The Functional Significance of Poricidal Anthers and Buzz Pollination: Controlled Pollen Removal From Dodecatheon

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The Functional Significance of Poricidal Anthers and Buzz Pollination: Controlled PollenRemoval From DodecatheonAuthor(s): L. D. Harder and R. M. R. BarclaySource: Functional Ecology, Vol. 8, No. 4 (Aug., 1994), pp. 509-517Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/2390076 .Accessed: 02/09/2014 12:41Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp .JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact support@jstor.org. .British Ecological Society is collaborating with JSTOR to digitize, preserve and extend access to FunctionalEcology.http://www.jstor.org This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/action/showPublisher?publisherCode=britecohttp://www.jstor.org/stable/2390076?origin=JSTOR-pdfhttp://www.jstor.org/page/info/about/policies/terms.jsphttp://www.jstor.org/page/info/about/policies/terms.jspFunctional Ecology 1994 8, 509-517 509 The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon L. D. HARDER and R. M. R. BARCLAY Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada 72N 1N4 Summary 1. Given the diminishing returns associated with animal pollination, floral mechan- isms that restrict pollen removal by individual pollinators and encourage transport on many pollinators generally promote a plant's cumulative success in pollen dispersal. Effective mechanisms for dispensing pollen should allow facultative adjustment of removal in response to the prevailing frequency of visits to a plant. 2. We investigated whether the poricidal anthers of Dodecatheon conjugens, a buzz-pollinated species, function as dispensing mechanisms by (a) comparing pollen removal in response to buzz frequencies that pollen-collecting bumble-bees (Bombus spp.) produce (510a L. D. Harder & b R. M. R. Barclay Fig. 1. Illustration of (a) Dodecatheon conjugens (scale bar = 1 cm) and (b) the position adopted by pollen-collec- ting bees during flower vibration (Bombus bifarius queen illustrated: scale bar = 05 cm). in general, and solanoid floral morphology, in par- ticular, represent evolutionary compromises that balance the attractive function of pollen against its primary role as the vehicle of male germ cells. Regardless of the pollinator attractant, many aspects of animal pollination limit successful pollen dispersal. In general, although increased pollen removal during individual pollinator visits enhances pollen dispersal per pollinator, it invokes mechan- isms that reduce the average probability of successful pollen dispersal per grain so that total dispersal suffers [e.g. pollinator grooming (details below), pollen layering, limited capacity to carry pollen; Harder & Thomson 1989]. This negative relation between pollen removal and total dispersal (dim- inishing returns) can be counteracted by restriction of pollen removal by individual pollinators to the extent allowed by pollinator availability (Lloyd 1984; Harder & Thomson 1989). Plants possess two general classes of floral mechanisms which may restrict pollen removal: packaging mechanisms, which limit the proportion of a plant's total pollen production that is exposed to pollinators at any time; and dispensing mechanisms, which govern the proportion of exposed pollen that a pollinator removes (Harder & Thomson 1989). Dispensing mechanisms may be particularly effective means of governing pollen removal because they allow adjustment of removal to the ambient frequency of pollinator visits (Harder & Wilson 1994). Although various floral features appear to be dispensing mechanisms (e.g. poricidal anthers, secondary pollen presentation, nectar pro- duction; Harder & Thomson 1989), few studies have assessed the ability of such features to limit pollen removal (see Harder 1990a; Harder & Wilson 1994; LeBuhn & Anderson, in press). Plants that bees visit solely to collect pollen should be particularly susceptible to diminishing returns because bees groom frequently and intensively (Michener, Winston & Jander 1978; Buchmann & Cane 1989; Harder 1990b). Bees detect differences in the amount of pollen they remove from flowers (Cane & Payne 1988; Buchmann & Cane 1989; Harder 1990b) and respond to such differences by altering grooming, either during the visit (Buchmann & Cane 1989) or while flying to the next flower (Harder 1990b). As a result, removal of few pollen grains stimulates little or no grooming, whereas removal of many grains prompts thorough grooming, thereby reducing the proportion of removed grains that reach stigmas. Such persistent exposure to diminishing returns should foster the evolution of dispensing mechanisms that limit pollen removal by pollen-collecting bees. Poricidal anthers could be one means of restricting pollen removal from nectarless flowers. In contrast to typical longitudinally dehiscent anthers, poricidal anthers allow escape of pollen through an apical slit or pore (Buchmann 1983). Because of this morpho- logy, incidental contact between pollen and pollina- tor is not possible and removal of pollen from such anthers requires active vibration. It is this require- ment for agitation by pollen-collecting bees which enables the evolution of restricted pollen removal. In particular, if poricidal anthers are dispensing mechanisms, then the vibration frequencies used by pollen-collecting bees should expel less pollen than higher frequencies, which bees cannot produce. A more specific statement of this hypothesis requires identification of the vibration frequencies experienced by buzzed flowers. Pollen removal is primarily a response to direct transmission of the vibrations produced by rapid contractions of the flight muscles: '. . the acoustical component of the buzzing behavior is really just a by-product of the actual interaction, and doesn't have much biological meaning' (Buchmann 1983, p.76; see also King 1993). Consequently, although buzzes include many high-frequency harmonics (Buchmann, Jones & Colin 1977), the fundamental frequency is of prime concern from the flower's perspective. In general, large-bodied bees buzz with a fundamental frequency of about 300Hz (Macior 1968; Buchmann et al. 1977; Corbet, Chapman & Saville 1988) and seldom above 400 Hz. Consequently, our hypothesis concerning the role of poricidal anthers as dispensing mechanisms predicts that vibrations less than or equal to 400Hz will expel less pollen than faster vibrations with equivalent energy. The specification that the fre- quencies considered involve equivalent energy recognizes constraints on energy output by bees. Our purpose in this study was to determine whether poricidal anthers act as a dispensing This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp511 mechanism and specifically whether the frequencies Pollen dispensing used by buzz-pollinating bees remove less pollen than by poricidal higher-frequency vibrations with the same energy anthers input. To assess this hypothesis we considered four aspects of the pollination biology of Dodecatheon conjugens Greene (Primulaceae) and its bumble-bee (Bombus) pollinators. First, we quantified pollen removal from virgin flowers by freely foraging bumble-bees to determine whether removal is restricted. Second, we measured the vibration fre- quencies by pollen-collecting bees to verify that D. conjugens flowers do not naturally experience vibra- tions in excess of 400Hz. Third, we mechanically vibrated D. conjugens flowers over a range of fre- quencies that included the frequencies produced by bees to test the prediction that bees could remove more pollen if they could buzz at higher frequencies. Fourth, because an efficient dispensing mechanism should adjust pollen removal to pollinator abun- dance, we measured removal from virgin flowers of different ages, which had waited different periods for their first visit. Because we could not measure the amplitude of vibrations produced by pollen-collec- ting bees, we also used mechanical vibrations to quantify the effects of amplitude on pollen removal. Finally, we comment on (1) features of poricidal anthers that could promote the convergent evolution of solanoid flowers and (2) the general dissimilarity in floral morphology between bee-pollinated species with poricidal anthers and nectar-producing species with longitudinally dehiscing anthers. Materials and methods STUDY SPECIES AND SITE Dodecatheon conjugens (shooting star) is a herbace- ous perennial that produces one to six pendant flowers on a short leafless scape (see Fig. la). The 6*5 mm long anthers project from the flower in a cone which is fully exposed to the pollinator as a result of reflection of the pink petals. The anthers dehisce introrsely by an apical slit which gradually elongates during a flower's 3 days of blooming. Flowers pro- duce an average?SE of 1270700?30440 pollen grains with a mean diameter of 12-6 ? 004 im (n = 51), but they do not produce nectar. We studied D. conjugens at Sibbald Flat, Alberta (51002'N; 114'49'W), where it is visited by at least nine species of bumble-bees (Bombus spp.). The late-May flowering period typically coincides with the emergence of workers of early-nesting species, so that the pollinating fauna includes a mixture of queens and small workers, although queens pre- dominate. Aspects of this study that considered bee characteristics primarily involved the most common visitors to D. conjugens, B. bifarius Cresson (mean?+SE mass of queens = 0-33?+0-01g, n =24), B. melanopygus Nylander (0-41 ? 0-01 g, n = 9) and B. occidentalis Greene (0-55 ? 0-02g, n = 13). RECORDING AND ANALYSIS OF BEE VIBRATIONS We recorded the sounds produced by bumble-bees as they collected pollen from D. conjugens flowers in the field. During recording we held an Electro-Voice 635A Omni-direct microphone and a broad-band capacitance microphone (Simmons et al. 1979) within 0-5 m of the bee. Detected sounds were recorded by a Racal Store 4DS instrumentation tape recorder oper- ated at 38cms-1 and later analysed with SIGNAL Software (Engineering Design, Belmont, Massa- chusetts, USA) to measure buzz duration and the frequency of thoracic vibration as indicated by the fundamental frequency. Some recordings were also analysed with a Kay Digital Sonograph (model 5800) to examine the harmonic structure of the sounds associated with flower vibration. POLLEN REMOVAL Flowers used in all experiments were covered with fine-mesh bags until anthesis to ensure that they contained their full complement of pollen. Immedi- ately before measuring removal, we picked a scape with one open flower and placed it in a water-filled vial. Pollen collected from flowers (see below) was preserved in 70% ethanol in individually marked vials until it could be counted. Prior to counting, all samples were sonicated for 1 min to disperse pollen and free it from the anthers if they had been included. Anthers in such samples were then inspected under a dissecting microscope and any pollen that they still contained was dislodged with a pin and returned to the sample. We used a Particle Data Elzone 180XY particle counter to count and measure the diameter of pollen grains in approximately 10% of each sample (see Harder 1990a for details). Removal by bees Because we could not directly measure pollen removal by freely foraging bees, we quantified the number of grains remaining in flowers after single visits and included anther length in the statistical analysis (ANCOVA) as a measure of initial pollen availability. Scapes with virgin flowers were placed in a water-filled vial and held near a bee as it foraged within the D. conjugens population. If the bee moved onto the experimental flower we recorded the dur- ation of the visit on a tape recorder and noted the species and caste of the bee. After the visit, we collected the anthers and their remaining pollen. This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp512 During pollen counting we measured the maximum L. D. Harder & length of one anther sac from each sample under a R. M. R. Barclay dissecting microscope (60x). This experiment involved virgin flowers in their first, second or third day of flowering to determine whether pollen removal varied with flower age. Mechanical removal To quantify the effectiveness of different vibration frequencies and amplitudes in removing pollen from D. conjugens flowers, we mechanically 'buzzed' flowers. Vibrations of known frequency and ampli- tude were produced by a Cambridge Technology Inc. model 350 transducer connected to a Cambridge Technology model 300 Dual Mode Servo. The fre- quency and amplitude of the 2cm long transducer arm were controlled by a custom-made, pure-tone sine-wave generator (University of Calgary, Techni- cal Services). Prior to each experiment, we determined the gain setting on the sine-wave genera- tor required to produce a given displacement (ampli- tude) of the end of transducer arm. During experiments, the frequency and gain from the generator were monitored on a Tektronix 2220 Digital storage oscilloscope. Output from the sine- wave generator was gated to produce 1 s buzzes. During an experimental trial we removed a flower from its scape and held it vertically against the horizontal transducer arm. The flower then received a is buzz of the specified frequency and amplitude (randomly assigned), which expelled some pollen into a micro-centrifuge tube positioned just below the tip of the anther cone. After the buzz, the anthers were cut from the flower into a second micro-centri- fuge tube, so that we collected both the removed pollen and that remaining in the flower. Three experiments involved mechanical vibration. The first experiment assessed the effect of vibration frequency on pollen removal for a fixed input energy. Frequencies from 100 to 100O Hz in 50Hz increments were involved, with four first-day flowers experienc- ing each frequency. Vibration amplitude was adjus- ted to equalize energy input for each frequency, based on energy equalling the product of amplitude and frequency (the 300 Hz treatment involved a 0*5mm amplitude). The second experiment evalu- ated the effect of amplitude (0.25mm, 0*5mm and 0*75 mm) on pollen removal from first-day flowers at 300 and 600Hz. The final experiment considered whether pollen removal varies with flower age and involved flowers in their first or second day of flowering. Frequencies from 100 to 1000Hz in lOOHz increments were involved in this experiment, with a fixed amplitude of 0-5mm. The frequency aspect of this experiment is not relevant to this study because it confounds increased frequency with increased input energy. Results CHARACTERISTICS OF BEE-GENERATED VIBRATIONS While visiting a Dodecatheon flower a bumble-bee grasps the base of the anther cone with her mandibles and curls her body under the anther cone in an inverted position (Fig. lb: for photographs see Macior 1964). Repeated contraction of the bee's indirect flight muscles produces vibrations that are transmitted to the flower directly through the mandi- ble-anther contact and probably to a lesser extent through the legs. This vibration expels pollen from the anthers onto the ventral surfaces of the bee's thorax and abdomen and produces a buzz which is audible from several metres (for more details see Macior 1964,1968; Buchmann etal. 1977; Buchmann 1983; Corbet etal. 1988). Most of the pollen removed in this manner is groomed into the corbiculae as the bee flies between flowers. The duration of individual visits to virgin flowers depended on the bee species involved (F2,34 = 4-90, P513 Table 1. Mean ? SE characteristics of different types of buzzes used by bumble-bees to remove pollen from Dodecatheon Pollen dispensing conjugens flowers. For each characteristic, means followed by different superscript letters differ significantly (P< 0.05) as by poricidal indicated by Tukey's multiple comparison tests anthers Constant Variable Multiple Single Characteristic amplitude amplitude pulses pulse Per cent occurrence 4-6 30-0 44.3 21-1 Duration* (s) 0.46a 0.56a 0.53a 0-16b 0-42-0-52 0-52-0-61 0 48-0 59 0 15-0-18 Frequency (Hz) 315 ? 5.2a 316 ?4.8a 317 + 4.3a 327 ? 4.9b No. of bees 20 30 26 28 * Based on log-transformed data, hence the asymmetric standard errors. interactions). Buzzes produced during pollen collec- tion involved vibrations that were about twice as rapid as wing-beat frequency during flight (mean ? SE = 177 ? 3*5 Hz, n = 29). POLLEN REMOVAL BY FREE-FORAGING BEES The amount of pollen that bees removed from virgin shooting-star flowers depended on floral character- istics, but did not differ among bee species (F2,33= 2*52, P> 0.05), regardless of whether statis- tical analysis incorporated visit duration as a covari- ate. Not surprisingly, bees left more pollen in flowers with longer anthers (F1,33= 5*64, P< 0.025), which generally produce more pollen. Pollen removal gen- erally increased with flower age (F2,33= 11*13, P< 0.001), with removal from third-day flowers significantly exceeding removal from first-day flowers (see Fig. 2). POLLEN REMOVAL IN RESPONSE TO MECHANICAL VIBRATION Frequency effects Our assessment of the effects of frequency on pollen removal strongly supports the hypothesis that vibra- tions within the range produced by bees expel less pollen than faster vibrations with equivalent energy (Fig. 3). Frequencies from 100 to 400Hz removed significantly less pollen than did frequencies from 450 to 1000Hz (F1,56= 16*52, P0.75). Over all frequencies, the proportion of pollen removed generally declined with increasing pollen size (F1,56= 16X00, P 0*7 -I 0 11 4-4~~~~~~~~~~~4 05- I 016 .0 0-3- 12 3 Flower age (days) Fig. 2. Relation of pollen removal (mean ? SE) from virgin Dodecatheon conjugens flowers by bumble-bees to flower age. The proportion removed was calculated from the number of grains remaining after a visit, adjusted for between-flower differences in anther length, and average pollen production. Numbers indicate sample sizes. This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp514 l l L. D. Harder & 0.4 0 4 R. M. R. Barclay > 0 0- 0 00 loo 200 300 400 soo 600 700 800 9oo 1000 40 Frequency (Hz) Fig. 3. Relation of pollen removal from virgin Dodecatheon conjugens flowers to vibration frequency during 1 s of mechanical vibration. (a) Mean ? SE removal at the specific frequency applied to each flower (n = 4 for each frequency); (b) contrasts the results for vibrations - 400 Hz. Effects offlower age Averaged over frequencies, flower age significantly affected pollen removal (F1,102 = 6 81, P< 0.025), as vibration removed a mean of 23-1% of the pollen from first-day flowers (lower SE = 20X6%, upper SE = 25X7%, n = 91, based on arcsin-transformed data) and 40X8% from second-day flowers (lower SE=36X0%, upper SE=45X7%, n=62). The increased removal from older flowers occurred con- sistently over all frequencies as age and frequency did not interact significantly (F9,102 = 0 99, P > 0.4). Discussion PORICIDAL ANTHERS AS DISPENSING MECHANISMS For animal-pollinated plants, effective control of pollen removal involves balancing restricted removal per pollinator, which ameliorates the impact of diminishing returns associated with pollen dispersal, against increased removal to provide all pollen an opportunity to reach stigmas (Harder & Thomson 1989; Harder & Wilson 1994). Selection of floral characters can produce this balance in two ways. First, the long-term average abundance of pollinators sets the fundamental extent to which pollen removal is best restricted. However, variation in pollinator abundance, between and within flowering seasons and among sites, will generally reduce the effectiveness of the average level of restricted removal in promoting successful pollen dispersal. Hence, the second outcome of selection that modifies pollen removal would be refinement of mechanisms that allow facultative adjustment of removal to the ambient pollinator abundance for each plant (see Harder & Wilson 1994). The characteristics of pollen removal from flowers of Dodecatheon conjugens indicate that the anthers of these flowers may be responses to such selection. First, these anthers restrict pollen removal, as illustrated by greater removal in response to vibra- tion frequencies exceeding those produced by pollen- collecting bumble-bees (Fig. 3). Second, pollen removal from virgin flowers increased with flower age during both bee visits (Fig. 2) and mechanical vibration. Because the period preceding a flower's first visit generally varies inversely with pollinator abundance, such age-related changes in removal result in greater removal per pollinator when individ- ual plants experience few visits. Hence the poricidal anthers of D. conjugens exhibit the necessary char- acteristics of a dispensing mechanism: they restrict pollen removal while allowing facultative adjustment of removal to pollinator abundance. Whether this 06- I I 10 0 - - 04 - 032 I O I 025 050 075 Amplitude (mm) Fig. 4. Relation of pollen removal from virgin Dodecatheon conjugens flowers to vibration amplitude during 1 s of mechanical vibration at 300 (solid line) and 600Hz (dashed line). This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp515 mechanism generally optimizes pollen dispersal Pollen dispensing remains to be demonstrated.. by poricidal To assess the applicability of our results from anthers Dodecatheon for other species with similar flower structure, and buzz-pollinated species in general, we consider two lines of evidence. First, we examine the limited data on pollen removal from other buzz-polli- nated species to identify characteristics that might be common to plants with poricidal anthers that are pollinated by large-bodied bees. Second, we discuss the mechanism by which bees produce buzzes, which necessarily determines the characteristics of the vibrations experienced by flowers during pollinator visits. Of particular interest is whether bees are capable of producing the higher frequencies that remove more pollen from buzz-pollinated flowers. Pollen removal from other buzz-pollinated species The limited data on pollen removal from other buzz-pollinated species indicate restriction of removal equivalent to that observed for Dodecatheon for a species with poricidal anthers (Snow & Roubik 1987), but greater removal from a species with longitudinally dehiscing anthers (Harder 1990a). Snow & Roubik (1987) measured pollen removal from the poricidal anthers of Cassia reticulata (Fabaceae) by three species of large-bodied bees (similar in size to the B. bifarius queens involved in our study) and a smaller halictid. The large bees removed about 15-25% of the pollen from virgin flowers and the smaller halictid removed negligible amounts. In contrast, Harder (1990a) found that worker bumble-bees removed a median of 43-5% of the pollen from virgin Pedicularis contorta (Scrophu- lariaceae) flowers. The floral morphology of this buzz-pollinated species isolates pollinators from direct contact with the anthers; however, it appears that this means of controlling pollen removal is less effective than poricidal anthers. Indeed, the propor- tion of pollen removed from this species was only slightly lower than that from a congener (P. brac- teosa) in which the nectar-collecting pollinators directly contact the anthers (Harder 1990a). Our study (see Fig. 3) corroborates the results of two previous studies that examined the effect of vibration frequency on pollen removal and found most effective removal above 400Hz. Buchmann et al. (1977) vibrated Solanum douglasii and S. xanti flowers (Solanaceae) with tuning forks of different pitches (details of pitches tested were not provided) and found that the 512Hz tuning fork expelled the most pollen. Additionally, they concluded that pollen was released gradually throughout the day, indicating the action of a dispensing mechanism. Corbet et at. (1988) microscopically viewed individ- ual kiwi fruit anthers (Actinidia deliciosa: Actini- diaceae) while they were vibrated at frequencies from 156 to 1076 Hz. Pollen within the anthers became especially dynamic at specific frequencies, with the greatest activity at about 500Hz. The mechanics of buzzing Buzzing involves operation of the bee's flight machinery, except that the wings are folded and move very little. Although the production of buzzes has received little direct analysis (see Esch & Goller 1991), extensive investigations of insect flight (reviewed by Pringle 1957, 1973) provide the neces- sary understanding of the processes involved. Of particular interest are mechanisms that control vibra- tion frequency, as the relevance of the control of buzzing for pollen dispensing depends on whether bees buzz at the highest possible frequency. A bee's 'thorax' (actually the fused thorax and first abdominal segment) is not a rigid sclerotized box; rather the large dorsal plate (scutum) can move relative to the remainder of the thorax. The two pairs of major flight muscles run from the scutum to the ventral (dorsoventral muscles) and posterior (dorsal longitudinal muscles) aspects of the thorax, making no direct connection with the wings. During flight, alternate contraction of these muscles alters the shape of the thorax, deforming the articulation of the wings with the thorax and causing the wings to flap. This indirect relation between the wings and the muscles that power flight enables these muscles to vibrate the thorax without inducing wing movement when the wings are folded. Unlike most muscles, the flight muscles of bees and other fast-flying insects are asynchronously con- trolled by the nervous system. Although nerve impulses induce contraction, stretching also activates these muscles to contract. Because of the arrange- ment of the flight muscles within the thorax, contrac- tion of one pair stretches the other pair, thereby stimulating the latter's contraction. This feedback allows a single nerve impulse to each muscle to induce a series of muscular contractions. Such asynchronous nervous control enables very frequent contraction, so that frequency is probably limited by the molecular mechanisms of contraction, rather than the speed of nervous activation (Pringle 1973). During flight and buzzing, rhythmic mechanical activity results from asynchronous muscle activation and intrinsic resonance of the flight machinery. The mechanical resonance depends on the elasticity of the skeleton and muscles and the inertia of the wings. During buzzing the system is largely freed from the inertial forces of the wings, because they are folded, so that the thorax vibrates about twice as fast during buzzing as during flight (Macior 1968; Buchmann et at. 1977; Corbet et at. 1988; this study). Hence, the thorax probably vibrates near its maximum fre- quency during buzzing, so that bees cannot produce higher frequencies even though such frequencies would liberate more pollen. This conclusion is consis- This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp516 tent with Corbet et al.'s (1988) observation that buzz L. D. Harder & frequency increases with ambient temperature, as R. M. R. Barclay increased temperature should cause a corresponding increase in maximal muscle efficiency. 'Tuning' the dispensing mechanism The preceding discussion reveals two points of speci- fic interest: (1) bees probably buzz at the highest frequencies they can produce, and (2) the available evidence for four plant species from three families (Buchmann et al. 1977; Corbet et al. 1988; this study, Fig. 3) indicates a peak sensitivity for poricidal anthers at around 500 Hz. This frequency is con- siderably higher than the frequencies produced by the large-bodied bees that pollinate these species, so that the anthers of buzz-pollinated plants seem to be 'tuned' out of the frequencies used by their pollina- tors. The associated restriction of pollen removal should help counteract particularly severe diminish- ing returns that are likely associated with reliance on pollen-collecting bees as pollen vectors. BUZZ POLLINATION AND THE EVOLUTION OF FLOWER FORM Harder & Barrett (1993) proposed that exserted stamens were relatively uncommon among species with flaring, tubular corollas and longitudinally dehi- scing anthers because they allow greater pollen removal than more included positions and are not consistently contacted by small pollinators. In con- trast, plants such as Dodecatheon that rely on pollen as the primary pollinator attractant typically have strongly exserted stamens (Vogel 1978; Buchmann 1983). Given that anthers contain the object of a pollen-collecting bee's search, it is not surprising that they also serve as an attractant signal, a function best satisfied if the anthers are exposed and obvious (Vogel 1978). Hence plants that offer pollen as the sole reward to pollinators may generally confront a conflict between the benefits of exserted anthers as a signal of reward availability and costs associated with a reduced ability to control pollen removal. Poricidal anthers likely represent an evolutionary resolution of this conflict because they can be openly displayed and yet can act as a dispensing mechanism. Poricidal anthers undoubtedly enable evolution of solanoid flowers as effective mechanisms for dispers- ing pollen on pollen-collecting bees. Apical dehis- cence of poricidal anthers facilitates their aggregation into a cone, thereby providing an effective means of directing pollen onto specific regions of the pollinator's body. If a flower with such an anther cone directs the cone downwards, then a buzzing pollinator that secures itself by grasping the base of the cone with its mandibles is obliged to curl its body under the cone's tip to catch the expelled pollen. This position necessarily results in pollen being deposited either between the bases of the bee's legs or between the thorax and abdomen-positions that are poorly cleaned during inflight grooming (Buchmann 1983). Given this pattern of pollen deposition on the pollinator, pollen receipt by recipi- ent flowers is enhanced if the stigma protrudes from the tip of the anther cone. Hence, the male and female organs of solanoid flowers probably function as a unit for increasing the precision of pollen placement and removal, despite the pollinator's motivation to maximize pollen collection. As a result, the perianth is not needed to constrain the pollinator's posture, as it is in many nectar-producing plants. Indeed, reflection of the petals away from the anthers probably allows bees to adopt a stereotypical position during pollen collection, thereby reinforcing the positioning function of the anther cone. This functional interpretation of solanoid flowers implies that the evolution of poricidal anthers preci- pitates further changes in floral form. Although plants with diverse floral morphologies possess pori- cidal anthers (Buchmann 1983), the independent evolution of solanoid flowers in unrelated families indicates that this particular morphology represents one adaptive peak for buzz-pollinated plants. Acknowledgements We gratefully acknowledge contributions to this study by the following individuals: M. B. Vander Meulen assisted in the field, C. E. Koehler analysed the sound recordings, S. A. Rasheed and M. J. Von- hof counted pollen, H. C. Proctor drew Fig. 1, D. J. I. Fry and W. G. Wilson clarified physical concepts, J. L. Wilkens and R. L. Walker provided technical advice and willingly loaned necessary equipment, and S. C. H. Barrett and S. A. Corbet commented on the manuscript. This study was supported financially by the Natural Sciences and Engineering Research Council of Canada. References Buchmann, S.L. (1983) Buzz pollination in angiosperms. Handbook of Experimental Pollination Biology (eds C.E. Jones & J.R. Little), pp. 73-113. Van Nostrand Reinhold, New York. Buchmann, S.L. & Cane, J.H. (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia, 81, 289-294. Buchmann, S.L., Jones, C.E. & Colin, L.J. (1977) Vibratile pollination of Solanum douglasii and S. xanti (Sola- naceae) in southern California. Wasmann Journal of Biology, 35, 1-25. Cane, J.H. & Payne, J.A. (1988) Foraging ecology of the bee Habropoda laboriosa (Hymenoptera: Anthophori- dae), an oligolege of blueberries (Ericaceae: Vaccinium) in the southeastern United States. Annals of the Entomo- logical Society of America, 81, 419-427. This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jsp517 Pollen dispensing by poricidal anthers Corbet, S.A., Chapman, H. & Saville, N. (1988) Vibratory pollen collection and flower form: bumble-bees on Actinidia, Symphytum, Borago and Polygonatum. Func- tional Ecology, 2, 147-155. Esch, H. & Goller, F. (1991) Neural control of fibrillar muscles in bees during shivering and flight. Journal of Experimental Biology, 159, 419-431. Faegri, K. (1986) The solanoid flower. Transactions of the Botanical Society of Edinburgh, 150th Anniversary Supplement (eds I. J. Alexander & N. M. Gregory), 51-59. Botantical Society of Edinburgh, Edinburgh. Harder, L.D. (1990a) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology, 71, 1110- 1125. Harder, L.D. (1990b) Behavioral responses by bumble bees to variation in pollen availability. Oecologia, 85, 41-47. Harder, L.D. & Barrett, S.C.H. (1993) Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology, 74, 1059- 1072. Harder, L.D. & Thomson, J.D. (1989) Evolutionary options for maximizing pollen dispersal of animal-polli- nated plants. American Naturalist, 133, 323-344. Harder, L.D. & Wilson, W.G. (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evolu- tionary Ecology, in press. King, M.J. (1993) Buzz foraging mechanism of bumble bees. Journal of Apicultural Research, 32, 41-49. Le Buhn, G. & Anderson, G. I. (in press) Anther tripping and pollen dispensing in Berberis thumbergii. American Midland Naturalist. Lloyd, D.G. (1984) Gender allocations in outcrossing cosexual plants. Perspectives on Plant Population Ecology (eds R. Dirzo & J. Sarukhdn), pp. 277-300. Sinauer, Sunderland, Massachusetts. Macior, L.W. (1964) An experimental study of the floral ecology of Dodecatheon meadia. American Journal of Botany, 51, 96-108. Macior, L.W. (1968) Pollination adaptation in Pedicularis groenlandica. American Journal of Botany, 55, 927-932. Michener, C.D., Winston, M.L. & Jander, R. (1978) Pollen manipulation and related activities and structures in bees of the family Apidae. University of Kansas Science Bulletin, 51, 575-601. Pringle, J.W.S. (1957) Insect Flight. Cambridge University Press, Cambridge. Pringle, J.W.S. (1973) Locomotion: flight. The Physiology of the Insecta, 2nd edn, vol. III (ed. M. Rockstein), pp. 433-476. Academic Press, New York. Simmons, J.A., Fenton, M.B., Ferguson, W.R., Jutting, M. & Palin, J. (1979) Apparatus for research on animal ultrasonic signals. Miscellaneous Publication, Royal Ontario Museum, Toronto, Ontario. Snow, A.A. & Roubik, D.W. (1987) Pollen deposition and removal by bees visiting two tree species in Panama. Biotropica, 19, 57-63. Vogel, S. (1978) Evolutionary shifts from reward to decep- tion in pollen flowers. The Pollination of Flowers by Insects (ed. A. J. Richards), pp. 89-96, Sixth Symposium of the Linnean Society of London. Academic Press, New York. Received 19 September 1993; revised 3 December 1993; accepted 14 December 1993 This content downloaded from 2.100.174.124 on Tue, 2 Sep 2014 12:41:38 PMAll use subject to JSTOR Terms and Conditionshttp://www.jstor.org/page/info/about/policies/terms.jspArticle Contentsp. 509p. 510p. 511p. 512p. 513p. 514p. 515p. 516p. 517Issue Table of ContentsFunctional Ecology, Vol. 8, No. 4 (Aug., 1994), pp. 427-550Front Matter [pp. ]Ecological Energetics and Food Acquisition in Dense Menorcan Islet Populations of the Lizard Podarcis lilfordi [pp. 427-434]Variation and Plasticity of Biomass Allocation in Daphnia [pp. 435-440]Thermoregulation During Summer Activity in Mojave Desert Dragonflies (Odonata: Anisoptera) [pp. 441-449]Scaling of Wingbeat and Echolocation Pulse Emission Rates in Bats: Why are Aerial Insectivorous Bats so Small? [pp. 450-457]Size-Dependent Predation by Dugesia lugubris (Turbellaria) on Physa acuta (Gastropoda): Experiments and Model [pp. 458-463]Mycophagy and Spore Dispersal by a Rat-Kangaroo: Consumption of Ectomycorrhizal Taxa in Relation to their Abundance [pp. 464-468]The Genetical Ecology of Nestling Growth in the Great Tit. Environmental Influences on the Expression of Genetic Variances During Growth [pp. 469-476]Ontogenetic Shifts in How Grasshoppers Interact with Landscape Structure: An Analysis of Movement Patterns [pp. 477-485]How Rearing Temperature Affects Optimal Adult Size in Ectotherms [pp. 486-493]Reactions of the Mountain Birch to Bud Removal: Effects of Severity and Timing, and Implications for Herbivores [pp. 494-501]Growth, Biomass Allocation and Foliar Nutrient Contents of Two Eucalyptus Species of the WetDry Tropics of Australia Grown Under CO2 Enrichment[pp. 502-508]The Functional Significance of Poricidal Anthers and Buzz Pollination: Controlled Pollen Removal From Dodecatheon [pp. 509-517]The Dependence of Herbivory on Growth Rate in Natural Plant Communities [pp. 518-525]Effects of Flower Number and Position on Self-Fertilization in Experimental Populations of Eichhornia paniculata (Pontederiaceae) [pp. 526-535]Evidence that Heavy Grazing May Promote the Germination of Lolium multiflorum Seeds via Phytochrome-Mediated Perception of High Red/Far-Red Ratios [pp. 536-542]Plant Allocation, Growth Rate and Successional Status [pp. 543-550]Back Matter [pp. ]

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