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Reproductive Biology |
2Division of Biological Sciences, 105 Tucker Hall, University of Missouri, Columbia, Missouri 65211-7400 USA; 4Center for Population Biology, University of California, Davis, California 95616 USA
Received for publication August 15, 2002. Accepted for publication November 22, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: flower heliotropism • maternal environmental effects • paternal environmental effects • Ranunculaceae • Ranunculus adoneus • solar-tracking flowers
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Sklenár, 1999
). Petal cell shape in snapdragons (Antirrhinum majus) determines light focusing depth, with potential implications for both pollinator attraction and flower temperature (Comba et al., 2000
). Flower orientation in tropical Convolvulus affects both pollinator preference and gynoecium temperature (Patiño and Grace, 2002
). Petal closure in Gentiana algida prevents pollen washout during thunderstorms (Bynum and Smith, 2001
). These examples illustrate that effects of floral traits on the microenvironment within flowers, while often neglected, are likely to be ubiquitous.
The widespread association of floral trait variation with modifications of the flower's microenvironment before and after pollination suggests that floral traits may be subject to selection through their effects on paternal and maternal environments as well as their impact on pollen donation and receipt. If traits that enhance floral attractiveness create a hostile environment for male gametophytes, then adaptive responses to pollinator-mediated selection could be slowed (Patiño et al., 2002
). In contrast, if the environmental effects of floral attractants on male quality and performance are favorable, attractive traits could spread more rapidly than predicted based on pollinator preference alone (Qvarnström and Price, 2001
). In this study, we address how flower heliotropism or solar tracking may influence pollen quality and performance by changing the floral microenvironment in the snow buttercup, Ranunculus adoneus.
Flower heliotropism represents a quintessential trait for studying the effects of floral variation on the parental environment for offspring (or gametophyte) development. Solar-tracking flowers are warmer and better illuminated than stationary flowers (Kevan, 1972
; Galen et al., 1993
; Kudo, 1995
; Patiño et al., 2002
). These microenvironmental differences may influence pollen quality at dispersal and rates of pollen germination and tube growth in the recipient pistil (Young, 1984
; Stanton and Galen, 1989
; Kudo, 1995
; Luzar and Gottsberger, 2001
; Patiño et al., 2002
). Variation in pollen viability, germination, and seed-siring capacity in relation to temperature and light quality during stamen development is widespread (Johannsson et al., 1994
; Demchik and Day, 1996
; Conner and Zangori, 1997
; Delph et al., 1997
). Similarly, temperature in the style can alter rates of pollen germination and tube growth (Kudo, 1995
). In snow buttercups and other species of cool arctic and alpine environments, solar tracking confers a positive maternal environmental effect by enhancing early seed growth rate and size at dispersal ("growth promotion" sensu Kevan, 1972
, 1975
; Galen et al., 1993
). Whether tracking also creates a favorable paternal or maternal environment for pollen development and performance in cold environments is not known.
To address the parental environmental effects associated with flower heliotropism, we ask the following questions: (1) Does paternal flower heliotropism influence pollen quality in Ranunculus adoneus? (2) Does maternal flower heliotropism affect the number of pollen grains germinating and pollen tubes per pistil in recipient R. adoneus flowers? (3) If so, does flower heliotropism alter pollen tube density by making flowers more attractive to pollinators (greater pollen deposition) or by enhancing conditions for pollen germination?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and staying closely aligned with the sun's rays. Overnight and during cloudy periods, stems are aligned vertically, with flowers facing the zenith. Solar tracking increases illumination by about 60% and temperature by 4°C for reproductive organs in R. adoneus (Stanton and Galen, 1989
). Additionally, heliotropic flowers exhibit a 57% increase in evapotranspiration compared to flowers aligned towards the zenith (C. Galen, unpublished data). In agreement with the impact of heliotropism on light and temperature of reproductive organs, seeds produced by tracking flowers are larger at maturity than those of experimentally restrained flowers (Stanton and Galen, 1989
). Seed size in turn has a positive impact on seedling establishment and estimated lifetime fitness (Stanton and Galen, 1997
).
Ranunculus adoneus is self-compatible but requires pollinator visitation to set a full complement of seeds (Stanton and Galen, 1989
). In our study population, outcrossing rate ranges from 0.3 to 0.8 (Stanton et al., 1997
). Flowers are visited by a variety of small flies, bees, and wasps. Insect residence time within flowers correlates positively with solar-tracking accuracy in nature (Stanton and Galen, 1989
).
Effect of paternal solar tracking on pollen quality
To assess the effect of flower heliotropism on pollen quality, pairs of neighboring snow buttercups with closely tracking terminal flowers (degrees deviation from the sun's rays 
20°) in the early green cup phase were randomly assigned between solar tracking (control) and stationary (tethered) treatments. The experiment was replicated on 3 July (10 donor pairs) and 9 July (15 donor pairs) 2001. We selected a third plant in the same stage of flower development to serve as a pollen recipient for each pair of donors. Recipients were located at equal distance from each member of the corresponding donor pair. Flowers of recipients were emasculated to prevent self-pollination and surrounded with fine-mesh (1-mm2 bridal veil) screening to exclude insect visitors (Stanton and Galen, 1989
). In each donor pair, the control flower was left free to track the sun, while the stationary flower was tethered in place. Tethering was accomplished by placing a piece of plastic straw around the stem and inserting a wire "stake" through the straw into the ground (Stanton and Galen, 1989
). Stems grow throughout anthesis, causing flowers to "escape" their tethers. To eliminate this problem, tethers on stationary flowers were checked and adjusted twice daily to maintain the appropriate flower orientation throughout the experiment. Tethered flowers were oriented facing the zenith or mid-day sun (90°) using a magnetic protractor (Ace 25865). One day after tethering, solar tracking accuracy of stationary and tracking flowers was measured between 0800–0900 and again between 1300–1400 with a modified sundial consisting of a shallow "funnel" with a pointer at the center (heliotropometer; Stanton and Galen, 1989
). The shadow cast by the pointer measures angular solar deviation over a 0–90° range. Anthers of donor flowers began to dehisce 2–3 d after the onset of treatments (F1,21 = 0.93, P > 0.34 for the difference in dehiscence schedule between treatments). Because pollen of R. adoneus is rapidly stripped from the anthers by insect foragers, a fine mesh (1-mm2 bridal veil) cage was placed over the plant between 0730 and 0800 on the first morning that the anthers began to dehisce. At mid-morning (0900–1100), six pistils were removed with sharp forceps from the assigned recipient and inserted upright into an agar layer in the bottom of a small petri dish. For each donor, two pistils were hand-pollinated by removing a dehiscent anther with sharp forceps and brushing it 3–5 times across the stigma surface. Separate anthers were used to pollinate each pistil. The remaining two pistils were left unpollinated to control for possible pollen contamination. When both donor flowers in a pair matured on the same day, pollinations were performed in a randomized order with respect to donor treatment. Immediately after pollinations, plates were tightly covered and placed in an open sunlit location for the remainder of the day. Overnight, plates were stored outdoors in a screened enclosure at the field site. After 24 h, pistils were collected and placed individually into vials of fixative (3 : 1, ethanol : acetic acid) for pollen tube counts. In the laboratory, pistils were rinsed in water, cleared using concentrated (8N) NaOH, and stained with 1% aniline blue to visualize pollen tubes (Martin, 1958
). We scored pollen germination by counting the number of pollen tubes entering the pistil.
To ensure that comparable amounts of pollen were transferred from the two donor flowers in each pair, a second set of pollinations was performed using the same technique and set of pollen donors, but the pollen from each donor was deposited onto a glass microscope slide. Donor anthers were brushed three times across a circle inscribed with a permanent marker on the slide surface. Immediately after pollen transfer, a small cube of fuschin gel was placed next to the circle and heated gently over an alcohol lamp to melting (Beattie, 1971
). After the liquefied gel covered the pollen sample, a cover slip was placed over the circle and the slide was transported to the laboratory. All pollen grains deposited in the circle were counted under a light microscope at 200x magnification.
To verify that tethering altered solar-tracking behavior, we tested whether the mean the degrees deviation from the sun's rays averaged over morning and afternoon measurements differed significantly between stationary and tracking flowers using mixed model analysis of variance (PROC MIXED), with treatment and donor pair designated as fixed and random effects, respectively. Variation among treatments in the number of pollen tubes per pistil and pollen grains per slide was analyzed similarly, by mixed model analysis of variance (mixed procedure, SAS version 6; SAS Institute, 1995
) with treatment as a fixed effect and donor pair as a random effect. Here and elsewhere, pollen tube and pollen grain counts per recipient flower were averaged and square-root (x + 1) transformed before analysis to correct for deviations from normality; separate analyses were conducted for each variable. Planned contrasts were used to test for effects of treatment (stationary vs. tracking donor flowers) on the number of pollen grains germinating and amount of pollen transferred.
Effect of maternal solar tracking on pollen performance
We measured the number of pollen grains germinating and pollen tubes reaching midway down the style of tracking (control, N = 11) and stationary (tethered, N = 12) snow buttercup flowers in July 1988. Plants were randomly selected and assigned to treatments on 17 July when their flower stems had just emerged from the melting snow. Tethered stems of terminal flowers were fixed at randomly chosen positions along an east–west trajectory, with incline averaging 78° ± 20° (SD, N = 12 plants) and flowers oriented at least 50° from the ground. Tethers were adjusted daily throughout the flowering period to maintain the initial orientation. All flowers were exposed throughout anthesis to naturally occurring pollinators. Degrees deviation from the sun's rays was measured for each flower between 0800–1000 and again between 1300–1500 on the second day of the female phase. After the petals faded at the end of anthesis (22–24 July), six pistils were collected from each flower (three each from the innermost and outermost whorls) into vials containing fixative (3 : 1, ethanol : acetic acid). In the laboratory, pistils were rinsed, cleared, stained with aniline blue (Martin, 1958
), and visualized under fluorescence microscopy. We counted the number of pollen grains germinating on the stigma surface and pollen tubes reaching midway down the style. A one-way ANOVA was used to verify the impact of tethering on mean deviation from the sun's rays, averaged over morning and afternoon measurements for each flower (PROC GLM; SAS Institute, 1995
). We compared tracking and stationary flowers for the average number of pollen grains germinating using a one-way ANOVA. To determine whether tracking directly affects pollen tube growth, we used an analysis of covariance (ANCOVA) to test for an effect of treatment on the number of pollen tubes reaching the midpoint of the pistil after variation due to the number of pollen grains germinating per pistil (covariate) was removed from the model.
Because stationary and tracking flowers differed significantly in both the amount of germinating pollen and the number of pollen tubes at mid-style (see Results, Fig. 1), a second experiment was performed to identify the mechanism by which solar tracking affects pollen tube number. Specifically, this experiment aimed to distinguish the effect of solar tracking on pollen deposition from its effect on pollen germination. In 2002, we randomly selected 15 snow buttercups with newly emerged flower stems and measured deviation of their flowers from the sun's rays on the first morning (0800–0900) and again in the afternoon (1400–1500) of the female phase (21–22 June). One flower was lost to grazing, reducing the sample size to 14 plants. When the petals faded at the end of anthesis (24 June), pistils were collected from inner and outer whorls of the gynoecium to count the total amount of pollen deposited and the number of pollen grains germinating. Two pistils per flower were sampled for each type of count. Pistils collected to assay pollen deposition were stained with fuschin gel and scored under the light microscope (Beattie, 1971
). Pistils used for pollen tube counts were processed as described earlier. Multiple regression analysis (PROC REG, SAS Institute, 1995
) was used to test whether the deviation of each flower from the sun's rays affected the amount of pollen deposited or the number of pollen grains germinating per pistil. For these analyses, we included morning and afternoon angles of incidence separately rather than averaging them, because we were interested in examining whether the impact of tracking accuracy on pollen receipt and germination differs between cool morning and warmer afternoon periods. Morning and afternoon measurements of the solar deviation for each flower were not strongly correlated in this experiment (r = –0.12, NS). In the analysis of pollen deposition, morning and afternoon angles of incidence were specified as independent variables and the mean number of pollen grains per stigma was used as the outcome variable. To assess whether deviation from the sun's rays affected the number of pollen grains germinating, we performed a second regression analysis using mean pollen tube density per pistil as the outcome variable. Type III sums of squares (partial regression coefficients) were used to evaluate the independent effects of morning and afternoon solar deviation on the number of pollen grains germinating after accounting for variation due to pollen deposition.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Effect of maternal solar tracking on pollen performance
Control and tethered flowers differed significantly in solar-tracking accuracy in 1988, with mean solar deviation of 14° ± 2° and 33° ± 3°, respectively (F1,17 = 25.68, P < 0.0001). Pistils of solar-tracking recipient flowers had significantly more germinating pollen and pollen tubes reaching midway down the style than pistils of stationary flowers (F1,21 = 7.66, P < 0.0115 and F1,21 = 8.99, P < 0.0069, respectively; Fig. 1). The impact of tracking on pollen tube density midway down the style is mediated through pollen germination. The number of pollen grains germinating explains 61% of the variation in pollen tube density (F1,19 = 137.59, P < 0.0001). When the number of grains germinating per pistil is included as a covariate in the analysis of tube density, the significance of the treatment effect vanishes (ANCOVA, F1,19 = 0.08, P > 0.78). Because snow buttercup achenes contain only one seed each, pollen tube : ovule ratio averaged 7.3 ± 1.0 (SE) in pistils of tracking recipients and 4.1 ± 0.6 (SE) in pistils of stationary recipients. From this experiment, we could not determine whether tracking alters pollen tube density by modifying pollen deposition or pollen germination because total pollen deposition was not measured.
Observations made in 2002 to address this question revealed that the positive impact of solar tracking on pollen tube density is mediated through pollen germination rather than pollen deposition. Multiple regression showed no significant effect of morning or afternoon tracking accuracy on the amount of pollen deposited per pistil (F1,12 = 1.33 and 0.56 respectively, P > 0.20 for both; Fig. 2). As expected, the amount of pollen deposited on the stigma had a significant positive effect on the number of pollen grains germinating per pistil (partial regression coefficient, b = 0.13 ± 0.046 (SE), t = 2.88, P < 0.0182). Additionally, in the morning when air temperatures are cool, deviation from the sun's direct rays significantly reduced the number of pollen grains germinating per pistil (b = –0.090 ± 0.037, t = 2.39, P < 0.04; Fig. 2). However, in the afternoon tracking behavior had no significant impact on pollen germination (b = 0.074 ± 0.067, P > 0.29).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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An alternative hypothesis for the superior performance of pollen from solar-tracking flowers involves differential selection on male microgametophytes during their development, under stationary vs. tracking flower environments. Under this scenario, the difference in pollen performance between treatments would have a genetic rather than environmental basis (Mazer and Gorchov, 1996
). Our experiment does not allow us to exclude this explanation. However, as elaborated below, flower heliotropism causes pronounced changes in several microenvironmental factors that have known influences on pollen viability, supporting the inference of paternal environmental effects.
Paternal environmental effects on pollen quality in flowering plants have been a topic of much recent interest (Schlichting, 1985
; Young and Stanton, 1990
; Delph et al., 1997
; Aizen and Raffaele, 1998
; Travers, 1999
). However, most studies have focused on the impact of spatial environmental heterogeneity on pollen donor quality. Temperature, UV-B intensity, herbivore pressure, and nutrient availability have all been implicated as potential sources of paternal environmental effects. The extent to which plant traits modify or buffer the paternal environment for pollen development has been less studied. Flint and Caldwell (1983)
suggest that anther walls reduce possible environmental effects on pollen quality by shielding the developing pollen from UV-B. For the 11 species that they studied, UV-B penetration never exceeded 2% of ambient dosages (but see Demchik and Day, 1996
). Patiño et al. (2002)
showed that the parasol-like shape of tropical convolvulaceous flowers provides a source of shade for the gynoecium and androecium with potentially positive effects on male gametophyte viability. In snow buttercups, flower heliotropism may ameliorate two environmental challenges to pollen fertility. First, heliotropism causes a 3°–5°C increase in flower temperature relative to ambient (Stanton and Galen, 1989
). In Petunia hybrida, a diurnal temperature increase of 5°C during pollen maturation in the laboratory significantly enhanced pollen tube growth rate (van Herpen, 1985
). Additionally, by increasing the rate of evapotranspiration from floral tissues, solar tracking may provide a more humid environment for developing pollen. High relative humidity during pollen maturation increases anther hydration and pollen germination in vitro (Gilissen, 1977
). These explanations are not mutually exclusive and further experiments manipulating floral microclimate will be necessary to distinguish between them (e.g., Patiño and Grace, 2002
).
For recipient flowers of R. adoneus, solar tracking directly affects seed size by improving the maternal environment for carpel photosynthesis (Stanton and Galen, 1989
; Galen et al., 1993
). Findings of the present study suggest that maternal flower heliotropism also enhances microenvironmental conditions for pollen germination. We explored pre- and post-pollination mechanisms for the positive effect of solar tracking on pollen tube density. Our results provide little support for the idea that solar-tracking recipient flowers gain a pollination advantage, though past studies have shown that insect visitors spend more time basking in closely tracking flowers (Stanton and Galen, 1989
). Instead, the present study suggests that by modifying the floral microenvironment, tracking increases the number of germinating grains per pistil in R. adoneus. Research on other species with heliotropic flowers has shown that solar tracking influences pollen germination, tube growth, and viability in vitro through its effects on pistil temperature (Kudo, 1995
; Patiño and Grace, 2002
). Pistil temperature is also a plausible explanation for the effect of solar tracking on pollen performance in R. adoneus. Poor tracking under warm afternoon conditions had no significant impact on pollen germination, while deviation of flowers from the sun's rays in the cool morning hours significantly reduced pollen germination success.
Our results add to a growing body of data illustrating environmental effects on pollen quality in nature. However, it is less clear that such effects translate into enhanced offspring fitness. Only two studies have demonstrated paternal environment effects on offspring phenotype in flowering plants (Lacey, 1996
; Galloway, 2001
). Both studies found that variation in abiotic aspects (temperature and light) of the paternal environment affected the expression of fitness-related traits early in the life cycle of seed progeny. Because solar tracking affects both of these environmental factors within flowers, it is tempting to infer that, along with its maternal effects on seed size (Stanton and Galen, 1989
), paternal environmental effects of heliotropism should enhance offspring quality in R. adoneus. However, this conclusion awaits a direct test for offspring effects, as could be provided by reciprocal crosses between tracking and nontracking plants (e.g., Galloway, 2001
).
Environmental effects on pollen performance should influence offspring quality if they promote opportunities for intrasexual selection (Willson and Burley, 1983
; Snow and Spira, 1991
). Male–male competition should ensue from high pollen tube : ovule ratios, when resources rather than mate availability limit the capacity of maternal parents to set seed (Bateman's principle, Bateman, 1948
; Willson and Burley, 1983
). Pollen supplementation has no significant impact on the number of seeds set by plants of R. adoneus at our study site (Stanton and Galen, 1989
; C. Galen, unpublished data). Conversely, resource availability, mediated in large part by the length of the growing season, has a pronounced effect on fecundity (Stanton and Galen, 1997
). Especially in late-melting, resource-poor portions of alpine snowbeds, effects of solar tracking on pollen tube density may have a large impact on offspring quality. Future studies, investigating how effects of parental solar tracking on offspring quality vary over the sharp resource gradient produced by increasing snow depth, should shed light on the adaptive significance of flower heliotropism as well as on the ecological importance of parental environmental effects in nature.
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FOOTNOTES |
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4 Author for reprint requests (galenc{at}missouri.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Bateman A. J. 1948 Intrasexual selection in Drosophila. Heredity 2: 349-368[Web of Science][Medline]
Beattie A. J. 1971 A technique for the study of insect-bourne pollen. Pan Pacific Entomologist 47: 82.[Web of Science]
Bynum M. R. W. K. Smith 2001 Floral movements in response to thunderstorms improve reproductive effort in the alpine species Gentiana algida (Gentianaceae). American Journal of Botany 88: 1088-1095
Comba L. S. A. Corbet H. Hunt S. Outram J. S. Parker B. J. Glover 2000 The role of genes influencing the corolla in pollination of Antirrhinum majus. Plant, Cell and Environment 23: 639-647
Conner J. K. L. A. Zangori 1997 A garden study of the effects of ultraviolet-B radiation on pollination success and lifetime fitness in Brassica. Oecologia 111: 388-395[CrossRef][Web of Science]
Delph L. F. M. H. Johannsson A. G. Stephenson 1997 How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78: 1632-1639[CrossRef][Web of Science]
Demchik S. M. T. A. Day 1996 Effect of enhanced UV-B radiation on pollen quantity, quality, and seed yield in Brassica rapa (Brassicaceae). American Journal of Botany 83: 573-579[CrossRef][Web of Science]
Flint S. D. M. M. Caldwell 1983 Influence of floral optical properties on the ultraviolet radiation environment of pollen. American Journal of Botany 70: 1416-1419[CrossRef][Web of Science]
Galen C. T. E. Dawson M. L. Stanton 1993 Carpels as leaves: meeting the carbon cost of reproduction in an alpine buttercup. Oecologia 95: 187-193[CrossRef][Web of Science]
Galloway L. F. 2001 The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). American Journal of Botany 88: 832-840
Gilissen L. J. W. 1977 The influence of relative humidity on the swelling of pollen grains in vitro. Planta 137: 299-301[CrossRef][Web of Science]
Johannsson M. H. J. A. Winsor A. G. Stephenson 1994 Genetic and environmental effects on in vitro pollen tube growth in Cucurbita. In A. G. Stephenson and T.-H. Kao [eds.], Pollen–pistil interactions and pollen tube growth, 307–309. Current topics in plant physiology, vol. 12. American Society of Plant Physiologists, Rockville, Maryland, USA
Kevan P. G. 1972 Heliotropism in some arctic flowers. Canadian Field Naturalist 86: 41-44
Kevan P. G. 1975 Sun-tracking solar furnaces in high Arctic flowers: significance for pollination and insects. Science 189: 723-726
Kudo G. 1995 Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72: 14-20[CrossRef][Web of Science]
Lacey E. P. 1996 Parental effects in Plantago lanceolata. I. A growth chamber experiment to examine pre- and postzygotic temperature effects. Evolution 50: 865-878[CrossRef][Web of Science]
Levin D. A. L. Watkins 1984 Assortative mating in Phlox. Heredity 53: 595-602[Web of Science]
Luzar N. G. Gottsberger 2001 Flower heliotropism and floral heating of five alpine plant species and the effect on flower visiting in Ranunculus montanus in the Austrian Alps. Arctic, Antarctic, and Alpine Research 33: 93-99[CrossRef][Web of Science]
Martin F. W. 1958 Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 125-128
Mazer S. J. D. L. Gorchov 1996 Parental effects on progeny phenotype in plants: distinguishing genetic and environmental causes. Evolution 50: 44-53[CrossRef][Web of Science]
Patiño S. J. Grace 2002 The cooling of convolvulaceous flowers in a tropical environment. Plant, Cell and Environment 25: 41-51
Patiño S. C. Jeffree J. Grace 2002 The ecological role of orientation in tropical convolvulaceous flowers. Oecologia 130: 373-379[CrossRef][Web of Science]
Qvarnström A. T. D. Price 2001 Maternal effects, paternal effects and sexual selection. Trends in Ecology and Evolution 16: 95-100
SAS Institute. 1995 SAS/STAT user's guide. Ver. 6.12. SAS Institute, Cary, North Carolina, USA
Schlichting C. D. 1985 Environmental stress reduces pollen quality in Phlox: compounding the fitness deficit. In D. L. Mulcahy, G. Bergamini Mulcahy, and E. Ottaviano [eds.], Biotechnology and ecology of pollen, 483–488. Springer-Verlag, New York, New York, USA
Sklenár P. 1999 Nodding capitula in the superparamo Asteraceae: an adaptation to unpredictable environment. Biotropica 31: 394-402[CrossRef][Web of Science]
Snow A. A. T. P. Spira 1991 Pollen vigor and the potential for sexual selection in plants. Nature 352: 796-797[CrossRef]
Stanton M. L. C. Galen 1989 Consequences of flower heliotropism for reproduction in an alpine buttercup (Ranunculus adoneus). Oecologia 78: 477-485[CrossRef][Web of Science]
Stanton M. L. C. Galen 1993 Blue light controls solar tracking by flowers of an alpine plant. Plant, Cell and Environment 16: 983-989[CrossRef]
Stanton M. L. C. Galen 1997 Life on the edge: adaptation versus environmentally mediated gene flow in the snow buttercup, Ranunculus adoneus. American Naturalist 150: 143-178[CrossRef][Web of Science]
Stanton M. L. C. Galen J. Shore 1997 Population structure along a steep environmental gradient: consequences of flowering time and habitat variation in the snow buttercup, Ranunculus adoneus. Evolution 51: 79-94[CrossRef][Web of Science]
Travers S. E. 1999 Pollen performance of plants in recently burned and unburned environments. Ecology 80: 2427-2434[Web of Science]
van Herpen M. M. A. 1985 Biochemical alterations in the sexual partners resulting from environmental conditions before pollination regulate processes after pollination. In D. L. Mulcahy, G. Bergamini Mulcahy, and E. Ottaviano [eds.], Biotechnology and ecology of pollen, 131–134. Springer-Verlag, New York, New York, USA
Willson M. F. N. Burley 1983 Mate choice in plants. Princeton University Press, Princeton, New Jersey, USA
Young H. M. L. Stanton 1990 Influence of environmental quality on pollen competitive ability in wild radish. Science 248: 1631-1633
Young T. P. 1984 Solar irradiation increases floral development rates in afro-alpine Lobelia telekii. Biotropica 16: 243-245[CrossRef][Web of Science]
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