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Reproductive Biology |
Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810, Japan
Received for publication March 7, 2003. Accepted for publication July 24, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: attraction • bumble bee behavior • floral color change • geitonogamous pollination • successive flower visits
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Waser, 1983
; Weiss, 1995
, 1997
; Weiss and Lamont, 1997
). Pollination success of animal-pollinated plants is influenced by the visitation frequency of pollinators (access to the plants) and their foraging behavior on the plants after arriving (Fægri and Var Der Pijl, 1976
). In several studies, the retention of post-color-change flowers enhanced the attractiveness of individual plants to increase the approach frequency of pollinators to the plants, i.e., long-distance attraction (Gori, 1983
, 1989
; Cruzan et al., 1988
; Weiss, 1991
; Niesenbaum et al., 1999
; Oberrath and Böhning-Gaese, 1999
; but see also Casper and La Pine, 1984
; Delph and Lively, 1989
). As for the after-arrival effects, some studies reported that color-changed flowers worked as a cue to discourage pollinators from visiting older flowers with little reproductive value, i.e., they worked as short-distance determinants (Casper and La Pine, 1984
; Gori, 1989
; Weiss, 1991
; Niesenbaum et al., 1999
; Oberrath and Böhning-Gaese, 1999
). In this situation, however, the effect on total pollination efficiency of the whole plant has not been demonstrated precisely. The relative importance of long-distance attraction vs. short-distance determinant cue should depend on the potential floral structure of individual plants. For example, plants having a large display size, like many woody plants, may not need to attract pollinators by keeping nonreproductive flowers, but may benefit from preventing long stays by pollinators, thus increasing the outcrossing efficiency.
Floral display size, i.e., the number of opening flowers per plant, is one of the most accurate indexes of their attractiveness, and plants with larger floral display can often induce more visits by pollinators (Cruzan et al., 1988
; Klinkhamer et al., 1989
; Klinkhamer and De Jong, 1990
). Generally, the higher the frequency of pollinator visits to individual plants, the greater the possibility for pollen transfer from other plants. However, successive flower visits by pollinators within plants may cause frequent pollen transport between flowers of the same plants, i.e., geitonogamous pollination (De Jong et al., 1992
; Harder and Barrett, 1996
; Harder and Wilson, 1998
). Geitonogamous pollination would be costly for self-incompatible plants by restricting the deposition of outcrossing pollen and by decreasing opportunities for pollen dispersal to other plants, i.e., pollen discounting (Holsinger et al., 1984
). Even in self-compatible species, acceleration of geitonogamous self-pollination may be harmful due to inbreeding depression. There are many studies indicating that plants with large floral displays often attract more pollinators than ones with small displays (Cruzan et al., 1988
; Klinkhamer et al., 1989
; Klinkhamer and De Jong, 1990
; Weiss, 1991
; Harder and Barrett, 1995
; Niesenbaum et al., 1999
; Oberrath and Böhning-Gaese, 1999
), but the increase in display size sometimes results in the acceleration of geitonogamous pollination from the increasing number of successive flower visits on the donor plant (De Jong et al., 1992
; Barrett et al., 1994
; Harder and Barrett, 1995
, 1996
).
To account for the significance of floral color change precisely, we should focus not only on the long-distance attractiveness of pollinators but also on the behavior of pollinators after arriving at the plants from the viewpoint of geitonogamous pollination. As shown in previous studies, floral-color change usually accompanies decreasing pollen and nectar reward and loss of both male and female reproductive abilities (Gori, 1983
, 1989
; Casper and La Pine, 1984
; Oberrath and Böhning-Gaese, 1999
). Also, some studies reported that the timing of floral color change depended on the timing of fertilization (Gori, 1983
; Ne'eman and Nesher, 1995
). However, it has not been clear how and to what extent the interactions between color-changed flowers and behavior of pollinators influence the mating success (outcrossing or selfing) of individual flowers.
The behavior of pollinators can influence the pollination efficiency through (1) extent of pollen removal from anthers and pollen deposition on stigmas during a single flower visit and (2) the number of successive flower visits during a single stay on a plant (De Jong et al., 1992
; Harder and Barrett, 1996
). Our goal in this study is to clarify the ecological significance of floral color change of woody plants having a large display size, especially from the viewpoint of the short-distance determinant within plants after the arrival of pollinators. We used a bumble-bee-pollinated shrub, Weigela middendorffiana (Carriere) K. Koch (Caprifoliaceae) whose flowers change color from yellow to red as the target species. The research objectives in this study were as follows: (1) clarification of the mating system in this species and comparisons of reward presentation and reproductive ability between pre- and post-color-change flowers, (2) clarification of the pattern of floral color change within plants and the factors affecting color change (including temperature and pollination status), (3) effects of floral color change on long-distance attraction of pollinators, and (4) effects of floral color change on pollinator behavior, i.e., successive flower visits during a stay on an individual plant.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Weigela middendorffiana inhabits montane to alpine regions in northeastern Asia. Plants usually attain 1–2 m in height, and the canopy size is nearly 1–2 m in diameter. Although clonal growth is rare, this species usually grows gregariously, and several individuals sometimes form a patch with a large canopy (approximately 5–10 m in diameter). Flowering begins in the middle in June and continues toward the end of July on Hokkaido, reflecting the variation of snowmelt times. Individual plants often have more than 20 inflorescences, and each inflorescence usually consists of 2–6 flowers, which develop simultaneously. Flowers are hermaphroditic and have a bell-shaped yellow corolla, approximately 3 cm long. Individual flowers have one pistil and five stamens. During anthesis, the inside part of the lower corolla changes color from yellow to red (Fig. 1). Flowers are predominantly visited by nectar-feeding bumble bees. The mating system and pattern of floral color change within a whole plant are unknown in this species.
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To investigate the extent of pollen limitation, self-compatibility, and interference between male and female functions, we compared the seed set (seed/ovule ratio) of manipulated flowers (hand cross-pollinated, bagged, bagged + self-pollinated, and emasculated + naturally pollinated) with the seed set of control flowers on 20 individually manipulated plants. Mean value of the seed set in each inflorescence was used for statistical analysis, i.e., sample size = 20. For comparisons among treatments, the Kruskal-Wallis test was used, and multiple comparisons between a control and each of the other treatments were conducted by the Steel's test.
The duration of each color phase
The effects of pollination events on the timing of color change and flower longevity were investigated using the manipulated plants at Site S in 2001. We measured the durations of yellow phase (from the opening to the day of color change) and red phase (from the color change to the withering of flowers) of all flowers on manipulated inflorescences at 1-d intervals. Flowering durations of individual inflorescences were compared among treatments (control, hand cross-pollinated, bagged, and emasculated + naturally pollinated) and between color phases (yellow and red) by two-way repeated-measures ANOVA.
To investigate the effects of flowering sequence within individual plants and the temperature during anthesis on the durations of yellow and red phases and total longevity of flowers, we measured the durations of yellow and red phases for 341 flowers of 109 inflorescences on 10 individual plants under natural conditions at Site S in 2001. We analyzed the duration of each color phase and total longevity by fitting a mixed effects model because this experimental design was formed by three sampling units—individual plant, inflorescences within a plant, and flowers within an inflorescence. Variation in the durations of yellow and red phases under natural conditions was analyzed to fit a linear mixed effects model, in which the duration of each color phase and total longevity of individual flowers were treated as a criterion variable. The cumulative flowering rate of each plant (i.e., the proportion of already opened flowers to total flower production during the season) and the average temperature during anthesis were treated as explanatory variables for data of longevity of flowers under natural conditions, using the nonlinear mixed effects model (NLME) statistical package (Pinheiro and Bate, 2000
). The cumulative flowering rate was represented as the progress of anthesis on a whole plant on the day the flower changed color. The average temperature during the anthesis of individual flowers was calculated using the daily mean temperature from the day of opening to the day of withering. Ambient temperature at Site S was estimated from a meteorological record in Sapporo using a lapse rate of temperature between the locations (–0.24°C/100 m elevation; T. Y. Ida and G. Kudo, unpublished data).
Reward presentation
Workers of Bombus hypocrita sapporensis Cockerell commonly visit W. middendorffiana flowers for nectar feeding but also occasionally for pollen collection (T. Y. Ida and G. Kudo, personal observation). To compare the amount of reward offered by yellow- and red-phase flowers, we quantified the nectar volume and the number of pollen grains for each color-phase flower; 20 flowers of each phase type from 10 plants for nectar volume and 20 flowers of each phase type from 10 plants for pollen grains on the first day of anthesis on yellow-phase flowers or soon after the color change on red-phase flowers. Nectar and pollen were collected between 1000 and 1300 at Site H in 2001. We inserted microcapillary tubes (Microcaps, Drummond Scientific, Broomall, Pennsylvania, USA) into the bottom of the corollas to remove all of the available nectar. We removed all five anthers from each flower using forceps stored them in a vial filled with 70% ethanol, and used a particle counter (Z2 Type counter, Beckman Coulter, Fullerton, California, USA) to count the number of pollen grains present. Mean nectar volume and the number of pollen grains were compared between the phases by the Mann-Whitney U test.
Residual reproductive ability
To compare the male and female residual reproductive abilities between the yellow- and red-phase flowers, we measured the pollen germination rate and the number of seeds produced by the artificial outcrossing for each phase of flowers at Site S in 2002. We collected pollen from anthers on each yellow-phase flower from 11 plants and each red-phase flower from 17 plants on the first day of anthesis and on the day of floral color change, respectively. Pollen samples were germinated in the laboratory at 20°C (optimum germination temperature among 10°, 15°, 20°, and 25°C in a preliminary experiment) on culture plates filled with 1% agar and 10% sucrose for 12 h. After that, we counted the number of pollen grains that had germinated under a microscope (at 40x). Pollen germination of yellow-phase flowers was determined by counting the first 300 pollen grains encountered on a grid across the well under a microscope. When the number of pollen grains remaining on the red-phase flowers was smaller than 300, germination of all pollen grains was checked. A pollen tube that had elongated longer than the diameter of the pollen grain was classified as germination. Pollen germination rates were compared between the phases by the Mann-Whitney U test. The artificial outcrossing treatment was performed on bagged flowers. We compared the potential seed-set ability of yellow-phase flowers on the first day of anthesis (18 flowers from five plants) and of red-phase flowers soon after the color change (10 flowers from five different plants from the yellow-phase census). In each case, we used pollen from yellow-phase flowers as mentioned earlier. The seed set was compared between the yellow- and red-phase flowers by the Mann-Whitney U test, in which mean values of individual plants were used.
Effects of yellow- and red-phase flowers on foraging behavior
To investigate the effects of floral composition of yellow- and red-phase flowers on the attractiveness and foraging behavior of bumble bees at the whole plant level, we observed the frequency of bumble bee visits to individual plants per hour (approach frequency), the number of successive flower visits within a plant per approach, the number of yellow- and red-phase flowers visited per approach, and the foraging trail of bumble bees within plants at Site K in 2002. Observation of the approach frequency was conducted with arbitrarily selected plants having various numbers and proportions of yellow- and red-phase flowers under natural conditions. We observed a total of 251 approaches during 98 observation sets (hours) over 3 d. In addition, density of flowering individuals within 5 m of each focus plant was also measured to assess the effect of neighboring plants on pollinator attraction. Moreover, we recorded the number of successive flower visits and visitation pattern on each of the color-phase flowers after arriving for 152 approaches. We performed a multiple regression analysis to investigate the effects of the number of yellow- and red-phase flowers within plants and the density of neighboring plants on approach frequency and the effects of the number of yellow- and red-phase flowers on the numbers of successive visits to total, yellow-phase, and red-phase flowers per approach.
Preference of bumble bees for yellow- or red-phase flowers was considered by comparing the expected number of visits to yellow- (or red-) phase flowers within plants and the actual number of visits to yellow- (or red-) phase flowers per approach. Assuming random visitation, the expected number of visits to yellow- (or red-) phase flowers per approach was calculated as a product of the number of successive flower visits and the proportion of yellow- (or red-) flowers at that time (the number of yellow- or red-phase flowers/the total number of flowers). The expected and actual numbers of visits to flowers of each phase were compared by the chi-square goodness-of-fit test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sequential pattern of floral color changes within plants was observed under natural pollination for 10 plants at Site S in 2001 (Fig. 3). Total flowering season of individual plants, i.e., from the opening of first flower to the withering of last flowers, ranged from 5 to 13 d. Plants had a duration of only yellow-phase flowers during first 1–2 d, mixed-phase stage during 3–10 d, and only red-phase during 0–5 d. Some plants lacked the duration of only red-phase flowers.
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Effects of yellow- and red-phase flowers on foraging behavior
We observed workers of Bombus hypocrita sapporoensism, B. ignitus Smith, and B. yezoensis Matsumura as flower visitors of W. middendorffiana. Because workers of B. hypocrita sapporoensis were the dominant pollinators for plants at Site K (about 90% of total bumble bee visits), we analyzed the foraging behavior of bumble bees without considering the interspecific variation of foraging behavior among each species. A multiple regression analysis revealed a positive relationship between the number of yellow-phase flowers and the approach frequency per hour (Table 3), while there was no significant relationship between the number of red-phase flowers and the approach frequency. Furthermore, existence of neighboring plants significantly enhanced the approach frequency of bumble bees.
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Bumble bees preferred yellow-phase flowers to red-phase flowers. While 444 visits to yellow-phase flowers were expected from random visits of bumble bees, we observed 567 visits. While 186 visits to red-phase flowers were expected, we observed only 61 visits. This difference was significant (P < 0.05, chi-square goodness-of-fit test).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Gori, 1989
; Oberrath and Böhning-Gaese, 1999
). Because floral color change in W. middendorffiana occurs only inside the corollas, it may be difficult to recognize the color change if pollinators do not access the flowers from the front side. Nevertheless, retention of color-changed flowers did not enhance the long-distance attractiveness significantly. Because W. middendorffiana often forms dense patches, they may have a sufficiently large display size composed of multiple plants to attract pollinators. In such a case, increasing display size of individual plants by the retention of nonfunctional flowers may not contribute to further attraction if pollinators do not strictly discriminate the individual canopy. It may be possible that red-phase flowers are important in attracting pollinators to more isolated plants as suggested by Casper and La Pine (1984)
. However, functions other than long-distance attractiveness seem to be important in this species.
Because W. middendorffiana is self-incompatible, pollen transport between flowers of the same plants (geitonogamous pollination) does not contribute to reproductive success. In this sense, the optimal pollination efficiency should be represented by the pollen transport maximizing the proportion of pollen exported to the stigmas of other plants relative to the amount of pollen removed from the donor flower. To enhance outcrossing efficiency, it would be necessary to reduce the number of successive flower visits by single pollinators on the plant and/or to reduce the pollen removal from anthers and deposition on stigmas of the same plant per visit (De Jong et al., 1992
; Harder and Barrett, 1996
; Harder and Wilson, 1998
). Emasculated flowers showed similar seed sets with unmanipulated flowers under natural pollination, indicating that interference between male and female functions within flowers may be small at least from the perspective of seed set, i.e., female success.
Oberrath and Böhning-Gaese (1999)
implied that the retention of color-changed flowers might increase the pollination efficiency because the existence of color-changed flowers enhanced the approach rate on plants but did not influence the successive visits per approach. In this study, the number of yellow-phase flowers positively correlated with the successive flower visits by bumble bees, whereas the number of red-phase flowers correlated negatively. It seems that the retention of color-changed flowers contributes to reducing geitonogamous pollination, i.e., color-changed flowers can control the behavior of bumble bees after arriving. Floral colors would advertise the amount of reward presentation enabling bumble bees to discriminate flowers with little reward before the visit, resulting in the reduced time on rewardless flowers. Flowers of the same inflorescences usually change color simultaneously in this species. Presentation of rewardless, color-changed flowers as a mass may allow bumble bees to recognize that the patch has a low resource level, resulting in their moving quickly through low reward patches (Heinrich, 1979
).
If the plants retained nonfunctional flowers without color change, pollinators might visit a certain number of rewardless flowers before leaving the plant or the patch. This should reduce the pollination efficiency due to pollen transport to the nonfunctional flowers, if the proportion of pollen removal from anthers and deposition on stigmas per visit are sufficiently large. Only a few successive flower visits might be effective for successful pollen export after the bee leaves a donor flower because most of the pollen from a specific donor flower deposited on the pollinator's body is lost during the subsequent few visits to other flowers (Harder and Barrett, 1996
; Rademaker et al., 1997
; Harder and Wilson, 1998
). In W. middendorffiana, approximately 70% of pollen grains were removed from the anthers and as many pollen grains as the number of ovules produced were deposited on a stigma after one bumble bee visit (T. Y. Ida and G. Kudo, unpublished data). This implies that pollen loss by geitonogamous pollination is serious even when bumble bees visit only a few nonfunctional flowers. Floral color change helps to reduce the loss by discouraging pollinators to visit the nonfunctional (color-changed) flowers.
In W. middendorffiana, the timing of floral color change and the duration of each color phase were independent of the timing of pollination events, but did depend on the progress of the flowering season within individual plants. The ambient temperature was negatively related to the durations of each color phase, indicating that the cost of retaining flowers would be larger in a warm environment than in a cool environment (Primack, 1985
; Motten, 1986
; Ashman and Schoen, 1994
). Despite the fact that the cost of retaining flowers was larger late in the flowering season within the plant than early in the flowering season, the duration of yellow-phase flowers late in the season within the plant was longer than that early in the season. In contrast, the duration of red-phase flowers was longer early in the season within the plant than late in the season. Such a variation in the timing of floral color change within plants contributes to maintaining the mixed situation of yellow- and red-phase flowers throughout the flowering season. Such a regulation of floral color change may reflect the importance of the strategy to control pollinator behavior within a plant to increase pollination efficiency in this species (i.e., a short-distance effectiveness of floral color change).
Delph and Lively (1989)
demonstrated that floral color change in Fuchsia excorticata did not contribute to pollinator attraction, while concluding that post-change flowers were retained to allow time for pollen tubes to reach the ovules. Although it is unknown if such physiological constraints exist in W. middendorffiana, variation in the time of color change so as to extend a coexisting duration of yellow- and red-phase flowers through a flowering season seems to contribute to pollination efficiency in this species.
Previous studies on floral color change have often focused on the significance of color-changed flowers in accessing the plant (Gori, 1983
, 1989
; Cruzan et al., 1988
; Weiss, 1991
; Oberrath and Böhning-Gaese, 1999
) and reported that the color-changed nonfunctional flowers would work as a cue to discourage pollinators from visiting them (Casper and La Pine, 1984
; Gori, 1989
; Weiss, 1991
; Niesenbaum et al., 1999
; Oberrath and Böhning-Gaese, 1999
). These results indicate that the retention of color-changed flowers would enhance the reproductive success by reducing the loss of outcross pollen, i.e., through female function. However, most previous studies did not account for the effects of color-changed flowers on reproductive success through male function although some studies implied the importance of male success (Gori, 1983
, 1989
). In this study, we demonstrated that color-changed flowers in W. middendorffiana might enhance pollination efficiency by reducing the number of successive flower visits during a single stay by bumble bees. This means that the retention of color-changed nonfunctional flowers mainly contributes to reproductive success through male function. Our conclusion is based on the observation results in the field in which pattern of plant distribution, size structure, or phenological stage of individual plants inevitably vary in addition to other external factors such as climatic variation. Furthermore, direct information on the relationship between pollinator behavior and pollination success is lacking. These may make the precise evaluation of the significance of floral color change difficult. To overcome these limitations, experimental approaches under controlled conditions are needed.
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FOOTNOTES |
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2 E-mail: gaku{at}ees.hokudai.ac.jp
; fax: ;pl81-11-706-4954
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Barrett S. C. H. L. D. Harder W. W. Cole 1994 Effects of flower number and position on self-fertilization in experimental populations of Eichhornia paniculata (Pontederiaceae). Functional Ecology 8: 526-535[CrossRef][ISI]
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Delph L. F. C. M. Lively 1989 The evolution of floral color change: pollinator attraction versus physiological constraints in Fuchsia excorticata. Evolution 43: 1252-1262[CrossRef][ISI]
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