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Pollen limitation of reproductive success in two sympatric alpine willows (Salicaceae) with contrasting pollination strategies¹

²Department of Biology and Nature Conservation, The Agricultural University of Norway, P.O. Box 5014, N-1432 Ås, Norway ³via Gallicciolli 2, 24121 Bergamo, Italy

Received for publication May 16, 2000. Accepted for publication July 21, 2000.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
We compared the extent of pollen limitation on female reproductive success of Salix lanata L., an entirely insect-pollinated willow, and S. lapponum L., which is 50 : 50% insect : wind pollinated (ambophilous). Supplemental hand-pollination significantly increased seed number per fruit by nearly 50% in the insect-pollinated willow, but had no significant impact on seed number in the dually pollinated species. Fruit set was not affected by the treatment in either of the species. These results demonstrate that pollen limitation on reproductive success is most pronounced in the species that depends entirely on insects for pollination. In general, pollinator visitation was highest to S. lapponum, but bumble bees were only observed on S. lanata, suggesting that the quantity and quality of pollinator visitation differed between the species. Our results empirically support the hypothesis that a dual pollination strategy is most effective in alpine environments with low and infrequent pollinator activity and high wind speeds.

Key Words: alpine • natural selection • pollen limitation • reproductive assurance • resource depletion • Salix • wind pollination

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The interspecific variation in pollen dispersal mechanisms is related to the spatial distribution of species. In particular, there is a geographical difference in the distribution of insect- and wind-pollinated species, and the latter are proposed to be proportionally more abundant in alpine habitats (Müller, 1881 ; Regal, 1982 ; Whitehead, 1983 ). For example, the proportion of wind-pollinated relative to insect-pollinated species in Norway is higher in the alpine compared to the lowlands (Ø. Totland, J. A. Grytnes, and W. Eide, unpublished data). In a detailed study on the high Andean genus Espeletia, Berry and Calvo (1989) found that species occurring at the highest elevations were wind pollinated while animal-pollinated species prevailed at lower elevations. Furthermore, in Hormathophylla spinosa, a typical insect-pollinated crucifer, Gomez and Zamora (1996) demonstrated that wind pollination plays an important role for reproductive success at high elevations. In Linanthus parviflorus, a self-incompatible predominantly insect-pollinated annual, wind pollination provided reproductive assurance in a windy exposed site (Goodwillie, 1999 ).

There are two main explanations for the increased proportion of wind-pollinated species in alpine habitats. First, the abundance and efficiency of pollinators and their diversity generally decrease with altitude, probably because of thermal constraints on pollinator flight activity and population density (Cruden, 1972 ; Levesque and Burger, 1982 ; Arroyo, Armesto, and Primack, 1985 ; Arroyo, Primack, and Armesto, 1985 ; McCall and Primack, 1992 ; Totland, 1993 ). Second, wind speed increases with altitude and this, combined with fewer obstacles to airborne pollen flow, could facilitate wind pollination in open alpine habitats to a greater extent than in, e.g., lowland forest habitats. In addition, pollinator activity and wind speed are interconnected: high wind speeds constrain pollinator flower visitation (Totland, 1994 ).

It could be hypothesised that because animal pollinators are scarce and their activity infrequent in alpine habitats, this constrains the reproductive success of the plants that they pollinate due to fewer pollen grains being deposited on stigmas relative to the amounts of resources available for reproduction. If so, selection could favor pollination strategies that make reproductive success less dependent on pollinator activity, such as self- or wind pollination, to assure reproduction under conditions of low and unreliable pollinator service (Baker, 1955 ; Stebbins, 1957 ; Barrett, 1988 ). However, few studies have actually tested this hypothesis by comparing the extent of pollen limitation on reproductive success between closely related species with contrasting pollination strategies (but see Parker, Nakamura, and Schemske, 1995 ; Ushimaru and Kikuzawa, 1999 ).

Species of the genus Salix exhibit a mixture of pollination strategies. Some appear to be entirely wind pollinated, some are entirely insect pollinated, whereas many are pollinated by both vectors (ambophilous) (Kevan, 1972 ; Argus, 1974 ; Meeuse, 1978 ; Sacchi and Price, 1988 ; Vroege and Stelleman, 1990 ; Fox, 1992 ; Douglas, 1997 ; Peeters and Totland, 1999 ). This dual pollination strategy within Salix is reflected in the flower and catkin forms of the species. They have outreaching stamens and pistils, the perianth is absent, and they often flower before leafing and release pollen in the air (Fisher, 1928 ). These features are typical for wind-pollinated species (Fægri and van der Pijl, 1979 ). On the other hand, in many species both sexes produce nectar (Kevan, 1972 ; Peeters and Totland, 1999 ), release a scent (Kevan, 1972 ; Tollsten and Knudsen, 1992 ), and have stiff catkins that are erect and highly visible (Fisher, 1928 ), suggesting that they are adapted to insect pollination (Fægri and van der Pijl, 1979 ). In a study of the pollination strategy of alpine Salix spp. in southern Norway, Peeters and Totland (1999) found that predominately insect-pollinated species produced more nectar and had longer flowers and bigger catkins than species that were pollinated by both insects and wind.

In this study, we compare the extent of pollen limitation on seed and fruit production in the alpine Salix lanata and S. lapponum. Results from another study (Peeters and Totland, 1999 ) done in the same study area and season as ours, show that almost the entire seed set of S. lanata is the result of insect pollination, whereas wind and insect pollination have about equal importance for seed set in S. lapponum. Because of the scarcity of pollinators and the generally frequent high wind velocity in our study area, the alpine of Norway, we predicted that pollen limitation would be most pronounced in S. lanata. Specifically we asked (1) whether pollen limitation on seed and fruit production differ between the two species, (2) whether the seed production by one catkin affects seed production in closely situated catkins on the same branch, and (3) whether pollinator visitation and the composition of the pollinator assemblage differ quantitatively and qualitatively between the two species.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Study area
This study was done on the south-facing slope of Kvannjolnuten (60°32' N, 7°32'E) at 1280 m elevation, 2.5 km east of Finse railway station in southwest alpine Norway. Average June, July, and August temperatures at Finse are 5.0°, 7.0°, and 6.8°C, respectively, and average total precipitation for the same months is 69, 88, and 111 mm (Aune, 1993a, b ). The snow melts around early June in the study site. Soil moisture at the site is high, and grasses and sedges dominate the vegetation. Both our study species, Salix lanata and S. lapponum, occur abundantly in the area.

Study species
Both study species are dioecious shrubs, reaching a height of 20–100 cm. Individual flowers occur in dense units termed catkins. The species grow intermingled in the study area. Flowering of S. lanata normally starts in early June, 1–2 wk earlier than flowering in S. lapponum. Catkin form differs profoundly between the species. Salix lanata has bright yellow flowers, but S. lapponum has dull grey flowers. The catkins of S. lanata are 27 mm long and those of S. lapponum are 20 mm. Salix lanata has on average 154 flowers per catkin, whereas S. lapponum has 119 flowers. Female flowers of S. lanata are also longer and produce more nectar than those of S. lapponum (Peeters and Totland, 1999 ). The average number of catkins per plant with open flowers per day is 16.9 for S. lanata and 11.1 for S. lapponum. Although their pollen production per anther is similar, the number of pollen grains in the air is about three times higher for S. lapponum than for S. lanata (Peeters and Totland, 1999 ). Both study species belong to the subgenus Vetrix and are thus closely related.

Pollen limitation
We employed supplemental pollen addition to assess whether the amounts of pollen reaching stigmas constrain seed and fruit production in the two species. For both species, we randomly selected 15 pairs consisting of two closely situated plants (maximum 3 m apart). In each pair one plant was assigned to be a control and the other to receive a supplemental pollination treatment. We marked one catkin on the control plant and two closely situated (maximum 10 cm apart) catkins on the experimental plant. One of the catkins on the experimental plant was supplementally pollinated while the other was left untreated. To accomplish pollen addition, we collected entire male catkins with pollen-laden anthers on plants growing 2–10 m from our experimental plant and carefully brushed these across the receptive stigmas on recipient catkins on at least 2 d during anthesis of the catkins. During hand-pollination, care was taken such that pollen was not dispersed in the air to the neighbor catkin that was used as a control. We collected three mature fruits (indicated by the presence of a narrow slit at the fruit tip) situated in the lower, middle, and upper part of the catkins and counted the number of seeds in each fruit. We used the average seed production of these three fruits in statistical analyses. We also counted the number of ripe and the number of undeveloped fruits on each catkin to assess their fruit production.

Our experimental procedure does not allow a test of pollen limitation on the whole-plant level because we did not pollinate all the catkins on the experimental plants. However, we could test whether boosted seed and fruit production of supplementally pollinated catkins resulted in decreased reproductive output, resulting from resource depletion, in closely situated catkins on the same branch (Haig and Westoby, 1988 ; Zimmerman and Pyke, 1988 ; Fox, 1992 ) by considering the following predictions. (1) If seed or fruit production of the supplementally pollinated catkins are significantly higher than of the control catkins on the other plants, then seed or fruit production of individual catkins are limited by pollen availability. (2) An increased seed or fruit production after supplemental pollination and a decrease in seed of fruit production in the catkin close to the supplementally pollinated catkin indicate that the boosted reproductive output after supplemental pollination resulted in resource limitation for reproduction in the closely situated catkin.

We used two-factor ANOVA, separate for each species, with treatment and pair as factors, to examine whether supplemental pollination affected seed number per fruit and percentage fruit set. To test for pollen limitation, we included the supplementally pollinated catkins and the catkins on the completely untreated plant in the treatment factor. To test for resource depletion, we included the untreated catkin on the pollinated plant and the catkins on the completely untreated plant in the treatment factor. To meet the assumptions of homogeneity of variance and normality of ANOVA, seed number per fruit was square-root transformed and percentage fruit set was arcsine square-root transformed.

Flower visitors
We measured the flower visitation to 48 and 52 randomly selected female plants of S. lanata and S. lapponum, respectively. Several times during each day of appropriate weather conditions for insect flight activity we carefully approached the plants and noted the number of insects on the catkins at one moment in time. Insects were broadly categorized into the following groups: large flies (e.g., Muscidae, Anthomyidae, Syrphidae), small flies (e.g., Chironomidae, Sciaridae), bumble bees (Bombus spp.), stinging wasps (Vespidae), parasitic wasps (e.g., Ichneumonidae), and Lepidoptera. Solitary bees do not occur at Finse. We also counted the number of catkins with open flowers on each plant on the days insect censuses were made. Then, we calculated a visitation index for each visitor group on each plant by averaging the numbers of insects per catkin. We used t tests to examine whether the number of visitors per catkin at one moment in time differed between the two species. Separate analyses were done for each visitor group and also for the total number of visitors.

Plant density
The density of males can influence pollination success of females in dioecious wind-pollinated species (Whitehead, 1983 ). Therefore, we counted the number of male catkins in a 2 m radius around the plants used for the flower visitation measurements above when they were at maximum flowering. We used a t test to examine whether the availability of male catkins differed significantly between the two species.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Pollen limitation
Supplemental hand-pollination increased mean seed number per fruit by 46% in S. lanata and by 20% in S. lapponum (Fig. 1A, comparison of seed number in hand-pollinated catkins with seed number in catkins on untreated plants). The increase in seed number after hand-pollination was significant only for S. lanata (Table 1). The boosted seed number after supplemental pollination in S. lanata had no negative effect on seed number in the catkins situated closest to those that were hand-pollinated. In fact, a statistically nonsignificant increase was evident (Fig. 1A, Table 1). No difference in seed number per catkin between the control catkins on the hand-pollinated plant and the catkins on untreated plants was evident in S. lapponum (Fig. 1A, Table 1).

View larger version (30K): [in this window] [in a new window]   Fig. 1. Mean seed number per fruit (A) and percentage fruit set of catkins (B) in Salix lanata and S. lapponum at Finse, Norway, in 1997 in an experiment testing for pollen limitation and resource depletion. The experiment consists of control catkins on completely untreated plants, supplementally pollinated catkins, and catkins in close proximity (maximum 10 cm apart) and on the same plant as the supplementally pollinated catkins. Vertical lines above bars are standard errors. See Table 1 for statistical analyses

Flower visitation
Large and small flies were the most abundant flower visitors to catkins of both species (Table 2). Bumble bees (mostly queens of Bombus lapponicus and B. alpinus) were only observed on S. lanata. Catkins of S. lapponum were significantly more often visited by muscoid flies and parasitic wasps than were catkins of S. lanata, whereas Lepidoptera were significantly more often observed on catkins of S. lanata. In total, the number of visitors at one moment in time was significantly higher (33%) in S. lapponum than in S. lanata (Table 2).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Female reproductive success was significantly limited by pollen availability in the entirely insect-pollinated willow (S. lanata), but not in S. lapponum, which employs both insects and wind as pollen vectors. The most likely reason for the difference in the extent of pollen limitation between the two species is their different pollination strategy. If so, our results indicate that a dual pollination strategy (ambophily) is most efficient for pollen dispersal and capture in alpine willows. Given the abiotic environmental conditions in alpine habitats, this is not surprising. The abundance of insect pollinators is low compared to most lowland habitats (Arroyo, Armesto, and Primack, 1985 ; Arroyo, Primack, and Armesto, 1985 ; McCall and Primack, 1992 ; Totland, 1993 ). In addition, conditions for wind dispersal of pollen grains are ample. Although pollen limitation on female reproductive success appears to be common in Salix (Kevan, 1972 ; Argus, 1974 ; Elmquist, Ågren, and Tunlid, 1988 ; Sacchi and Price, 1988 ; Fox 1992 ), no studies known to us have compared the extent of pollen limitation of willows with known wind to insect pollination ratios under similar environmental conditions. Floral traits of S. lanata (yellow catkins, higher nectar content, larger female flowers) are likely to be better suited for pollinator attraction than those of S. lapponum (greyish catkins, lower nectar content, smaller female flowers). However, despite this, insect visitation frequencies to catkins were in general higher in S. lapponum than in S. lanata. It is likely that pollinator availability is lower during the slightly earlier flowering of S. lanata compared to that of S. lapponum (1–2 wk) and that this explains the difference in pollinator visitation frequency between the species. The higher visitation to S. lapponum than to S. lanata could also contribute to the difference in pollen limitation between them. However, although the number of catkin visits differ between the species, it is possible that the quality of visits is higher to S. lanata compared to S. lapponum because bumble bees, and to a lesser extent Lepidoptera, were most frequent on S. lanata. Further studies are needed to assess in more detail the importance of pollinator visitation relative to the pollination strategy in relation to the difference in pollen limitation between the two willows.

Given our results of significant pollen limitation in S. lanata and no pollen limitation in the dual-pollinated S. lapponum, it is pertinent to ask why S. lanata is not pollinated by wind in addition to insects, to the same degree as S. lapponum. Although their pollen production per anther is equal, the amount of S. lapponum pollen in the air is about three times higher than that of S. lanata (Peeters and Totland, 1999 ), showing that pollen release from anthers by wind is much higher in S. lapponum than in S. lanata. The extended length of stamens facilitates pollen release in the air (Fægri and van der Pijl, 1979 ; Whitehead, 1983 ). However, stamen length does not differ between the two species (Peeters and Totland, 1999 ). It is possible that differences in pollen form, size, or stickiness cause the differences in pollen release in the air and so also explain the greater pollination success of S. lapponum compared to S. lanata. Further studies are required to test this hypothesis.

Although the availability of males in our study area was similar for the two species, it is possible that pollinator availability, particularly bumble bees, to S. lanata at Finse is significantly lower than at lower elevation or during other seasons. Thus, if we conducted our study at a lower elevation or in another season with higher pollinator availability and less wind, it is possible that the extent of pollen limitation would not differ between the species.

Boosted seed production in supplementally pollinated S. lanata catkins did not cause a resource depletion that reduced seed production in neighboring catkins. This suggests that seed production of catkins on the same branch is autonomous and independent of the investments in reproduction in other catkins on the same branch, consistent with what Fox (1992) found in Salix alaxensis in Alaska. This result could imply that seed set is pollen limited on the whole-plant level in S. lanata, but because we only supplementally pollinated a single catkin per plant, we cannot make such a conclusion. Nevertheless, because maturation of all fruits on a plant occurs almost simultaneously in the two studied willows, resources for reproduction may be committed in advance (see also Fox, 1992 ) and may not be redistributed among catkins according to pollination success. In addition, seed maturation may also be partly supported by photosynthesis of the green developing fruit (Bazzaz, Carlson, and Harper, 1979 ; Galen, Dawson, and Stanton, 1993 ). This factor may be further enhanced by increased air temperature within catkins (Kevan, 1990 ).

We conclude that the contrasting pollination strategy of S. lanata and S. lapponum is the main causal basis for the differences found in the extent of pollen limitation on seed production between them. The dual pollination by both wind and insects in S. lapponum functions as a reproductive assurance mechanism under conditions of low and sporadic pollinator service during spring in alpine habitats.

	FOOTNOTES

 
¹ The authors thank Peter Kevan and an anonymous reviewer for constructive comments on the manuscript and the Research Council of Norway for financial support to Ø.T. Field work for this paper was done while M.S. visited Norway on an ERASMUS grant. We thank the Alpine Research Centre at Finse for living facilities.

⁴ Author for reprint requests (e-mail: orjan.totland{at}ibn.nlh.no)

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