Generalist bees pollinate red-flowered Penstemon eatonii: duality in the hummingbird pollination syndrome.
To varying degrees, all pollinators use just a subset of the floral diversity presented by plant communities. Pollination syndromes have been used to conveniently classify associations between kinds of pollinator and correlated suites of floral traits (Faegri and van der Pijl, 1979; Wilson et al., 2004). The hummingbird floral syndrome is especially striking. In western North America, species representing at least 15 eudicot families have evolutionarily converged on a narrowly defined suite of floral traits adapted for hummingbird attraction, foraging and pollination (Grant and Grant, 1968), including 10 or more lineages within Penstemon (Wilson et al., 2007). The implicated traits include: a red, deep, narrowly tubular corolla; a lack of evident scent; absence of any conspicuous "landing platform"; and, anthers/stigmas exserted just enough to daub and pick up pollen on the hovering hummingbird's facial feathers as it imbibes nectar (Grant and Grant, 1968; Wilson et al., 2004). This suite of floral traits has been shown to favor hummingbird foraging and their efficient acquisition, export and later deposition of pollen (Castellanos et al., 2003, 2004). By that measure of male fitness, limited experiments indicated that nectaring bumblebees were inferior to hummingbirds in pollinating one species, P. barbatus (Castellanos et al., 2003). However, can bees contribute substantially to maternal fitness (e.g., seed production) by any of these archetypal hummingbird flowers?
We report here that scarlet tubular-flowered Penstemon eatonii Gray (Plantaginaceae), when farmed for seed in the western U.S., generated massive seed yields for multiple years in the absence of hummingbirds. The flowers in this population were solely visited and effectively pollinated by foraging generalist bees.
The native seed farm is near Worland, Wyoming (44[degrees]57'N, 117[degrees]58'W) in an agricultural strip along the Bighorn River. The surrounding sagebrush-steppe habitat supports Broad- tailed, Calliope, and Rufous hummingbirds (USGS Bird Checklists of the United States). Since 2000, the short-lived native perennial P. eatonii has been continuously grown in monoculture on a 1.3 ha field (Fig. 1). The original seed came from the wild near American Fork, Utah. Neighboring fields (each 0.2-5 ha) included coflowering P. angustifolia, Prunus besseyii (Rosaceae), and Hedysamm boreale (Fabaceae), all wildflowers visited abundantly by honeybees and native bees. Any hummingbirds were noted since 2003.
Bees were surveyed at blooming P. eatonii during warm calm sunny weather on 9 Jun. 2008. Bees at flowers were identified and counted during a walking scan census along three 30 m lengths of row. After 5-6 h of bee activity, 14 fresh P. eatonii flowers were randomly taken along three 10 m lengths of row, one per plant. Flowers were carefully emasculated and refrigerated. The next day, their stigmatic pollen loads were counted while viewing intact stigmas microscopically. Seed of P. eatonii was mechanically harvested, cleaned, and weighed late each summer (2002-2008).
More insights came from P. eatonii grown in a suburban garden in Logan, Utah where plants could be daily observed and manipulated. Nectar that had accumulated in eight virgin flowers was withdrawn at 1100 h using a 5 pi microcapillary pipette. Volume was calculated from the pipette's measured height of nectar. Sugar concentrations were measured using a hand-held refractometer (Bellingham and Stanley Ltd., Tunbridge Wells, U.K.). Ovules were counted for one of the pair of locules of 10 dissected fresh flowers. Potentially UV-reflective floral surfaces were microscopically examined while using a portable 365 nm LED UV lamp (Nichia Corp., Tokushima, Japan). Anther morphology was viewed microscopically using herbarium material cleared in ethanol. Lastly, during 5 y at the Logan garden, the foraging rounds of the Penstemon specialists (=oligoleges), Osmia brevis (Megachilidae), and Pseudomasaris vespoides (Masaridae) were observed at a mix of penstemons that included P. eatonii Quantitative data are summarized in the results as the mean 1 SD.
Only bees visited flowers of P. eatonii on the Wyoming farm since 2002. On 9 Jun. 2008, only honey bees were seen at P. eatonii flowers (28-29 bees per 30 m of row), which was generally true during bloom that year. From 2002-2008, no hummingbirds were seen or heard during daily casual observation of farmed P. eatonii, although they are in nearby Worland. In 2008, honey bees came from 40 hives placed 950 m distant from the P. eatonii field. In the six preceding years, honey bee hives were absent. In 2004, numerous females of the solitary bee Anthophora ursina foraged for pollen but not nectar at P. eatonii. This bee was seen at P. eatonii flowers in the Logan garden but not at concurrently blooming blue-flowered P. cyananthus, P. speciosus, or P. stridus. These latter species were daily visited by Penstemon specialists (O. brevis and P. vespoides) seeking pollen and nectar. Neither specialist visited adjacent P. eatonii.
All honey bees landed upright and faced into the corollar opening of a P. eatonii flower (Fig. 1). They may have been attracted at close range by the bright UV-reflectance of the dentate rims of the anther sutures, which are visible from the corollar opening. Most foragers inserted their heads fully into the corolla, proboscis extended, to drink from the basal nectary. By midday, new virgin flowers had 4.4 1.6 [micro]l of dilute nectar (20-28% w/w concentration). No robbery holes were seen. At flowers of P. eatonii, 11 of 20 surveyed honey bee foragers carried corbicular pellets of pale pollen resembling that of P. eatonii. Honey bees periodically groomed and packed loose pale pollen while foraging at P. eatonii. Extrapolating these bee surveys to the 1.3 ha field on 9 Jun., 10,500 honey bees foraged at P. eatonii in the 11,200 m of farmed rows.
Stigmas from freely visited new flowers of P. eatonii bore only tiny pale tricolpate grains typical of Penstemon. After 5-6 h, visiting honey bees had cumulatively deposited 52 30 pollen grains on each of 14 stigmas (range 10-104 grains). Ten locules had 46 3 ovules, or 92 ovules per flower.
The field of P. eatonii yielded 123-312 kg/ha/yr of dean seed each year (differences mostly due to weather). The larger value approaches the maximum predicted seed yield for cultivated P. eatonii (Stevens et al., 1996). Harvested seed yield in 2008 was 2 g/plant, or about 1400 seeds, given that there are 690,000 seeds/kg (Stevens et al., 1996), or 15 floral-equivalents if all ovules are fertilized. Pollination solely by bees thus yielded up to 1/4 billion seeds of P. eatonii annually from the Worland seed field.
The more obvious floral traits of P. eatonii dearly fit the hummingbird syndrome, but P. eatonii had massive seed yields at the Worland farm though pollinated solely by generalist bees. Multivariate analyses of floral traits by Wilson et al. (2004) grouped P. eatonii with other red tubular-flowered penstemons visited by hummingbirds. The generous volumes of dilute nectar that we measured match other red-flowered penstemons (Wilson et al., 2007). Nonetheless, polylectic (generalist) bees were key pollinators of P. eatonii in our study, as shown both by stigmatic pollen loads and the yield of several billion seeds produced over 6 y. Apparently, P. eatonii has traits favoring pollination by hummingbirds without hindering pollination by mid-sized polylectic bees, at least in terms of maternal fitness. Manipulative floral experiments with Dudlyea greenei likewise showed that floral specialization for hummingbirds accommodated generalist bees as pollinators (Aigner, 2004). An evolutionary order of derivation-bee, then hummingbird-is supported by a Penstemon phylogeny (Wilson et al., 2007; Wolfe et al., 2006). If that evolutionary transition is gradual, then intermediate stages should engage both bees and hummingbirds, as is the case for P. eatonii.
Our own sensory biases might downplay the possibility of a mixed pollination syndrome for some redflowered penstemons. Several defining hummingbird syndrome traits are large and visually striking. Conversely, floral traits that attract or favor bees can be less apparent to us. We found, for instance, that the anther rims of P. eatonii brightly reflect ultraviolet light. Experiments by Lunau et al. (2011) showed that foraging orchid bees were attracted more to artificial red flowers that reflected UV wavelengths too; hummingbird visits continued apace. Thus, UV-reflective red flowers can attract visits from both bees and hummingbirds without compromise.
Bees at P. eatonii were all floral generalists (polylectic), both in this study and for earlier collections. The two western oligolectic bees of Penstemon, O. brevis and 0. penstemonis, were rare among bees taken at P. eatonii (4 of 259 specimens in the USDA-ARS Pollinating Insect Research Unit (PIRU), Utah State University, Logan, UT, collection). Instead, these two oligoleges frequent a host subgroup with blue or purple flowers (1/3 of the 272 Penstemon species). Their anthers commonly dispense pollen through narrow slits rimmed with pointed teeth (Lodewick and Lodewick, 1999). Torchio (1974) described how females of a pollen-wasp butt the staminode to reach the nectaries, thereby rasping their punctate thoracic dorsa against the dentate anthers. In response, pollen rains down from the anther slits. This action was seen and heard daily by females of this pollen-wasp and the two specialist Osmia bees foraging at blue-flowered penstemons in the Logan garden. These oligoleges were never seen at coflowering, adjacent P. eatonii.
Curiously, P. eatonii anther sacs are dentate too, but they open more widely, enabling generalist bees to forage by standing outside of the corolla tube, scrabbling with their legs to dislodge pollen. In so doing, they effected pollination. A narrowed corolla, like that of P. eatonii, positions a nectar-foraging hummingbird to more consistently pick up and later transfer pollen (Castellanos et al., 2004). The forward-facing, openly dehiscent anthers of P. eatonii (Fig. 2) are suited for this purpose but likely preclude the peculiar, but effective, anther rasping used by Penstemon oligoleges while they stand beneath the overarching stamens. For the combination of hummingbird and oligolectic bee, fitness trade-offs seem inevitable. As a corollary to Aigner's (2004) insights, then, we predict that no Penstemon of the hummingbird syndrome will be frequented by Penstemon specialists. Observations by Wilson et al. (2004) are supportive; they found no specialist Pseudomasaris wasps at flowers of any red-flowered Penstemon.
Narrowly tubular red corollas were posited to restrict attraction and access to just hummingbirds while deterring bees that take pollen and nectar to feed their brood, thereby depleting the plant's rewards and pollination potential (Castellanos et al., 2004). Hummingbirds do visit wild P. eatonii (Wilson et al., 2004); bees do also (Bateman, 1980). Tiny bees readily "steal" nectar and pollen from P. eatonii without stigma contact. They comprise 83% of the 259 individuals (36 of 56 species) taken at P. eatonii flowers and housed in the PIRU collections; only 2% were bumblebees. Multiple regressions of floral visitor classes on floral traits of Penstemon (Wilson et al,, 2004) likewise found that small generalist bees (e.g., Lasioglossum) were strongly associated with red tubular hummingbird flowers rather than the typical bee-pollinated species. Floral traits of P. eatonii may attract, reward, and position hummingbirds for pollen transfer, but they fail to exclude the very nectar or pollen thieves that were posited to be the targets of "anti-bee" adaptations. Conversely, it would be maladaptive for P. eatonii to deter visits by larger generalist bees because of their pollination value.
Bees were essential pollinators of P. eatonii at this farm but was that an artifact of cultivation? At another rural seed farm in southwestern Colorado, like-sized fields (0.3 ha) of P. barbatus were abundantly visited by broad-tailed hummingbirds (R. Hammon, pers. comm.), a bird also common in the Worland region. Both farms grew H. boreale plus two to three other penstemons for seed. The massive display of P. eatonii at Worland (Fig. 1) was a "bonanza resource" for bees, especially without hummingbirds to deplete nectar. However, for 10,500 honey bees foraging on just 1.3 ha of P. eatonii, nectar competition seemed likely. Wild bees might be less inclined to visit blooms at more scattered plants, especially if hummingbirds regularly removed their nectar. However, native bees greatly outnumbered hummingbirds at wild P. eatonii growing in central Utah (Bateman, 1980).
Red-flowered penstemons can be sorted by floral morphology into two functional groups relevant to bee access and pollination. The corollar opening of P. eatonii is rimmed by stubby petal lobes that are flared like the bell of a trumpet (Fig. 2A) giving pollen-foraging bees a landing platform. In contrast, the lower petal lobes of P. barbatus are deeply reflexed (Fig. 2B). The anthers of P. eatonii open quite broadly and are at the mouth of the flower (Fig. 2A). A mid-sized bee standing astride the flower's mouth can take pollen using its legs without entry or specialized behavior. From that position, it also contacts the stigma. Each honey bee seen at P. eatonii flowers at Worland sought nectar, thrusting its head into the corolla to reach its tongue to the basal nectary (Fig. 1 inset). In contrast, bumblebees placed on P. barbatus flowers (Castellanos et al., 2003) struggled to work the strikingly different corolla opening (Fig. 2B), underscoring how such simple corolla differences matter for foraging bees and pollination.
The floral traits of P. eatonii and its mixed pollinator syndrome are shared by P. centranthifolius (Mitchell, 1989). Like P. eatonii, P. centranthifolius has red tubular somewhat drooping flowers with radially flared stubby corolla lobes. It too seems to be effectively pollinated by honey bees and native larger-bodied generalist bees that scrabble at the anthers for pollen, as well as by nectar-foraging hummingbirds (Mitchell, 1989). It evolved independently of P. eatonii (Wilson et al., 2007; Wolfe et al., 2006).
What then is the evolutionary trajectory of the mixed pollinator strategy of P. eatonii and others like it? They could be transitioning from bee- to hummingbird pollination, a reasonable scenario for this rapidly evolving genus (Wolfe, 2006). Female fitness (seeds) is well-served by mid-sized female bees, but they can take 95-99% of host pollen out of circulation (e.g., Cane et al., 1996; Schlindwein et al., 2005), a potential cost for male fitness (Thomson and Thomson, 1992). Alternatively, these penstemons (Table 1) may embody a mixed but evolutionarily stable pollinator strategy that is overtly adapted for hummingbirds but also served by mid-sized polylectic bees. Pink-flowered P. pseudospectabilis maximized seed set when visited by both hummingbirds and bees (Lange and Scott, 1999; Reid et al., 1988); both groups also visit pink-flowered P. newberryi (Kimball, 2008). Attracting pollinators with such contrasting life histories as migratory hummingbirds and ground-nesting bees should better stabilize annual visitation intensities; for instance, populations of broad-tailed hummingbirds fluctuated three-fold annually at one montane location (Calder et al., 1983). Manipulative experiments with P. eatonii breeding and pollination ecologies could quantify female and male fitness tradeoffs for its contrasting pollinators.
Acknowledgments.--We thank Paul Wilson, Randy Mitchell and Peter Bernhardt for their valuable reviews. We dedicate this paper to the memory of Dr. Philip Torchio and his clever studies into the foraging mechanics of pollen wasps at Penstemon.
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JAMES H. CANE, (1) USDA-ARS Pollinating Insect Research Unit, Utah State University, Logan, 84322; and RICK DUNNE, Absaroka Farm, Worland, Wyoming, 82401. Submitted 25 March 2013; Accepted 11 November 2013.
(1) Corresponding author
Table 1.--List of Penstemon species with red tubular corollas, divided into a group lacking landing platforms and those judged to possess a landing platform suitable for foraging bees Red Penstemon Red Penstemon lacking platform with platform P. barbatus P. baccharifolius P. cardinalis P. centranthifolius P. labrosus P. fasciculatus P. pinifolius P. havardii P. rostriflorus P. isophyllus P. kunthii P. lanceolatus P. miniatus P. murryanus P. partyi P. subulatus P. superbus P. utahensis P. unightii
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|Title Annotation:||Notes and Discussion|
|Author:||Cane, James H.; Dunne, Rick|
|Publication:||The American Midland Naturalist|
|Date:||Feb 1, 2014|
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