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Brief Communication |
Department of Biology, Middlebury College, Middlebury, Vermont 05753 USA; Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697 USA
Received for publication January 11, 2007. Accepted for publication May 30, 2007.
ABSTRACT
Flowers of most plant species are visited by a variety of animals. Some of these visitors are effective pollinators while others remove resources without transferring pollen. Studies comparing the effectiveness of different visitors as pollinators often compare taxa without considering variation in behavior within a taxon. Wilson and Thomson (Ecology 72: 1503–1507, 1991) documented the effects of honey bees and bumble bees on the pollination dynamics of Impatiens capensis. They found that pollen-collecting honey bees removed large numbers of pollen grains from anthers but deposited little of it on stigmas; bumble bees, which sought nectar, removed less pollen but deposited more of it on stigmas. It is unclear whether the low pollen transfer efficiencies of honey bees are explained by their morphology or by their pollen-collecting behavior. We repeated the work of Wilson and Thomson at a site where honey bees were foraging for nectar, not pollen. We measured the quantity of pollen remaining in anthers, the number of pollen grains deposited on stigmas, and seed production after single visits by honey bees and bumble bees. The differences between the taxa disappeared when they were foraging in a similar manner. Our results clearly demonstrate the importance of foraging behavior on the pollination effectiveness of floral visitors.
Key Words: Apis mellifera • Balsaminaceae • Bombus impatiens • bumble bees • honey bees • pollinator effectiveness • Vermont
Different floral visitors have different effects on pollen removal, pollen deposition, and/or seed production of the flowers they visit. The relative importance of floral visitors to the reproductive success of plants is a function of how effectively they transfer pollen from anthers to stigmas, as well as their relative visitation frequency. Fenster et al. (2004)
reviewed the various metrics biologists have used to measure pollinator effectiveness, ranging from how many of each floral visitor species carry conspecific pollen to the potential for geitonogamy for each species; these measurements determine the "quality" of each floral visitor. The "quantity" of each visitor species is its visitation rate to flowers. The quality and quantity of each visitor then contribute to their "pollinator importance" (Olsen, 1997
). Sometimes the most common pollinator is also the most effective pollinator (Willmer et al., 1994
; Fishbein and Venable, 1996
; Stone, 1996
; Olsen, 1997
; Freitas and Paxton, 1998
; Ivey et al., 2003
). Often, however, the most effective pollinator can be unexpected (also reviewed by Fenster et al., 2004
). For example, uncommon bumble bees visiting the "hummingbird-pollinated" Ipomopsis aggregata transfer pollen more efficiently and their visitation results in greater seed production than the more common hummingbirds (Mayfield et al., 2001
). Other examples of the uncoupling of quantity and quality of floral visitors reiterate the importance of measuring quality and quantity of pollinator visits separately (Spears, 1983
; Schemske and Horvitz, 1984
; Potts et al., 2001
; Wolff et al., 2003
; McIntosh, 2005
).
Pollen removal from anthers and deposition on stigmas by floral visitors are often measured to compare pollinator quality (reviewed in Fenster et al., 2004
). In elucidating the differences among visitors in their pollen transfer efficiencies, Thomson and Thomson (1992)
imagined three idealized pollinators based on the proportion of pollen they remove from anthers that is deposited on conspecific stigmas. Thomson et al. (2000)
refer to "high removal–high deposition" pollinators that deposit a large proportion of the large quantity of pollen they remove from anthers onto stigmas, "low removal-high deposition" pollinators that remove little pollen from anthers but deposit a high proportion of that pollen on stigmas, and "high removal–low deposition" pollinators that remove large amounts of pollen from anthers and deposit little of that pollen on stigmas. As such, high removal–low deposition pollinators are very poor pollinators: they waste pollen by removing significant amounts and deposit little on receptive stigmas. When high removal–low deposition pollinators are the only floral visitors, pollination occurs but there is tremendous pollen wastage (Lau and Galloway, 2004
). When both high removal–low deposition and low removal–high deposition pollinators visit a plant species, the pollination effectiveness of the low removal–high deposition pollinator will be reduced if flowers are first visited by high removal–low deposition pollinators (Wilson and Thomson, 1991
; Harder and Barclay, 1994
; Gross and Mackay, 1998
; Williams and Thomson, 2003
; Carmo et al., 2004
). Even within a pollinator taxon, the pollen removal–deposition dynamics may vary with pollinator behavior at flowers (collecting nectar vs. collecting pollen, for instance; Goodell and Thomson, 1996
; Freitas and Paxton, 1998
; Williams and Thomson, 2003
). This context-dependent pollinator effectiveness reflects the complexity of ecological interactions and animal behavior.
Wilson and Thomson (1991)
examined the pollen transfer dynamics of honey bees (Apis mellifera) and bumble bees (Bombus impatiens) visiting the flowers of jewelweed (Impatiens capensis Meerb., Balsaminaceae). At their study site (on Long Island, New York, USA), honey bees collected pollen from jewelweed flowers by hanging upside-down from the anthers and scraping pollen onto their bodies. Bumble bees visited the flowers for nectar and in doing so, walked headfirst into the corolla, rubbed their dorsal surfaces against the anthers, and incidentally transferred pollen. These behavioral differences resulted in different pollen transfer efficiencies: honey bees removed large quantities of pollen from anthers (twice as much as Bombus) but deposited 10 times less pollen on the stigmas of female-phase flowers and thus qualified as high removal–low deposition pollinators. However, in Wilson and Thomson's study, honey bees could have been inefficient pollinators because of their morphology (honey bee workers are usually smaller, slimmer, and less hairy than B. impatiens workers) or because of their behavior (actively collecting pollen from flowers). These two aspects were correlated at their study site: honey bees always collected pollen. In contrast, at a study site in Vermont, we found honey bees collecting nectar rather than pollen from jewelweed flowers, which allowed us to address how the pollen transfer dynamics of honey bees are influenced by their behavior. Flowers at both of our study sites were also visited by nectar-collecting B. impatiens, which allowed direct comparison of their foraging efficiencies between the sites. As an extension of Wilson and Thomson's study and to relate pollinator taxon and behavior more tightly with the female component of plant reproductive success, we also examined seed production resulting from floral visits by nectar-collecting honey bees and bumble bees.
MATERIALS AND METHODS
All fieldwork was completed during August and September 2003. The study site was a large field bordered by forest and hay fields on the outskirts of Middlebury, Vermont, USA (44°02'53.81'' N, 73°06'07.72'' W, 145 m elevation). Pollinators other than A. mellifera and B. impatiens that were present and visiting flowers included other Bombus species, wasps, and hummingbirds; because these other pollinators were relatively rare during 2003, we do not include their pollen transfer dynamics in this paper. Chasmogamous flowers of I. capensis are protandrous: they are male for about 24 h before the androecium falls off to reveal the receptive stigma. This species is self-compatible, but selfing occurs only through pollinator movement between chasmogamous flowers on the same plant because of the marked protandry of individual flowers. Outcrossing rates of chasmogamous flowers ranges from 0.29 to 0.71 (Waller and Knight, 1989
); cleistogamous flowers do not open and have an outcrossing rate of zero.
We closely followed Wilson and Thomson's methods to make our results as comparable as possible. Like Wilson and Thomson, we examined the pollen transfer dynamics of Apis mellifera and Bombus impatiens resulting from single floral visits. We also replicated their experiment by varying the exposure time of flowers to pollinators but did not include these results here because they did not directly test the effect of foraging behavior on pollen dynamics. Flower buds were bagged with bridal veil during the afternoon. For pollen removal experiments, we unbagged flowers the following morning, when they were in male-phase (N = 109). For pollen deposition (N = 84) and seed production (N = 83) experiments, we unbagged the flowers 36 h after bagging, when the androecium had dropped off and the flowers were in female-phase.
We measured three variables resulting from single visits: pollen not removed from the androecium by bees, pollen deposited on stigmas by bees, and seed production. To measure pollen not removed, anthers were collected without being visited by a pollinator (control) or after a single visit by A. mellifera or B. impatiens. Anthers were placed in microcentrifuge tubes, dried 24 h, suspended in 95% ethanol, and sonicated for 15 min to further extract pollen from the androecium. Pollen grains were counted with a Coulter Z2 particle counter (Beckman Coulter, Fullerton, California, USA) using a 70 µm orifice in the sampling tube; three subsamples of 0.1 mL were counted and averaged for each flower. To directly compare our pollen removal data with similar data in the Wilson and Thomson study, we read pollen numbers (mean and SE) from their Fig. 1. It should be noted that the y-axes for pollen remaining in the androecium are incorrect in both figures in Wilson and Thomson (1991)
: instead of reading 103 pollen grains remaining, the axes should read 104 pollen grains (P. Wilson, California State University Northridge, personal communication).
|
). Control stigmas were also collected from previously bagged, unvisited flowers to detect pollen deposition on stigmas as the androecia dropped off. All pollen grains on each stigma were counted using a compound microscope. For seed production, we unbagged female-phase flowers and exposed them to single visits or no visits. We rebagged them until the corolla had fallen off (usually within 24 h) to prevent further visitation, then bags were removed to allow natural fruit development. We censused developing fruits weekly to monitor fruit abortion and to differentiate aborted fruits from eaten fruits. We counted maturing seeds per fruit three weeks later, before the fruits had dehisced. We timed the length of visits by bees to a subset of the single visits to flowers to determine whether visit length could explain any differences in pollen dynamics between the taxa.
We used ANOVA to detect variation among treatments (no visits and single visits by each bee taxon) using SPSS 11.0 (SPSS Mac OS X version 11.0.4, SPSS Inc., Chicago, Illinois, USA). Treatment (visitor species and unvisited) was used as a fixed effect. We compared the two taxa in their pollen removal and deposition and seed production effects using independent sample t tests. Pollen remaining in anthers was untransformed; the number of pollen grains deposited on stigmas and seed number were rank-transformed before analysis. We analyzed seed number in two ways: in one, aborted fruits were assigned seed number of zero, and in the other we removed aborted fruits before analysis. Because plants did not have enough flowers available to completely nest these experiments within each plant, plant individual could not be used as a blocking factor in these analyses.
RESULTS
When they both foraged for nectar (this study), honey bees and bumble bees did not differ in the number of pollen grains remaining in anthers (t = 0.42, df = 54, P = 0.67, Fig. 1A), the number of pollen grains deposited on stigmas (t = 0.6, df = 67, P = 0.55, Fig. 1B), the number of seeds produced after a single visit (aborted fruits assigned a seed number of zero: t = 0.51, df = 62, P = 0.61, Fig 1C; aborted fruits deleted: t = 0.13, df = 39, P = 0.90), or the length of a single visit (Apis: mean = 20.5 s, SD = 14.8, N = 38; B. impatiens: mean = 16.7 s, SD = 8.0, N = 18; t = 1.02, df = 54, P = 0.3). Bees removed so little pollen that pollen numbers of visited flowers were not significantly different than those of unvisited flowers (F2,108 = 0.45, P = 0.64). However, unvisited flowers had less pollen deposited (F2,83 = 4.5, P = 0.013) and fewer seeds per fruit (F2,82 = 5.32, P = 0.007) than flowers visited a single time (Fig. 1A–C). As expected, single visits by B. impatiens in this study and that of Wilson and Thomson did not differ in either the number of pollen grains remaining in the androecium (t = 1.14, df = 52, P = 0.26) or the number of pollen grains deposited on a stigma (t = 1.09, df = 51, P = 0.28). In contrast, pollen dynamics resulting from visits by Apis differed significantly between the two studies: pollen-collecting Apis in Wilson and Thomson's study left significantly fewer pollen in the anthers (t = 5.78, df = 81, P < 0.0001; Fig. 1A) and deposited significantly fewer pollen on stigmas (t = 4.26, df = 76, P < 0.0001; Fig. 1B) than the nectar-collecting Apis in our study.
Much more pollen was available in anthers of flowers at Wilson and Thomson's site, so we also analyzed the absolute number of pollen grains removed from anthers by the two types of visitors. To extract these data from the figures of Wilson and Thomson, for each visit type, we subtracted the mean number of pollen grains remaining in anthers from the mean number of pollen grains in unvisited anthers. We estimated the standard error of this value as the sum of the standard errors of these pollen numbers. The number of pollen grains removed differed between the studies: single visits by both B. impatiens and Apis removed significantly more pollen from anthers in Wilson and Thomson's study than did single visits by the bees in our study (t = 2.95, df = 52, P < 0.005 for B. impatiens; t = 6.21, df = 81, P < 0.0001 for Apis; Fig. 1D). Apis removed significantly more pollen than B. impatiens in Wilson and Thomson's study (t = 3.51, df = 79, P = 0.0007), whereas the difference in pollen removal between the taxa in our study was not statistically significant (t = 0.21, df = 54, P = 0.84).
In a further comparison of our results to those of Wilson and Thomson, we calculated the percentage of pollen that bees removed from anthers then deposited on stigmas during a single visit. Pollen transfer efficiencies were lower for both taxa in Wilson and Thomson's study (0.003% of the pollen removed by Apis in a single visit was deposited on stigmas, 0.088% for B. impatiens) than in our study (0.64% and 0.28%, respectively).
DISCUSSION
Pollen removal from anthers and deposition on stigmas are strongly affected by the foraging behavior of pollinators. When Apis collect pollen and Bombus collect nectar from flowers of I. capensis (Wilson and Thomson's study), Apis act as a high removal–low deposition forager, removing significantly more pollen from anthers than Bombus but depositing significantly less pollen on stigmas. However, when both Apis and Bombus are collecting nectar (this study), they both act as low removal–high deposition pollinators during single visits to flowers. In addition, a single floral visit for nectar by either taxon has similar duration and results in similar numbers of seeds produced. These data suggest that foraging behavior explains the differences between the taxa in Wilson and Thomson's study.
Other researchers have also found effects of foraging behavior on pollination efficiency. Sometimes foraging for nectar results in higher pollination effectiveness (Freitas and Paxton, 1998
), but not always. Other researchers have concluded that pollen-collecting bees are more efficient than nectar-collecting bees at facilitating female function because they carry more pollen on their bodies (Free and Williams, 1972
; Gomez and Zamora, 1999
; Cane and Schiffhauer, 2001
; Stubbs and Drummond, 2001
; Javorek et al., 2002
), especially when nectar foragers approach flowers from the side (Goodell and Thomson, 1996
; Williams and Thomson, 2003). Such studies seldom measure pollen removal, however, so the overall contribution of different foraging modes to plant reproductive success remains uncertain, as the models of Thomson and Thomson (1992)
demonstrate. It is certain, however, that the specific behavior of pollinators in many systems greatly influences their pollen transfer efficiencies.
There is a striking difference in the pollen transfer efficiencies (percentage of pollen removed from anthers that is deposited onto stigmas) by bees between our study and Wilson and Thomson's study. In particular, pollen-collecting bees in their study transferred between one and two orders of magnitude less pollen from anthers to stigmas than the nectar-collecting B. impatiens in both studies. We found pollen transfer efficiencies of nectar-collecting bees to be in the range of those reported for other bee pollinated taxa (0.1% reported by Snow and Roubik [1987
] for Cassia visited by Centris bees, Conner et al. [1995
] for Raphanus flowers visited by Apis; 0.6% reported by Harder and Thomson [1989
] for Erythronium visited by Bombus, Young and Stanton [1990
] for Raphanus visited by Apis; 1.0% reported by Freitas and Paxton [1998
] for Anacardium visited by Centris). In contrast, the pollen transfer efficiencies for pollen-collecting Apis in Wilson and Thomson's study are much lower than these values. This low transfer efficiency cannot be the result of avoidance of female-phase flowers, because only visited flowers were included in the experiments. Instead, it is likely that pollen-collecting bees contact anthers with their ventral surface, which is easily groomed, while nectar-collecting bees contact anthers with their dorsal surface, which is not readily groomed (Thorp, 2000
). In addition, when bees are collecting pollen for use by the colony, they may be efficient at transferring pollen into their corbiculae, which do not contact the stigmas of subsequently visited flowers (Thorp, 2000
; Williams and Thomson, 2003
). Apis wet pollen with nectar before storing it in corbiculae (Michener, 1999
), making it impossible for this pollen to be dislodged onto stigmas of subsequently visited flowers.
The proportion of pollen that Bombus groom off of their bodies is directly proportional to the amount of pollen they remove from anthers (Harder and Thomson, 1989
). Therefore, pollen deposition on stigmas can be inversely proportional to the amount of pollen Bombus remove from anthers, which could explain the pollen dynamics of B. impatiens. Flowers of I. capensis at Wilson and Thomson's site had 67% more pollen in their anthers than flowers at our site (which might represent geographical variation in this trait or differences in pollen extraction or counting techniques between the studies). This translated into much more pollen being removed in single visits by both Apis and B. impatiens in their study than in ours, but did not translate into different pollen deposition rates on stigmas by B. impatiens. The B. impatiens at our site were less wasteful with the pollen that collected on their bodies, perhaps because they groomed less pollen off their bodies. Bombus impatiens removed more pollen from the anthers of I. capensis on Long Island, groomed off more pollen, and therefore deposited similar total quantities (but a smaller proportion) on stigmas compared to B. impatiens in Vermont. Pollen-collecting Apis also removed large quantities of pollen but deposited little (perhaps because they efficiently move pollen into their corbiculae or they groom large quantities off of their bodies). In fact, little is known about the fate of pollen picked up by honey bees. Structural and behavioral adaptations for grooming were elucidated by Hlavac (1975)
, Michener et al. (1978)
, and Thorp (1979)
, but the models of pollen grooming by Harder and Thomson (1989)
were derived from data on Bombus; it is not clear whether these models can be applied to other bee genera. What we have clarified in this study is that nectar-collecting Apis remove less pollen than pollen-collecting Apis, but deposit more on stigmas, shifting them from high removal–low deposition pollinators to low removal–high deposition pollinators.
If and when differences exist between Apis and Bombus in their foraging patterns (collecting nectar vs. pollen), the order of floral visitation is important. When pollen-collecting Apis visit flowers first, they will remove pollen that could be more efficiently transferred by Bombus. However, in most temperate climates and at high elevations, Bombus forage earlier in the morning and continue to forage in inclement weather, when Apis are not active (Willmer et al., 1994
; Kearns and Thomson, 2001
; Potts et al., 2001
; Stubbs and Drummond, 2001
; Stanghellini et al., 2002
). This will mitigate the deleterious effects of pollen-collecting Apis: many flowers will already have been visited by Bombus by the time Apis start foraging, yielding several effects. First, with Bombus visiting flowers earlier, their efficient pollen transfer will result in significant pollen deposition on stigmas. Second, they will have removed at least some of the pollen from anthers, leaving less for pollen-collecting Apis (or any pollen-collector) to inefficiently transfer. In fact, with less pollen available for removal by pollen-collecting bees, the negative effects of pollen-collectors might disappear, if grooming intensity is positively related to pollen removal.
Wilson and Thomson (1991)
describe the context dependent value of different pollinators: pollen-collecting Apis alone are poor pollinators but they do move pollen from anthers to stigmas. When pollen-collecting Apis coexist with nectar-collecting B. impatiens, Apis becomes an antagonist, removing pollen from the system that B. impatiens can more effectively transfer. We would like to add yet another context to this scenario: the behavioral flexibility of pollinators. Although nectar-collecting Apis are more efficient pollinators of I. capensis than pollen-collecting Apis, we document here that when Apis are collecting nectar rather than pollen, they are equally efficient pollinators as B. impatiens. When individuals of both taxa are collecting nectar, the order of visitation and the relative abundance of these two visitors are irrelevant to I. capensis because they are equally efficient at transferring pollen from anthers to stigmas (as found on other plant species by Tepedino, 1981
; Dieringer, 1992
; Dag and Kammer, 2001
; Thomson and Goodell, 2001
).
There is a wealth of literature on the effectiveness of different floral visitors as pollinators. Almost all of the studies described the pollen transfer efficiencies as taxon-specific features, not recognizing that the behavior of the visitor will greatly affect the quantity of pollen it removes from anthers and deposits on stigmas. Our work clearly demonstrates that, when comparing different pollinators, researchers should consider pollinator behavior.
FOOTNOTES
1 The authors thank L. von Hasseln and S. Lena for their assistance in the field; B. Wood for permission to work on her property; P. Wilson, J. Thomson, D. Stratton, and an anonymous reviewer for helpful comments on the manuscript; and M. Quesada and the Centro de Investigaciones en Ecosistemas at UNAM, Morelia, Mexico, for hospitality to H.J.Y. This research was supported by grants from VT-EPSCor and the Howard Hughes Medical Initiative to Middlebury College. 
4 Author for correspondence (hjyoung{at}middlebury.edu
)
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