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a Department of Entomology and Alabama Agricultural Experiment Station, Auburn University, Alabama 36849-5413;and b USDA-ARS Bee Biology and Systematics Laboratory, Utah State University, Logan, Utah 84322-5310
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: Hydrophyllaceae • Limnanthaceae • Limnanthes • Phacelia • pollination • ultraviolet-B radiation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Aspects of flowering critical to the reproduction of pollinating bees may be sensitive to elevated UV-B, including flowering phenology and flower production (Demchik and Day, 1996; Feldheim and Connor, 1996). Prolonged UV-B exposure can disrupt flowering phenologies of bee-pollinated mustard plants (Feldheim and Connor, 1996). In an ecological context, obligate plant/pollinator mutualisms are likely to be more responsive to such disruptions. For the solitary bee Dieunomia triangulifera, a Helianthus specialist, seasonal synchronization of bee emergence and host flowering enables females to harvest more pollen and thus produce more progeny (Minckley et al., 1994). Synchrony between the reproductive cycles of solitary bees and their host plants is common (Wcislo and Cane, 1996). However, if intensified UV-B delays host plant flowering, bees will emerge when host flowers should be available but are not. Bee emergence is unlikely to be altered by UV-B because bee nest cells should be well shielded from UV-B by nesting material. Another possible response to enhanced UV-B may be greater plant mortality or diminished flower production. These two host plant responses would require visiting female bees to spend more time and energy finding unvisited flowers, which could reduce plant reproductive potential or increase pollen residence time on the bee's body before reaching a receptive stigma. The volume and nutritional value of pollen and nectar may be diminished by UV-B as well. Taken collectively, these floral responses to UV-B could diminish the number of bees pollinating plants or alter the attractiveness of plants vying for pollinator services.
In our experiment, we assessed the floral responses of two annual, bee-pollinated plants, Limnanthes alba and Phacelia campanularia, to five incremental dosages of UV-B. We monitored the lifetime production of bloom and the temporal availability, quantity, and quality of pollen and nectar, because the foraging behaviors of bees are largely defined by these attributes, which in turn influence their value as pollinators. We present for the first time models that simultaneously predict flowering success, flowering phenology, and nectar and pollen yields for large plant populations subjected to a broad range of UV-B intensities. Reproductive success of a native solitary bee foraging at these plants will be reported elsewhere (Sampson and Cane, unpublished data)
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Seeds of L. alba were supplied by Oregon State University (Corvallis, Oregon) and P. campanularia seeds were purchased from Wild Seed, Inc. (Tempe, Arizona). Limnanthes alba seeds were germinated on moist paper towels for 7 d at 10°C in the dark. Phacelia campanularia seeds were removed from cold storage and placed onto Whatman filter paper moistened with gibberellic acid solution (0.01 mg/mL GA3) in plastic petri dishes. Phacelia seeds remained in the petri dishes for 24 h at 18C in the dark. P. campanularia seeds were then removed from the dishes and remaining GA3 rinsed away with distilled water. We expected only minor residual effects of the seed pretreatment on the morpholological characteristics of P. campanularia plants, as the embryo should rapidly metabolize the GA3.
On 17 August 1995, 200 seeds of each plant species were sown among 80 plastic pots containing 1700 cm of partially sterile Promix potting medium (Premier Horticulture Inc., Redhill, Pennsylvania). Five seeds of the same species were placed into each pot. The Promix was watered to saturation daily at 1600 Central Standard Time. Nitrogen, phosphorus, and potassium in the Promix were amended weekly with Peter's 15–16–17% water-soluble plant food once plants reached 3 wk of age. The daily temperature cycle for the glasshouse was supposed to be 25°C day/20°C night. However, on very hot, humid days, afternoon temperatures inside the glasshouse peaked at 32°C.
Experimental design
Potted plants were arranged in the glasshouse on a 1.6 x 10 m bench in a complete block design (2 blocks of UV-B lamp banks x 5 UV-B dosages x 2 plant species). A block experiment was chosen to prevent confounding the UV-B treatments with any temperature, humidity, or light gradients occurring inside the glasshouse and along the bench. Treatments could not be randomized within blocks because, to achieve a UV-B gradient along the bench, we tilted the lamp banks to vary the distance from the leaf canopy to the bulb. Plants growing closer to the lamps received more intense UV-B. Four pots of each plant species were randomly assigned to one of five UV-B treatments per experimental block. Pots remained in fixed positions rather than being rotated within a treatment, to avoid damage to intertwined vegetation as well as pollen loss. Systematic grouping of pots of the same plant species in trays within a UV-B treatment was necessary to prevent faster growing P. campanularia plants from shading L. alba from UV-B and ambient sunlight.
UV-B dosimetry
UV-B radiation was delivered by two banks of 14 UVB313 fluorescent lamps (Q-Panel Inc., Cleveland, Ohio). We intended to supply five lifetime UV-B dosages of 3, 6, 9, 12, 15 kJ·m·dto the plants. Since most of the natural UV-B was removed by glass walls, we had to supply a range of UV-B dosages that included ambient UV-B intensity (5 kJ·m·d). However, UV-B irradiance supplied by our lamp banks at the plant canopy increased with plant height and decreased with filter solarization. We did not raise the lamp banks because mature plants of both species rarely exceeded 30 cm. Phacelia also grew faster than Limnanthes and if we had raised the lamp banks, Limnanthes plants would have received disproportionately less UV-B. Instead, UV-B fluctuations due to plant growth and filter solarization were modeled for a few plants so slight adjustments to the intended UV-B could be calculated for every plant within each of the five UV-B treatments. After averaging the radiation dosages for the plants within each treatment, the five adjusted ultraviolet-Bbe300 dosages received by mature plants were close to the intended UV-B dosages measured when plants were seedlings. The new UV-B dosages were 2.74, 5.01, 9.17, 11.75, and 15.93 kJ·m·d. The range of UV-B dosages we used encompassed treatment levels used in other studies. The Green, Björn, and Murphy model modified by Fiscus and Booker (USDA-ARS, Raleigh, North Carolina) calculated global and annual UV-B irradiances and showed that our five UV-B dosages corresponded, respectively, to 24.5% increase and 7.0, 29.6, 34.0, and >34.0% reduction in spring (normal mean flowering time for the plants) ozone column level over Auburn, Alabama (32°62' N, 85°48' W). Although the latter three UV-B dosages are unrealistically intense, they are comparable to those used for other experiments and are useful for demonstrating tolerances of healthy flowering plants to intensified UV-B.
UV-B treatments commenced 28 August 1995, when seedlings were 11 d old and ~6 cm high, and ended 8 November 1995. All plants received artificial UV-B for 238 h. All 28 lamps were in continuous operation for 5 h/d centered at solar noon. For an additional 80 h that plants were scheduled to be dosed with UV-B, cloud cover prevailed. Lamps were not lit during this overcast period to avoid exaggerated plant damage that can occur from UV-B at reduced intensities of sunlight measured in watts per square metre (Krupa and Kickert, 1989). The average ratio of UV-B to sunlight was 0.12 and remained uniform throughout the 5-h UV-B dosing period. UV-B/sunlight ratios were also the same for both plant species.
Biologically effective UV-B radiation (wavelengths between 280 and 313 nm) was recorded daily using a Model 3D broadband UV radiometer (Solar Light Co. Inc., Philadelphia, Pennsylvania). The radiometer had a spectral response equivalent to Caldwell's generalized plant action spectrum and was calibrated with a UV-visible spectroradiometer (Model 742, Optronics Laboratories, Orlando, Florida.) which had been calibrated with an NIST traceable 1000 W tungsten-halogen standard. We modified the spectral output of our Q-Panel UV-producing lamps by removing UV-C with 0.013 mm thick cellulose acetate filters (Read Plastics, Rockville, Maryland). UV-C represents wavelengths shorter than 280 nm that do not naturally occur at the earth's surface, but are produced by artificial UV light sources. Replacing the acetate filters every 5 d maintained greater and more uniform intensities of UV-B. Sunlight intensity was monitored with a LI-COR pyranometer (Model LI-189, Lincoln, Nebraska).
Flowering
We recorded the numbers of plants that produced or failed to produce flowers at the five specific UV-B treatments. The flowering frequency of plants was analyzed using a 2 x 5 contingency table [two responses (flower/no flowers) x five UV-B treatments]. Possible linear trends in the proportion of plants that flowered were identified with the Cochran-Armitage trend test for categorical data (Agresti, 1990).
We tracked bloom by counting flowers every 3–4 d until each plant died. Cumulative flower production (a sigmoid curve) was modeled over time for every plant. It was difficult to quantify key phenological events that occurred between flower counts. Therefore a nonlinear regression line created a continuity between the discrete flower counts. This regression line fitted cumulative flower production for each plant and was estimated by nonlinear regression (PROC NLIN; SAS, 1985) using the following equation:
where CFP is cumulative flower production, LFP is total lifetime flower production, t is time in days, DMF is the day of maximum flower production, and c is a constant.
Total lifetime flower production (LFP) for some plants had to be extrapolated from the sigmoid model. Every model met convergence criteria at 95% confidence. A new estimated parameter was identified as the day a plant produces its first flower (DOF) and this parameter was calculated with the following equation:
The difference between the day of first flower (DOF) and the day a plant produces the most flowers (DMF) was an additional variable referred to as time to maximum flowering (TMF). TMF was equivalent to one-half the duration of a plant's flowering period. Doubling TMF gave us an accurate estimate of the time during which a plant produced its lifetime supply of flowers. The parameters LFP, DOF, DMF, and TMF were all obtained from the sigmoid model. The linear relationships DOF, TMF, and LFP shared with lifetime UV-B dosage were tested with SAS PROC GLM (SAS, 1985).
Pollen
Flowers were taken for pollen analysis from four randomly selected plants per UV-B treatment. Limnanthes alba anthers dehisced pollen gradually throughout a flower's lifetime. Therefore, this pollen was only collected from older, female-phase L. alba flowers. Conversely, P. campanularia quickly dehisced all five anthers during the earlier male phase. We removed P. campanularia anthers with their pollen from only male-phase flowers. Whole Limnanthes flowers and Phacelia anthers were collected every 3 d and placed into precleaned glass vials. Each vial was filled with filtered ethanol and the suspension dispersed in an ultrasonic bath. Half of the agitated subsample of the pollen suspension was counted using a HIAC-Royco PS-320 particle size analyzer (Pacific Scientific Inc., Silver Spring, Maryland). Doubling the pollen counts yielded total pollen production per flower.
ANCOVA models were used to analyze pollen production for L. alba and P. campanularia. Pollen harvest date was the covariate for the ANCOVA and accounted for increasing variance in pollen production resulting from a seasonal increase in the production of male-sterile flowers in both plant species. Individual plant variation was a random effect and was used as an error term for testing the null hypotheses that UV-B dosage effect equaled zero for all ANCOVA and MANCOVA analyses.
On 10 November, 2 d after UV-B treatments ended, we collected 19 pollen samples for pollen protein analysis. Each sample contained all of the pollen produced by 50 arbitrarily chosen flowers from 10 to 16 P. campanularia plants from each UV-B treatment. For more intense UV-B treatments, there was insufficient pollen for the protein analysis. Therefore, pollen was pooled into a low UV-B (2.74 and 5.01 kJ·m·d) and high UV-B (9.17, 11.75, and 15.93 kJ·m·d) treatment category. Anthers of L. alba produced too little easily accessible pollen to obtain the minimal 1.0-mg sample required for the protein assay. Protein concentrations in P. campanularia pollen were analyzed by the Bradford assay (Bradford, 1976), first modified for foliar samples (Jones, Hare, and Compton, 1989) and now adapted for pollen (Roulston and Cane, unpublished data) using the Biorad reagent (Bio-Rad Laboratories, New York). Cattail pollen, Typha latifolia L., was our standard. The percentage protein in the P. campanularia pollen for low and high UV-B categories was compared by ANCOVA analysis using sample mass as the covariate.
Nectar
Nectar volume and concentration were simultaneously measured every 3–4 d from two flowers on each plant. Nectar samples were taken from five randomly chosen plants in each of the five UV-B treatments. Measurements began 14 h after the plants were watered in an attempt to reduce variation in nectar flow due to fluctuations in plant water potential. Total nectar secreted during a flower's lifetime could not be accurately measured because repeated probing with microcapillary tubes damaged nectaries. We instead sampled female-phase flowers when adequate quantities of nectar were produced and the anthers did not obstruct the insertion of the microcapillary pipettes. Nectar concentration was measured with Bellingham and Stanley pocket refractometers (Tunbridge Wells, UK) modified for small volumes (0.2 µL). Nectar volumes between 0.05 and 0.1 µL for L. alba flowers required three neighboring flowers to be sampled and pooled to get a drop large enough for a reliable refractometer reading. This was justified because an ANOVA showed that 69% of the variation in sugar concentration occurred among L. alba plants and not among flowers on the same plant. Refractometer readings were converted to micrograms of sucrose equivalents per microlitre using a standard curve constructed from data provided by Bolten et al. (1979). Mass of sugar (micrograms sucrose equivalents) per nectar sample was the product of sugar concentration (micrograms of sucrose equivalents per microlitre) and nectar volume (microlitres). Numerous environmental variables contribute significantly to floral trait variation (Martinez del Rio and Burquez, 1986; Frazee and Marquis, 1994). Therefore, air temperature, relative humidity, and flower size (corolla diameter) were monitored after nectar was removed from each flower.
The frequency distributions of nectar volume, sugar concentration, and nectar sugar mass were left-skewed. Observations were log10 transformed, and the new resulting histograms were normal. Heteroscedasticity (increasing variance of the trait with greater UV-B intensity) was also reduced as was shown with the Kolmogorov D test. We used ANCOVA to test the effect of UV-B, relative humidity, and individual plant variability on floral nectar and pollen production, pollen quantity, and protein concentration. MANCOVA was used for testing the overall effect of UV-B on nectar volume and concentration simultaneously. Since UV-B can have both harmful and beneficial effects, contrasts to test possible trends (linear, quadratic, and cubic) in the data were constructed from polynomial coefficients (Lentner and Bishop, 1993).
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RESULTS |
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Components of flowering phenology and flower production
On average, L. alba plants produced their first flowers within 33 d after seedling emergence (Fig. 2A). Lifetime UV-B dosage did not prolong this period in the life cycle of L. alba (Fig. 2A), foreshorten the duration to maximum flowering (Fig. 2B), or decrease lifetime flower production (Fig. 2C). These results contrast sharply with the poorer success of entire L. alba plants to produce any flowers at increased UV-B dosages (Fig. 1).
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Pollen production and pollen protein concentration
UV-B (Fig. 3A), relative humidity, and plant variability (Table 1) did not influence the pollen production of L. alba and P. campanularia flowers, and enhanced UV-B did not alter the concentration of protein in P. campanularia pollen grains (Fig. 3B). Relative humidity did inhibit pollen yield for P. campanularia flowers (Table 1B). Generally, P. campanularia produced flowers with more pollen than L. alba (F = 24.30, df = 1, 268, P < 0.0001). However, gynodioecious P. campanularia produced significantly smaller flowers that produced fewer pollen grains later in the season (F = 23.53, df = 1, 133, P < 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Nectar fuels the foraging flights of adult bees and is the carbohydrate source in most larval provisions. Our results show that enhanced UV-B had little effect on nectar volume and concentration of P. campanularia or L. alba flowers. In a companion study to ours, Feldheim and Connor (1996) showed that doubling UV-B had no detectable impact on mustard nectar volume, sugar concentration, or floral visitation rates by European honey bees. However, intensified UV-B can reduce leaf area, leaf mass, and leaf number (Krupa and Kickert, 1989). Since leaves are the primary source of photosynthate for nectar sugars, UV-B may still have subtle effects on nectar sugar content. We did detect a subtle quadratic relationship between the sugar content of P. campanularia nectar and UV-B intensity. This effect is unlikely to be an appreciable predictor of bee floral visitation to Phacelia, since factors such as individual variability in plants and fluctuating relative humidity considered in this study were far more important in defining the pattern and richness of its nectar standing crop.
Female bees also provision their nests with pollen, the sole source of dietary protein for nearly all 30 000+ bee species. Pollen quantities and protein concentrations vary greatly among plant species (Roulston and Cane, unpublished data) with marked consequences for maturation time, survival, and adult bee size and longevity (Levin and Haydak, 1957; Schmidt et al., 1995). Enhanced UV-B did not diminish pollen production per flower for either plant species and did not influence the protein concentration of P. campanularia pollen. Therefore, pollen yields of individual flowers and the protein component of a larval bee's provisions are unlikely to suffer from enhanced UV-B received by floral host plants.
Oligolectic bees gather pollen from only a few closely related plant genera (Wcislo and Cane, 1996). They typically produce one generation per year and emerge from diapause when their host plants bloom. Reproductive success of oligolectic bees depends on the ability of a female bee to build and provision her nest before host bloom fades. Therefore, the longer the host is in bloom, the greater chances for her to increase offspring production. We found that UV-B can delay bloom, compress the flowering period, and reduce lifetime flower production for P. campanularia plants. Diminished flower production in a finite patch will diminish bee carrying capacity, commensurate with a decline in the number of oligolectic bee pollinators that the patch can support. A bee diapausing in a dark subterranean burrow or woody stem would not be affected by variations in solar UV-B intensity. Therefore, bee emergence would precede bloom of hosts that respond like P. campanularia, leaving a female bee with fewer days to provision her nest cells, provided she could survive the initial absence of host flowers for her own nutritional needs. Feldheim and Connor's pioneering UV-B studies with European honey bees and weedy exotic annuals could not have anticipated this possible result for native solitary bees and their floral hosts.
Polylectic bees, such as the European honey bee, gather nectar and pollen from various unrelated plant taxa. Flowering plants are to varying degrees pollinated by polylectic bees (Strickler, 1979). Fewer bees may visit Phacelia plants after intensified UV-B sufficiently alters the production or temporal availability of flowers so as to make the plant a less attractive host for polylectic pollinators (Motten, 1982; Burd, 1995). A steady stream of pollinator visitation can be expected for plants such as L. alba, which do not experience a delayed bloom and reduced lifetime flower production.
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FOOTNOTES |
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REFERENCES |
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; L. alba
plants, 
. Linear regression lines: slope 
0, ——; slope = 0, – – –.
