrub is usually less than 2.5 m tall. The plants bloom in April, with inflorescences occurring at the ends of the shoots. Male inflorescences have 10–300 flowers and are 5–15 cm long, whereas female inflorescences have up to 30 flowers and are 2–5 cm long. Each flower has four dark-purple petals, and individual flowers are 8–10 mm in diameter in both sexes. The flowers are visited by a variety of insects, including small bees, flies, and beetles. Fruit matures over the winter and is ripe by the following spring. A female flower has one ovule and produces a one-seeded fruit.

Study site
The study was conducted in a cedar plantation on Mt. Tsukuba, in Ibaraki Prefecture, Japan (lat 36°10' N, long 140°10' W, 280 m elevation). The mean annual temperature is 14.8°C, and the mean annual precipitation is 1020 mm. The canopy height of the forest reaches 20 m, and the height of the shrub layer was 3 m. The study population was chosen from a wood lot of the Forestry and Forest Products Research Institute's experimental forest. Aucuba japonica dominated the shrub layer. Zanthoxylum piperitum (Rutaceae) and Helwingia japonica (Cornaceae) were less common components of the shrub layer and flowered at the same time as the study species.

Flower and fruit production
The total number of flowers per inflorescence (which includes buds and withered flowers in this study) was sampled on 117 male plants (973 inflorescences) and 71 female plants (516 inflorescences). The number of fruits was recorded in early December. At this time, aborted fruits could easily be distinguished from mature fruits, but fruit dispersal by birds, which occurs from late December through March, had not yet begun.

Flowering phenology
Male flowering phenology was measured in terms of the number of flower buds, open flowers, and withered flowers on three dates from 7 April to 30 April 1997 (1060 inflorescences, 160 individuals). Withered flowers were counted by determining the number of peduncles that remained after a flower abscised. For male flowers, the dates of the start and peak of flower production were estimated for each inflorescence by means of linear regression. The start date was defined as the day when the number of flower buds started to decrease (i.e., when the first buds began to expand into flowers). The finish date was defined as the day on which the number of withered flowers equaled the total number of flowers in the inflorescence, and the middle date was defined as the halfway point between the start and finish date. Only inflorescences that exhibited decreases in the number of buds and increases in the number of withered flowers on at least two of the three observation dates were used in the analysis.

Because decreasing number of buds and increasing number of withered flowers in the female inflorescences was rarely observed in the sample described above, regression analysis was not used to evaluate female phenology. Instead, phenology was inferred from direct, detailed observations made every 3 d of 40 inflorescences (five inflorescences on each of eight female plants). An additional 55 male inflorescences (five inflorescences on each of 11 male plants) were also observed on the same 3 d to allow a direct comparison between the sexes of the duration of an inflorescence and the proportion of flowers on an inflorescence that were open on the middle day of the flowering period.

The flowering season was arbitrarily divided into five periods (period 1: 1 Apr–6 Apr, period 2: 7 Apr–12 Apr, period 3: 13 Apr–18 Apr, period 4: 19 Apr–24 Apr, period 5: 25 Apr–30 Apr). Each inflorescence in the study was scored from 1 to 5 based on the periods in which its start and middle days occurred. That approach allowed a comparison of the average phenology of the male and female inflorescences.

To study the longevity of the female flowers, 15 female inflorescences (five on each of three individuals) were covered with a paper bag before anthesis to prevent pollen deposition. The phenology of these bagged inflorescences was observed every 3 d.

Pollen limitation study
To determine whether fruit set was pollen limited, all flowers on all inflorescences of ten female plants were pollinated by hand in April 1998, and their fruit set was compared with that of naturally pollinated plants. One to three inflorescences on each of another ten female plants were pollinated by hand and their fruit set was compared with that of another one to three naturally pollinated inflorescences on the same plant. The number of fruits was recorded in November.

Fruit drop study
Fruits of A. japonica develop and mature from the end of flowering in April and early May until December. During this process, many immature fruits drop, especially from July to September. In June 1998, to evaluate whether this fruit drop is a means to adjust fruit set to resource availability or selective abortion, I randomly thinned 36 inflorescences on ten individuals to between 20 and 50% of their original fruit set. In November, fruit set on these thinned inflorescences was then compared with fruit set on unmanipulated inflorescences within the same plant.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Unless otherwise indicated, all ranges presented in this section represent mean ± 1 standard deviation (SD).

Display size
The mean number of flowers in a male inflorescence was 51.8 ± 26.8, vs. 8.2 ± 5.0 in a female inflorescence. This sixfold difference was statistically significant (t test, P < 0.001). Male plants also had more inflorescences per plant than did females. Males averaged 7.9 ± 9.4 inflorescences per plant vs. 6.4 ± 6.6 for females. A Mann-Whitney U test showed this difference to be significant (P < 0.001).

Male flowering phenology
The detailed monitoring of 55 male inflorescences showed that blooming lasted an average of 18.4 ± 3.0 d in male inflorescences, and on the middle day of an average inflorescence 48.8 ± 10.0% of the flowers were open (Table 1). The pattern of anthesis and withering in male inflorescences fit a linear regression model well (Fig. 1), so it was possible to reliably estimate the middle day of the flowering period for the larger sample of male inflorescences. For this larger sample, the majority of the male inflorescences started blooming in period 2 and reached their middle day of blooming in period 4 (Fig. 2). The mean total number of buds, open flowers, and withered flowers per inflorescence differed significantly among start periods (one-way ANOVA, F = 4.89, P < 0.05): between periods 1 and 2 (Tukey's HSD test, P < 0.01) and 1 and 3 (P < 0.05). There were also significant differences among the periods in which the middle day was reached (F = 19.40, P < 0.001): between period 2 and 5 (P < 0.05), 3 and 5 (P < 0.05), 2 and 3 (P < 0.01), and between other all pairs (P < 0.001). The large number of flowers per inflorescence in period 4 consisted mostly of inflorescences that were reaching the middle days of their lifespan (Fig. 3).

View larger version (19K): [in this window] [in a new window]   Fig. 1. An example of the pattern of flowering phenology for proportion of (a) flower buds and (b) withered flowers to total number of buds, open flowers, and withered flowers per inflorescence. Each line represents one inflorescence. Decreases in the number of flower buds and increases in the number of withered flowers were approximately linear

View larger version (32K): [in this window] [in a new window]   Fig. 2. Frequency distribution of flowering phenology at (a) the day when flowering started and (b) the middle day of flowering period. In (a), males started flowering earlier than females (P < 0.001). In (b), the timing of the most abundant inflorescences for both males and females occurred in period 4.

View larger version (52K): [in this window] [in a new window]   Fig. 3. The relationship between flowering phenology and the number of flowers per inflorescence for (a) females and (b) males

Fruit set
In 1997, fruit set occurred for an average of 60.8 ± 29.3% (N = 71) of the female flowers on a plant. In 1998, an average of 37.0 ± 35.4% of the flowers set fruit (N = 93). In 1997, no relationship was found between the proportion of flowers that set fruit and the total number of flowers per inflorescence, the total number of inflorescences per plant, and the total number of flowers per plant (Fig. 4).

View larger version (21K): [in this window] [in a new window]   Fig. 4. The relationship between fruit set and female floral display sizes. Fruit set did not vary with (a) the number of flowers per inflorescence, (b) the number of inflorescences per individual, or (c) the total number of flowers per individual. The slope of each linear regression did not differ significantly from 0 at (a) P = 0.999, (b) P = 0.995 and (c) P = 0.995

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The results of the test of random hand-thinning suggested the possibility that developing fruits are selectively aborted. If there is a display effect, small inflorescences would receive less pollen than large ones, and the probability of genetically suitable pollination would be lower in small inflorescences than in large ones, even if the amount of pollen deposited equals the number of ovules. However, the fruit set of small inflorescences was the same as that of large ones. Since the factor that restricted fruit set was not limitations on the availability of pollen, fruit set does not appear to correlate with the attractiveness of each display to pollinators. Even small inflorescences of A. japonica receive adequate numbers of pollinator visits, and inflorescence size has no effect on fruit set. This differs from the results reported for some hermaphroditic herbs (Campbell, 1989 ; Andersson, 1996 ). Because trees or shrubs are much larger than herbs, the floral display in hermaphrodite trees or shrubs may not correlate positively with female fitness because the plant is able to reproduce by geitonogamy (Kato and Hiura, 1999 ).

If an investment in one sexual function enhances the fitness in an accelerating manner, selection may favor the evolution of separate sexes (Charnov, 1979 ). In dioecious plants, the female's reproductive costs per flower are greater than the costs of male flowers because fruit production is more expensive than pollen production (Lloyd and Webb, 1977 ; Allen and Antos, 1988 ; Cipollini and Whigham, 1994 ); for this reason, females usually produce fewer flowers than males, as is the case for A. japonica (Lloyd and Webb, 1977 ; Bell, 1985 ; but see also Delph, Galloway, and Stanton, 1996 ; Eckhart, 1999 ). Under these circumstances, insects that can distinguish the number of flowers per inflorescence such as bumble bees are undesirable pollinators for the plant because they may show male-biased visitation.

Male-biased visitation is likely to lead to pollen loss (i.e., because the pollinators preferentially visit male inflorescences and thus may not visit the smaller female inflorescences) and reduces mating probability. Therefore dioecious plants tend to be pollinated by opportunistic pollinators (Thomson and Brunet, 1990 ; Charlesworth, 1993 ). However, as discussed in the introduction, some studies have shown that visitation rates differed between males and females in dioecious and gynodioecious plants. Vaughton and Ramsey (1998) reported that the extent of differential visitation to male and female flowers depended on the insect species. In the case of A. japonica, however, fruit set was not limited by pollen, so female fitness was not decreased by a low level of pollinator visitation. Furthermore, female flowers appeared to extend floral longevity until pollen deposition occurred. In females of this species, increased floral longevity and the small number of flowers might combine to eliminate or greatly reduce the effect of pollen limitations. Females of A. japonica appear to adopt a strategy that alleviates the reproductive disadvantages of their growth habit (as understory dioecious shrubs) such as male-biased visitation, low mating probability, and dependence on unspecialized pollinators.

In this study, the average fruit set was highest for inflorescences that reached their flowering peak in period 4, when the largest number of male inflorescences were also flowering and pollen was most available. In dioecious species, the timing of flowering generally differs between males and females, with males beginning to flower earlier than females (Lloyd and Webb, 1977 ; Willson, 1979 ; Beach, 1981 ). The significance of this pattern seems to relate to the smaller number of flowers per female inflorescence. The flower lifespan in a male inflorescence was longer than that in a female inflorescence, probably because the probability of pollination is uncertain and extending male floral longevity reduces the risk of pollination failure (Rathcke and Lacey, 1985 ).

This is especially true for species with obligate outcrossing, which tend to flower longer than species capable of self-pollination (Pojar, 1974 ; Primack, 1985 ). In order to enhance reproductive fitness, males presumably need to flower longer than females because males cannot predict the timing of the peak of female flowering. The effect of flowering phenology on male reproductive success was seldom studied until recently. Konuma and Yahara (1997) showed that total male fitness increased with increasingly early first-flowering dates in an andromonoecious perennial herb, Heracleum lanatum var. nipponicum. These authors believed that earlier flowering enhanced male fitness because of the existence of male-male competition. Female fitness also varied with flowering phenology. In some goldenrod (Solidago spp.) species, clones that flowered at different times differed in their seed set, and the restriction factor for seed set changed along with changes in the phenology of flowering (Gross and Werner, 1983 ). In this study, differences in fruit set among the five periods defined for flowering phenology were also difficult to explain completely by resource limitation. At the start and finish dates for flowering phenology, pollen limitation could occur because of the low density of flowers and low levels of activity by pollinators. However, the main factor that restricted fruit set in the study population was resources, because flowers at the start and finish of the period of flower phenology were in the minority.

The fact that the larger female inflorescences started to flower earlier implies that it can be difficult to saturate all female flowers with pollen in larger inflorescences (Rathcke and Lacey, 1985 ; Zimmerman, 1990 ). If the rate of arrival of pollen (via pollinators) is constant (i.e., if display size is not a factor in attracting pollinators), then it will take longer for all ovules in larger female inflorescences to be fertilized. In many dioecious species, the longevity of a female flower is greater than that of a male flower because females must wait for pollen to arrive, whereas males have completed their function as soon as pollen is shed (Primack, 1985 ).

Unlike male flowers (which open, dehisce pollen, wither and fall on a schedule that is probably unaffected by pollinators), the phenology of female flowers proved to depend to some extent on the activities of pollinators. The female flowers in bagged inflorescences stayed fresh and receptive much longer than female flowers on the same plant that experienced normal insect visitation. This result showed that female flower lifespan increased in the absence of pollen; thus, female flowers seemed to receive pollen relatively early after anthesis in the study population. If so, it would be important for males to synchronize their peak of flowering with an unpredictable female peak of flowering; in fact, this is what occurred. A dioecious species generally has a lower mating chance than both selfish and self-incompatible hermaphroditic species (Tainaka and Itoh, 1996 ). Nevertheless, dioecious species attain higher fruit set than hermaphroditic species (Sutherland and Delph, 1984 ; Sutherland, 1986 ). This evidence supports the observation that surplus flowers fulfill male function in hermaphrodite plants. In this study the duration of flowering in male inflorescences was longer than that of female inflorescences. Longer flowering duration in a male inflorescence improves pollination success with opportunistic pollinators and with chance loss of function by wind and rain.

	FOOTNOTES

 
¹ The author thanks K. Kamo for comments on the study plan; N. Tanaka and N. Yamashita for field assistance; and D. Charlesworth, M. Johnston, and G. Muenchow for comments on an earlier version of the manuscript.

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