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Variations in bumble bee preference and pollen limitation among neighboring populations: comparisons between Phyllodoce caerulea and Phyllodoce aleutica (Ericaceae) along snowmelt gradients¹

Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810, Japan

Received for publication November 21, 2002. Accepted for publication April 11, 2003.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Two alpine-snowbed shrubs, Phyllodoce caerulea and P. aleutica (Ericaceae), co-occur in locales in northern Japan with early to late snowmelt, but they have different mating systems. Phyllodoce caerulea is an obligate outcrosser in any population, whereas the selfing ability of P. aleutica is highly variable among neighboring populations along snowmelt gradients: it shows high self-compatibility in early to middle snowmelt populations but low self-compatibility in late snowmelt populations. We investigated the relationships between pollinator availability and mating systems of these species along three snowmelt gradients. Relative abundance of flowers and nectar standing crop of P. caerulea decreased from early to late snowmelt plots. Bumble bees preferred P. caerulea to P. aleutica in early and middle snowmelt plots, while their preference shifted to P. aleutica in late snowmelt plots. Pollen limitation was severe in P. aleutica in early to middle snowmelt plots but it was severe in P. caerulea in late snowmelt plots. Seed-set success under natural conditions of P. aleutica was higher than that of P. caerulea in all plots. Thus, we infer that the selfing ability of P. aleutica under pollinator limitation acts as a reproductive assurance. We conclude that the interaction through pollination between the sympatric species is strong enough to cause a phenotypic change in mating system even within a local area.

Key Words: bumble bee • Ericaceae • mating system variation • nectar volume • Phyllodoce aleutica • Phyllodoce caerulea • pollen limitation • pollinator preference

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Mating system variation within a plant species is often caused by changes in pollinator effectiveness (Barrett and Eckert, 1990 ). Uncertain or insufficient pollinator service is suggested as an important factor in the acceleration of self-pollination in flowering plants (Lloyd, 1979 ; Shoen, 1982 ; Glover and Barrett, 1986 ; Dole, 1992 ; Fausto et al., 2001 ). Interspecific competition for pollinators may enhance the selfing ability of competitively inferior species for reproductive assurance (Levin, 1972 ). Some studies have demonstrated that selfing ability may vary within a species among populations depending on the intensity of pollinator competition with other species (Wyatt, 1986 ; Rathcke and Real, 1993 ; Fishman and Wyatt, 1999 ). It is notable that these studies on mating system variations have been conducted among populations across various geographical scales. In addition, most studies were conducted under the alternative conditions whether a competitor was present or absent. It is not clear if intraspecific variation in mating system can occur also on a local scale or how such a variation reflects the dynamics of competitive situations between the sympatric species.

When a steep environmental gradient exists within a local area, competitive situations may change between co-occurring plant species sharing the same pollinators along the gradient, if they respond differently to the environmental change with modification of performance such as flowering phenology, flower production, and nectar production. In such a case, the mating system of a species that experiences different pollination situations may differ along the gradient. A previous investigation conducted along snowmelt gradients in alpine snowbeds revealed that two sympatric alpine plants, Phyllodoce caerulea and Phyllodoce aleutica (Ericaceae), had considerably different mating systems (Kasagi, 2002 ). Seed set by artificial selfing was low in P. caerulea throughout the snowmelt gradient (ranging 1.0–4.3% in population mean), whereas self-compatibility of P. aleutica was relatively high in early and middle snowmelt populations (ranging 10.8–23.9% in population mean) but was low (0.3–0.7%) in late snowmelt populations within a local area. Seed set by a net-bagging treatment, i.e., autogamous selfing without the aid of pollinators, of both species reflected the patterns of self-compatibility: 0.3–0.6% in P. caerulea throughout the snowmelt gradients and in P. aleutica, 7.2–21.5% in early and middle snowmelt populations but only 0.2–0.9% in late snowmelt populations. Thus, the selfing ability of P. aleutica fluctuated among neighboring populations. We assume that variations in the mating system of P. aleutica might reflect the changes in pollinator effectiveness along the snowmelt gradients caused by an interaction with P. caerulea, because both species are predominantly bumble bee-pollinated and their flowering seasons overlapped highly within a community (Kudo, 1991 ).

To verify this hypothesis, we observed the bumble bee preference between the species along three snowmelt gradients at three snowbed sites and clarified the mechanism controlling the bumble bee preference by measuring the nectar reward. Then, we assessed the effectiveness of pollinators between the species by comparing the extent of pollen limitation along the gradients. Finally, we evaluated the relationship between the patterns of pollen limitation observed along the snowmelt gradients and selfing ability reported by Kasagi (2002) in each species.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Research site
We selected three snowbeds as research sites between 1700 and 1880 m a.s.l. in the central part of the Taisetsu Mountains, Hokkaido, northern Japan (43°33' N, 142°53' E; peak altitude: 2290 m a.s.l.; Fig. 1). Each research site was located near Lake Hisago (HIS), Mt. Goshiki (GOS), and Mt. Pon-kaun (PON) and was 3.5–6 km from the others. We established three plots along the snowmelt gradient (E plot, early snowmelt plot; M plot, middle snowmelt plot; L plot, late snowmelt plot) at every site. Three plots at each site were located by separating 100–700 m from each other. The size of each plot was 20 x 20 m. The normal snowmelt timing at our sites is mid-June at E plots, early July at M plots, and mid-July at L plots.

View larger version (42K): [in this window] [in a new window]   Fig. 1. Three research sites (HIS, GOS, and PON; see Materials and Methods for an explanation of abbreviations) located in the central part of the Taisetsu Mountains, northern Japan. At each snowbed-site, snowmelt usually progresses from higher to lower elevations. Three 20 x 20 m plots (E, M, and L plot) were arranged along a snowmelt order at each site, i.e., early, middle, and late snowmelt

Both Phyllodoce species are common at snowbeds and flowering occurs simultaneously about 2 wk after snowmelt in the Taisetsu Mountains (Kudo, 1991 ). Normal peak flowering seasons are mid-July at E plots, late July to early August at M plots, and mid-August at L plots. Both Phyllodoce species are mainly bumble bee pollinated and monopolize bumble bees from other co-flowering species, such as Sieversia pentapetala, Peucedanum multivittatum, and Veronica stelleri, because Phyllodoce species produce large amount of nectar and are found in dense patches in the Taisetsu Mountains.

Floral composition of two Phyllodoce species
We counted the flower number at peak flowering of both species at each plot at HIS in 1996, 1997, 1999, 2000, and 2001 and at GOS and PON in 1999 and 2000. For the comparisons of floral composition between the species along the snowmelt gradients, we conducted a chi-square test to evaluate heterogeneity in the frequencies of flowers of the two species among the plots (E, M, and L plot) within each site and each year.

Nectar volume and standing crop
We measured the nectar volume per flower of both Phyllodoce species at every plot at HIS in 1997, 1999, and 2001 and at GOS and PON in 1999. The measurement was conducted in the morning on a sunny day during peak flowering season by inserting a capillary tube into each flower of randomly selected 20–40 plants in each species at each plot. An inflorescence in each plant had been covered with nylon-mesh nets for 24 h prior to the nectar measurement to exclude bumble bee visitations. Yearly variation in nectar volume was compared by three-way ANOVA using the data of HIS factored by year (1997, 1999, and 2001), plot (E, M, and L), and species (P. caerulea and P. aleutica). Between-site variation in nectar volume was compared by three-way ANOVA using the 1999 data factored by site (HIS, GOS, and PON), plot (E, M, and L), and species (P. caerulea and P. aleutica). Furthermore, we estimated the nectar standing crop per unit area at every plot in each species by multiplying mean flower number per 1 x 1 m quadrat by mean nectar volume per flower obtained at each plot in 1999.

Bumble bee preference between the species
We observed bumble bee visitation to P. caerulea and P. aleutica flowers at each plot at HIS in 1993, 1997, 1999, 2000, and 2001 and at GOS and PON in 1999 and 2000. We set a 5 x 5 m quadrat within each plot to observe the bumble bee visitation. At peak flowering, we observed the foraging pattern of bumble bees during 2–3 h in the morning on a sunny day at each plot when bumble bees were most active. Additionally, we observed twice (2 d) at the E and L plots at HIS in 1993, and we did not observe the E plot of PON in 2000 because of bad weather conditions. In total, we observed bumble bee visitation 28 times throughout the research period. The observations of bumble bees at HIS in 1997, 1999, and 2001 and at GOS and PON in 1999 were conducted together with the measurement of nectar volume.

We recorded bumble bee visitation on inflorescences of each Phyllodoce species and also simultaneously counted the inflorescence number of each species within a quadrat. Visitation frequency of bumble bees to each species was assessed by a chi-square test against the expectation of proportional visitation based on the proportion of inflorescence number for each observation.

Pollination experiments
We conducted pollination experiments to assess the extent of pollen limitation of both species in 1999 and 2000. We randomly chose 28–84 plants of each species at each plot and marked one inflorescence per plant for a monitoring of seed set under natural pollination, i.e., control. Furthermore, for 15–25 plants among the plants selected, we also performed a hand-pollination treatment for a different inflorescence on each plant to measure seed-set ability without pollen limitation. Pollen for the hand-pollination treatment was collected from three donors growing at 5–20 m apart from each recipient plant.

We harvested all infructescences for the pollination experiments just before dehiscence and preserved them in 70% ethanol. Then we counted the number of matured seeds and aborted or unfertilized ovules for every fruit under a microscope in the laboratory. Fruit set was defined as the proportion of flowers that developed into fruits in each inflorescence. Seed set was defined as the proportion of ovules that developed into matured seeds within an inflorescence. We defined the relative reproductive success (RRS) of an inflorescence by multiplying fruit set by seed set to estimate the seed-set success at the inflorescence level accurately. We defined the extent of pollen limitation per plant level as 1 – C/P, where C and P are the RRS of the control and the hand-pollination treatment, respectively.

To assess the RRS under natural pollination, we performed a two-way ANOVA factored by species (P. caerulea and P. aleutica) and plot (E, M, and L) after arcsine square-root transformation at each site in each year. The differences in RRS among plots within each site were compared by the Bonferroni-Dunn test in each species in each year (P < 0.0167). The extent of pollen limitation (1 – C/P) along the snowmelt gradients was assessed by two-way ANOVA factored by species (P. caerulea and P. aleutica) and plot (E, M, and L) after arcsine square-root transformation at each site in each year.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Floral composition
The proportion of P. caerulea flowers relative to P. aleutica flowers decreased along the snowmelt gradients at all sites in most years (Table 1). The frequencies of flowers of the two species significantly differed across the plots (E, M, and L) within each site and each year (P < 0.001; chi-square test). The number of P. aleutica flowers increased along the snowmelt gradients, indicating that P. aleutica commonly dominates at late snowmelt places in this area, whereas that of P. caerulea flowers often decreased at L plots although there were large fluctuations among years.

View larger version (28K): [in this window] [in a new window]   Fig. 2. Nectar volume per flower of Phyllodoce caerulea (filled bars) and Phyllodoce aleutica (open bars) at each plot (E, M, and L) of three sites (HIS, GOS, and PON) in 1997, 1999, and 2001 (means + 1 SE). N = 20–40

Estimated nectar standing crop was larger in P. caerulea than in P. aleutica at the E and M plots of every site (Table 2). Phyllodoce caerulea presented 2.0–9.5-fold volume of nectar at the E and M plots compared to P. aleutica. However, the nectar standing crop of P. aleutica became larger than that of P. caerulea at the L plots, in which P. aleutica presented 2.6–9.8-fold volume of nectar compared to P. caerulea.

Throughout the 28 observations over plots and years, we counted 40 742 bumble bee visitations to inflorescences of both species, in which the number of visitations per observation ranged from 183 to 2579. Frequencies of bumble bee visitation per inflorescence per hour were 0.37–2.49 at E plots, 0.38–2.71 at M plots, and 0.20–0.55 at L plots in P. caerulea and were 0.15–0.66 at E plots, 0.15–0.88 at M plots, and 0.31–1.26 at L plots in P. aleutica throughout the sites and years. Observed bumble bee visitation to P. caerulea inflorescence at E and M plots was significantly higher than the expectation of proportional visitation based on the floral composition for every observation (P < 0.001; chi-square test; Fig. 3). In all but one case at L plots, however, observed visitation to P. caerulea was significantly lower than the expectation (P < 0.001). These results indicated that bumble bees tended to visit P. aleutica more frequently than expected only where P. aleutica inflorescences were dominant. This situation was observed only around the L plots throughout the sites and years. Thus, bumble bees preferred P. caerulea to P. aleutica unless floral composition was highly biased to P. aleutica.

View larger version (24K): [in this window] [in a new window]   Fig. 3. Relationship between the floral composition and bumble bee preference between the two Phyllodoce species. Proportion of inflorescence number of P. caerulea relative to P. aleutica at each measurement point is labeled as proportion of P. caerulea inflorescence, and the proportion of visitation frequency on P. caerulea relative to P. aleutica is labeled bumble bee preference for P. caerulea. In total, 28 observation data from all sites (in 1993, 1997, 1999, 2000, and 2001) are shown. Diamonds are data from E plots, circles are from M plots, and squares are from L plots. The dotted line crossing the figure is the expected relationship when attractiveness of both species is similar

View larger version (34K): [in this window] [in a new window]   Fig. 4. The extent of pollen limitation of two Phyllodoce species at each plot of three sites in 1999 and 2000 (means + 1 SE). Pollen limitation was calculated by 1 – C/P, where C is seed set by natural pollination and P is seed set by hand-pollination treatment. Filled bars indicate P. caerulea and open bars indicate P. aleutica. N = 15–25. See Table 5 for statistical analyses

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Bumble bee preference
In our system, the two Phyllodoce species are the most common nectar resource for bumble bees because of their predominance across a wide range of snowmelt gradients (T. Kasagi and G. Kudo, personal observation). Plant density often affects the visitation frequency of pollinators (Rathcke, 1983 ; Feinsinger et al., 1991 ; Kunin, 1993 ), and floral composition among species sharing the same pollinators is a fundamental factor determining the pollinator preference (Rathcke, 1983 ; Campbell and Motten, 1985 ; Possingham, 1992 ; Goulson, 1994 ). In addition, floral nectar rewards affect the pollinator foraging behavior (Cresswell and Galen, 1991 ; Possingham, 1992 ), and a high nectar production often increases pollinator attraction, especially in bee-pollinated plants (Thomson and Plowright, 1980 ; Galen and Plowright, 1985 ). The proportion of P. caerulea flowers relative to P. aleutica flowers decreased along the snowmelt gradients in every site and year. Moreover the decrease in nectar production of individual flowers along the snowmelt gradients was more intensive in P. caerulea than P. aleutica throughout the sites and years. Consequently, the superiority of nectar standing crop shifted from P. caerulea to P. aleutica in late snowmelt populations. Reproductive effort of alpine dwarf shrubs is generally sensitive to the restriction of growing season length along snowmelt gradients (Kudo, 1991 ). Decreasing flower proportion and nectar volume of P. caerulea at late snowmelt plots indicate that P. caerulea has a lesser physiological tolerance to short growing season length than P. aleutica. Bumble bee preference shifted obviously from P. caerulea to P. aleutica at late snowmelt plots in accordance with a reversal of nectar standing crop between the species. Such a difference in physiological constraints between the species likely causes a shift of bumble bee preference. The replacement of attractiveness between the species and the shift of bumble bee preference may be a common trend along the snowmelt gradients in our system.

Pollen limitation
The extent of pollen limitation of P. caerulea was high at late snowmelt plots and that of P. aleutica was high at early to middle snowmelt plots. The patterns of pollen limitation corresponded to the shift of bumble bee preference. This indicated that the patterns of pollinator effectiveness along the snowmelt gradients were reversed between the species. Although pollinator visitation frequency may not always be a good indicator of pollination success (Stanton et al., 1991 ; Wilson and Thomson, 1991 ), the extent of pollen limitation often reflects the pollinator availability (Campbell, 1987 ). Pollinator abundance and activity often fluctuate among years even within the same sites (Fishbein and Venable, 1996 ), whereas the extent of pollen limitation along the snowmelt gradients was mostly constant across the years (1999 and 2000) in both Phyllodoce species. When some plant species compete for pollinators, competitively inferior species are often susceptible to a pollination process resulting in low reproductive success (Waser, 1978 ; Rathcke, 1983 ; Campbell and Motten, 1985 ; Kohn and Waser, 1985 ; Campbell, 1986 ; Feinsinger et al., 1988 ; Galen and Gregory, 1989 ; Murcia and Feinsinger, 1996 ; Caruso, 1999 ; Fishman and Wyatt, 1999 ).

As another possibility, the decrease in pollen limitation of P. aleutica at L plots might be caused partly by the increase in conspecific pollen receipt due to the considerably high floral density of P. aleutica. Interspecific movement of bumble bees sometimes occurred between the two Phyllodoce species (T. Kasagi and G. Kudo, personal observation). If seed set is influenced by the interference of heterospecific pollen (Waser and Fugate, 1986 ; Galen and Gregory, 1989 ; Caruso and Alfaro, 2000 ), frequency of interspecific movement of pollinators could be important.

Implications for variation in mating system
Variation in self-compatibility in P. aleutica along the snowmelt gradients, i.e., high in early and middle snowmelt populations and low in late populations (Kasagi, 2002 ), was in accord with the trend of pollen limitation. Despite higher pollen limitation, seed set success under natural pollination of P. aleutica was higher at E and M plots than that at L plots (Table 3). Furthermore, P. aleutica had higher seed set than P. caerulea even at E and M plots (Table 3), where P. aleutica suffered from intensive pollen limitation (Table 5 and Fig. 4). These facts suggest that high selfing ability under pollinator limitation acts as a reproductive assurance mechanism (e.g., Levin, 1972 ; Wyatt, 1986 ; Fausto et al., 2001 ). In a previous study (Kasagi, 2002 ), seed set by artificial outcrossing was 19–39% at E plots and 25–41% at M plots, whereas seed set by artificial selfing was 11–24% at E plots and 11–19% at M plots, and there was a significant difference between the treatments. These results indicate the lower fertilization ability of self pollen and/or early-acting inbreeding depression in P. aleutica despite of high selfing ability.

In contrast, P. caerulea showed a low selfing ability throughout the snowmelt gradients (Kasagi, 2002 ). Phyllodoce caerulea commonly dominates at early to middle snowmelt populations (Kudo and Ito, 1992 ) despite the lower seed-set success under natural pollination, probably because effective outcrossing seed production contributed without extensive pollen limitation. Why didn't P. caerulea shift to a more selfing strategy at late snowmelt plots where pollen limitation was severe? Because the reproductive activity of P. caerulea should decrease at the marginal part of the distribution range along a snowmelt gradient as mentioned before, late snowmelt populations may be maintained not by sexual reproduction but by vegetative growth. In such a case, phenotypic change of mating system may be difficult.

It is reported that P. caerulea has a very high selfing ability in northern Europe (Molau, 1993 ). This indicates that intraspecific variation in mating system may be common in Phyllodoce species in response to pollination availability. An important question is whether P. aleutica behaves as an outcrosser when a competitor, P. caerulea, is lacking. Although P. caerulea and P. aleutica usually co-occur in the Taisetsu Mountains, only P. aleutica exists in the Tateyama Mountain Range of Central Japan located about 900 km southwest of the Taisetsu Mountains. Phyllodoce aleutica at the snowbed of the Tateyama Mountain Range shows very low seed set by selfing (0.9–1.5%) but high seed set under natural pollination (22–32%) irrespective of snowmelt conditions (T. Kasagi and G. Kudo, unpublished data), indicating predominant outcrossing throughout the snowmelt gradient. This is critical evidence that high selfing ability of P. aleutica in the Taisetsu Mountains may be caused by the competition for pollinators with P. caerulea as a reproductive assurance mechanism.

	FOOTNOTES

 
¹ The authors thank T. Ohgushi, H. Ishii, and two anonymous reviewers for their comments on the manuscript; S. Suzuki, K. Narita, and M. P. Butler for their helpful suggestions; and Y. Shimono, S. Kasagi, S. Kosuge, A. Tajima, and A. Hirao for their field assistance.

² kasagi{at}ees.hokudai.ac.jp ; FAX: +81-11-706-4954

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