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Reproductive Biology |
Department of Biology, Southwest Missouri State University, 901 S. National, Springfield, Missouri 65804 USA
Received for publication September 26, 2000. Accepted for publication February 13, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: glades • habitat fragmentation • hawk moth pollination • Oenothera • Onagraceae • pollination limitation • Sphingidae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hainsworth, Wolf, and Mercier, 1985
; Ayre and Whelan, 1989
; Ackerman and Montalvo, 1990
; Johnston, 1991
; Young and Young, 1992
; Burd, 1994
). Species that evolved in a constant, predictable pollinator environment may currently be experiencing pollination limitation due to the recent loss of a pollinator or a reduction in pollinator activity, often associated with anthropogenic factors such as habitat fragmentation (Sih and Baltus, 1987
; Spears, 1987
; Jennersten, 1988
; Sowig, 1989
; Johnston, 1991
; Aizen and Feinsinger, 1994
), the use of insecticides in agriculture and forestry (Thomson, Plowright, and Thaler, 1985
; Kearns, Inouye, and Waser, 1998
), or the introduction of exotic species (Tuskes and Emmel, 1981
; Kearns, Inouye, and Waser, 1998
). Alternatively, species that have historically experienced unpredictably fluctuating pollinator environments may have evolved the overproduction of flowers and ovules as a bet-hedging mechanism to take advantage of "boom" years with heavy pollinator activity (Cohen and Dukas, 1990
; Burd, 1995
). In such species, reproduction in many years will be pollination limited.
Plants pollinated by hawk moths (Lepidoptera: Sphingidae) may be particularly prone to pollination limitation. Fluctuating hawk moth populations (Knowlton, 1953
; Chase and Raven, 1975
; Miller, 1981, 1983
) combined with migration (Grant, 1937
; Knowlton, 1953
; Ohba, Wasano, and Matsuda-Ohba, 1999
) and variation in the time of first brood production (Brou and Brou, 1997
) could create an unpredictable pollinator environment. Furthermore, hawk-moth-pollinated plants are characterized by the production of large, showy flowers containing copious amounts of nectar (Proctor, Yeo, and Lack, 1996
). Burd (1995)
argues that plants with costly flowers and unpredictably variable pollination will be selected to overproduce ovules as a bet-hedging strategy.
Hawk-moth-pollinated plants may also be more prone to reduced pollinator activity as a result of habitat fragmentation. Many pollinators discriminate against smaller and/or less dense patches of flowers as they represent a lower quality food source (Silander, 1978
; Groom, 1998
). Hawk moths may be more likely than other insect pollinators to pass up such patches, due to their energetically costly hovering flight (Bartholomew and Casey, 1978
; Heinrich, 1983
; Voigt and Winter, 1999
) and their ability to fly long distances (Linhart and Mendenhall, 1977
; Chase et al., 1996
).
Despite this, few studies exist that examine pollination limitation in hawk-moth-pollinated plants, especially in relation to habitat fragmentation. Fruit set in Viola cazortensis, pollinated by diurnal hawk moths, may be pollinator limited as it naturally varies with hawk moth abundances (Herrera, 1990
). In addition, inadequate pollen transfer by hawk moths has been demonstrated in at least two plant species. Pavlik, Ferguson, and Nelson (1993)
found that seed set in Oenothera deltoides ssp. howellii was pollination limited, with only 26 and 37% of maximum seed output in two different years. In Ruellia humulis, a native prairie plant with a hawk moth pollination syndrome, estimated outcrossing rates have changed from a historical value of 
50% to a current value of <1%, suggesting a reduction in hawk moth visitation (J. Heywood, Southwest Missouri State University, unpublished data).
As a result of recent human activities, the glade habitat to which the Missouri evening primrose, Oenothera macrocarpa (Onagraceae), is native in Missouri has been significantly reduced and fragmented (Nelson, 1985
), leading to the concern that pollinator visitation rates may have declined. Both floral syndrome (Baker, 1961
; Faegri and van der Pijl, 1979
) and prior studies (Nonnenmacher, 1999
; Mothershead and Marquis, 2000
) suggest this species is hawk moth pollinated. The purpose of this study was to determine whether O. macrocarpa is experiencing pollination limitation. Specifically, the following questions were addressed. (1) Is fruit and/or seed set of O. macrocarpa pollination limited? (2) If so, does the extent of pollination limitation vary among populations that differ in size, density, and habitat quality?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The large, yellow, funnelform flowers are up to 12 cm in diameter with a long-slender corolla tube up to 13 cm in length (Great Plains Flora Association, 1986
). Floral tubes contain copious nectar, but no scent is apparent. Pollen grains are relatively large and are connected by long, elastic viscin threads that hold the pollen grains together (Ting, 1966
). Individuals are reported to be self-incompatible (Crowe, 1955
; Mothershead and Marquis, 2000
), and this was confirmed by artificially selfing and bagging flowers on ten plants at Henning.
In 1999, plants included in this study flowered from 12 May to 6 June. Flowers opened with anthers dehisced in the evening between 1800 and 2100 (Central Daylight Savings Time). Sunset occurred at 2000. Plants frequently produced more than one new flower per night. Individual flowers are reported to stay open for one night and wilt the next morning (Steyermark, 1963
). However, during this study individual flowers remained open through the day and into the next evening. Second-night flowers were easily distinguished from first-night flowers as they had anthers stripped of pollen, stigmas that appeared dried, and petals that were ragged and less vibrant in color. The color difference between first- and second-night flowers was most readily apparent after dark. Flowers wilted back sometime following the second evening, but remained attached to the ovary for one to several days before abscising.
The fruits are conspicuous, four-winged capsules that are green and fleshy when first produced and dry out, turning brown as they mature. Fruits dehisce apically in mid- to late-summer.
Study sites
Three sites owned and operated by the Missouri Department of Conservation were used for this study. (1) The Ruth and Paul Henning Conservation Area is located within the city limits of Branson in southwestern Missouri, USA. The White River Balds Natural Area is 146 ha of dolomite and limestone glades located within the Henning Conservation Area. The population used for this study is located on the south-facing slope of South Cox's Bald, which is part of the White River Balds Natural Area (36°40' N, 93°19' W). (2) Busiek State Forest and Wildlife Area is located 29 km south of Springfield, Missouri, USA. Most of Busiek's 1014 ha are forested, but it contains 109 ha of dolomite glades. The experimental population is located on a glade above the firing range on the west side of the park (36°52' N, 93°14' W). (3) The Drury-Mincy Conservation Area is a two-tract conservation area located east of Branson, Missouri, containing a total of 500 ha of dolomite glades. However, O. macrocarpa is not known from these glades. The study population is located at a small, highly disturbed roadside site near the public campgrounds in the Mincy area (36°33' N, 93°14' W).
Experimental procedures
Prior to flowering, experimental plants were chosen haphazardly from throughout the entire local population at each site. Only plants with three or more flower buds were included in the experiment. Experimental plants were randomly assigned to either a control group or a treatment group (Table 1). Because plants were readily accessible to the public at Mincy, they were marked only with plastic tags at ground level. At Henning and Busiek plants were marked with green wire flags in addition to the plastic tags. All other procedures were the same at all three populations.
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1700 for the duration of the flowering period. On each such evening, all open flowers on experimental plants were marked with colored thread that indicated the date of flowering. Flowers on control plants were not otherwise manipulated. Some flowers on treatment plants were given supplemental pollen. Flower age at the time of supplementation was recorded as first night or second night. Across all sites and all plants, 41% of marked flowers on treatment plants were supplemented, with a range of 12.5–100% of the flowers per plant. A wooden toothpick was used to collect supplemental pollen from newly opened flowers on five to seven different plants not otherwise included in the study. The pollen was mixed thoroughly in a plastic petri dish to reduce the chances of using a high proportion of incompatible pollen. Pollen was then applied with wooden toothpicks to the stigmas of supplemented flowers, making sure that all four stigma lobes were evenly covered with pollen. Supplemental pollen was collected in the same population in which it was used.
Supplemental pollination was completed around dusk, but before total darkness, for obvious practical reasons, but also to minimize disturbance of natural hawk moth pollinators. First-night flowers were often not completely opened at this time. These flowers were easily opened by peeling back the sepals, causing no noticeable damage to other floral structures.
The fate of each flower on experimental plants was followed. Starting about 4 June some of the marked fruits began to abort. Aborted fruits were collected upon discovery, always after they abscised from the plant. Mature fruits were collected from 12 June to 23 July. Prior to the final collection, only fruits that had abscised from the plant were collected. By 23 July all fruits had either abscised or begun to dry out. Thus all remaining fruits were collected on this date even if they were still attached to the plant. When fruit and aborted ovaries abscised, they most often fell on the ground directly below the attachment point, frequently with the colored thread still attached. This made identification of individual fruits easy. For each flower produced, a fruit or aborted ovary was collected with a few exceptions when a corresponding fruit or aborted ovary was not able to be located. Aborted and mature fruits were kept in a freezer (–30°C) until seeds could be counted.
Ovules were scored either as unfertilized ovules, aborted seeds, or mature seeds. Aborted seeds were ovules that had clearly initiated development into a seed, but had not achieved maturity. The distinction between unfertilized ovules, aborted seeds, and mature seeds was generally clear, and unfertilized ovules and aborted seeds were easily counted. The combined total number of unfertilized ovules, aborted seeds, and mature seeds in a fruit was assumed to be equal to the total number of ovules initially present in the ovary. Fertilization success for a flower was calculated as the total number of mature and aborted seeds in the fruit divided by the total number of ovules in the ovary. Seed set per flower was calculated as the number of mature seeds divided by the total number of ovules in the ovary. Aborted ovaries were able to be included in all analyses of fertilization success and seed set because the number of ovules and aborted seeds in them could easily be counted.
Reproductive output can be affected by plant size (Krannitz and Maun, 1991
; Lawrence, 1993
) and conspecific plant density (Handel, 1983
; Kunin, 1997
; Roll et al., 1997
; Bosch and Waser, 1999
). To assess whether these variables are associated with reproductive output in the study populations, plant size and local conspecific plant density were estimated for each experimental plant. Size was estimated by the number of stems and the number of flower buds at the beginning of the experiment as well as by the number of flowers produced. Local conspecific plant density was measured as the number of plants of O. macrocarpa within a 10-m2 circular plot centered around each experimental plant. Many plants in the study populations did not flower in 1999, so conspecific plant density was measured both as flowering plant density and total plant density. Plants were counted as having flowered if they had fruits, attached ovaries, or flower scars on the stems. These measurements were taken after the flowering period.
Flowers were observed throughout the flowering season for floral visitors, both at night and in the early morning. Observations were limited, with only 12 h of observations occurring at night (2000–2400) and 4 h occurring in the early morning (0200–0600). For periods after dark, observations were made with flashlights covered with a film of red plastic to reduce disturbance to hawk moths.
Statistical analysis
All statistical analyses were conducted using the MINITAB Statistical Package version 12.1 (Minitab, 1998
). All multifactorial ANOVAs were conducted with the GLM procedure and all mean squares were based upon adjusted sums of squares. Site was treated as a fixed-effects factor in all ANOVAs that included site since the three study sites were deliberately chosen to represent extremes in population size and disturbance as well as to be close to Springfield, Missouri. Contingency table analyses were conducted with a Minitab macro (Threeway, written by J. S. Heywood), which performs hierarchical G tests for all terms in a log-linear model (Sokal and Rohlf, 1995
). All statistical conclusions were based on a Type I error rate of 0.05. All analyses of total seed number per flower and percentage seed set per flower yielded qualitatively identical results, so only analyses of percentage seed set are reported.
Unfertilized ovules were not difficult to detect, but there is always the possibility that they were undercounted due to reabsorption or dessication. If such a counting bias existed, then aborted fruits would appear to have fewer total ovules than mature fruits, and mature fruits with lower seed set would appear to have fewer total ovules than mature fruits with higher seed set. This, in turn, would influence the experimental results since seed set would be overestimated with the bias being greater for fruits with lower seed production. To test for such a bias, two separate ANOVAs were conducted. The first examined the effects of flower treatment and fruit production (scored as yes/no) on the mean total number of ovules counted from flowers of treatment plants. The second ANOVA examined the effects of fruit production and plant treatment on the mean total number of ovules counted in nonsupplemented flowers on all plants. In both analyses, all factors were fixed and only main effects were tested.
Fruits were collected from both supplemented and nonsupplemented flowers on treatment plants in hopes that differences among individual plants could be controlled statistically using a repeated-measures analysis, thereby increasing statistical power. However, this approach would be invalid if manipulations involved in pollen supplementation affected either fertilization success, seed set, or fruit maturation of nonsupplemented flowers on the same plant. To test for such effects, seed set, fertilization success, and fruit maturation rates for nonsupplemented flowers were compared between treatment plants and control plants. ANOVAs were used to examine fertilization success and seed set, with plant treatment and site as crossed, fixed factors and individual plant as a random factor nested under both treatment and site. A three-way contingency table analysis was used to examine the relation between fruit set, plant treatment, and site. For this analysis, individual flowers were used as the experimental units, with fruit set recorded as yes/no and flowers from different plants combined. The pattern of dependence between the three variables was decomposed into log-linear components (Sokal and Rohlf, 1995
), in which the effects of plant treatment on fruit set are partitioned into a two-way interaction between fruit set and plant treatment, plus a three-way interaction between fruit set, plant treatment, and site. Because some fruits were not recovered, this analysis was repeated three times with the missing fruits either included as aborted fruits, included as mature fruits, or excluded from the analysis entirely. Results from all three analyses followed the same pattern and so only the results obtained by including missing fruits as aborted fruits are reported.
No significant differences were found between control plants and treatment plants in the mean fertilization success, seed set, or fruit set of nonsupplemented flowers (see RESULTS). Therefore, these three measures of reproductive success were compared between nonsupplemented and supplemented flowers on treatment plants. A three-way contingency table analysis was used to examine the relation between fruit set, flower treatment, and site using the same approach described previously. For fertilization success and seed set, the effects of flower treatment were assessed by a repeated-measures ANOVA, with individual plant as a random factor nested under site and plant and site both crossed with flower treatment. This is a split-plot design, with each individual plant defining a main plot and flower treatments defining subplots. As a consequence, no appropriate error term was available for testing plant effects, nor is there any interest in such a test since genotype is confounded with local environment across each population. Flowering date (days after 1 January) was included as a covariate in case there was a temporal trend in pollinator activity. Several simpler ANOVAs were conducted in order to make multiple comparisons among the three flower treatments (nonsupplemented, supplemented first-night, supplemented second-night). The effects of flower treatment on fertilization success and seed set were examined separately for each site, with plant included as a random, crossed factor. Tukey's test was used for pairwise comparisons among flower treatments.
A MANOVA was conducted using the GLM procedure to make comparisons between the three populations for the number of initial flowering buds per plant, the number of stems per plant, the number of flowers produced, local plant density, and local flowering plant density. As the MANOVA was significant (Wilk's F = 3.966, df = 8, 182, P = 0.001), one-way ANOVAs were used to make comparisons among the populations separately for each variable.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Fruit set
Fruit production was significantly dependent on both flower treatment and site (Table 7). Based on the hierarchical log-linear model, the simplest model that fits the data is one of conditional independence between flower treatment and site (G = 11.14, df = 8, P = 0.194; Sokal and Rohlf, 1995
). Fruit set was 100% in all populations for second-night supplemented flowers and 80% in all populations for supplemented first-night flowers (Fig. 2). However, fruit set for nonsupplemented flowers varied from a low of 35% at Busiek to a high of 83% at Mincy (Fig. 2). At Henning and Mincy, there appear to have been no differences in fruit set between nonsupplemented and first-night supplemented flowers. On the other hand, fruit set at Busiek appears to have responded to first-night supplementation with increased fruit set (Fig. 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Several differences among the populations could account for the among-site differences in the degree of pollination limitation. Differences in pollination limitation presumably reflect differences in pollinator activity levels (Campbell, 1987
; Johnston, 1991
). Differences in pollinator activity levels may, in turn, be caused by differences in plant population size (Jennersten, 1988
; Lamont, Klinkhamer, and Witkowski, 1993
), differences in the size of the total floral display (Rathcke, 1983
; Stephenson and Bertin, 1983
; Groom, 1998
; Bosch and Waser, 1999
), or differences in forest canopy cover (Walters and Stiles, 1996
). The Henning population, where significant pollination limitation was not observed, is a large, continuous population located on high-quality glade habitat. This site currently has little encroachment by woody species, resulting in an open population with a very large floral display. At Mincy, pollination limitation was intermediate. This is a small population that is devoid of woody species. Both conspecific plant and flowering plant density were highest in this population. Thus, despite the small total number of plants, the high density and openness of this population may have made it attractive to pollinators. Finally, the Busiek population is located on a glade with heavy encroachment by woody species. In this population, pollination limitation was greatest, with nonsupplemented flowers having very low seed and fruit set. Woody encroachment at this site has effectively divided what once may have been a continuous population into smaller patches. Furthermore, plants produced significantly fewer flowers here than at the other two sites. Thus, although local plant and flowering plant densities were not significantly different from those at Henning, the patchiness of the habitat in combination with fewer flowers produced per plant resulted in a smaller floral display, which may have been less attractive to pollinators.
If a plant is experiencing resource limitation in addition to pollination limitation, then increased fruit or seed set of supplemented flowers may come at the expense of nonsupplemented flowers on the same plant (Lee, 1988
, and references therein). This would result in lower seed and fruit set of nonsupplemented flowers on treatment plants as compared to control plants. However, seed and fruit set were not significantly different between these two groups. Furthermore, the total number of ovules produced by flowers was not different among plant or fruit treatments, suggesting that supplementation of some flowers did not result in the absorption of ovules in nonsupplemented flowers.
Resources, and not pollinators, have sometimes been found to be the primary limitation to female reproduction (Stephenson, 1981
; Lee, 1988
), and even plants experiencing pollination limitation may become limited by resources when sufficient pollen is available (Campbell and Halama, 1993
; Corbet, 1998
). Although this study did not directly test for resource limitation, the fact that seed set was lower than fertilization success, even after supplementation, suggests that resources were limiting. This is not surprising since the glade habitat is typified by desert-like conditions and little to no topsoil (Nelson, 1985
). Fruit set, however, was apparently not resource limited as only one mature seed per fruit was required for fruit production despite the potential for an average of 83.2 seeds per fruit. The apparent lack of selective abortion of few-seeded fruits may indicate that resources do not limit fruit production per flower.
Fertilization success of <100% after supplementation suggests that resources were not the only source of limitation to seed set by supplemented flowers. Self-pollen can limit reproduction in self-incompatible plants by covering the stigmatic surfaces and preventing access to ovules by compatible pollen. Self-pollen was found to limit reproduction in Oenothera speciosa (Wolin, Galen, and Watkins, 1984
) and Oenothera fruticosa (Silander and Primack, 1978
). Flowers of O. macrocarpa in this study often had self-pollen on the stigma in varying amounts immediately after flower opening (J. M. Moody-Weis, personal observation), potentially preventing compatible, outcross pollen from reaching the stigma. Cross-incompatible or nonviable pollen in the pollen mixture used for supplementation could also have prevented compatible pollen tube growth. Although stigmas were believed to be saturated with pollen, it is possible that reduced fertilization success was due to the use of insufficient quantities of pollen (Young and Young, 1992
). Alternatively, too much pollen may have been deposited, resulting in the mutual interference of pollen tubes preventing the fertilization of all ovules (Young and Young, 1992
). Finally, peak stigma receptivity may have been missed (Young and Young, 1992
). Low stigma receptivity may explain the reduced effectiveness of pollen supplementation for second-night flowers.
Seed and fruit predation may limit reproduction even if no other limiting factors exist (Ehrlén, 1992
; Bigger, 1999
). However, neither seed nor fruit predation was observed during this study prior to fruit maturation, although two fruits were lost to rodent predation at Henning after fruits were mature. Even in the unlikely event that ovules or seeds were removed by a predator that went undetected, predation would not explain the incomplete fertilization success or seed set that was observed because these were based on the total number of ovules remaining within mature fruits, not the number present at flower initiation.
Despite fitting the hawk moth pollination syndrome, closer examinations in several species of Oenothera have revealed mixed-pollination systems (Wolin, Galen, and Watkins, 1984
; Barthell and Knops, 1997
). If a mixed-pollination system occurs in O. macrocarpa, visitation by non-hawk-moth pollinators would be most likely to occur during the day after flower opening. Small bees were observed visiting plants in the morning, and Nonnenmacher (1999)
reports similar observations. It may be possible for these small bees to effect cross-pollination. However, they were not observed to contact the stigmas. To determine whether diurnal species could effect successful pollination, the period of stigma receptivity would need to be established.
There are two general explanations for the existence of pollination limitation. First, the production of excess ovules may be an adaptive strategy that allows individuals to adjust their reproductive output in response to unpredictable variations in pollinator densities, or behaviors (Bierzychudek, 1981
; Stephenson, 1981
; Hainsworth, Wolf, and Mercier, 1985
; Lee, 1988
; Ayre and Whelan, 1989
; Ackerman and Montalvo, 1990
; Johnston, 1991
; Young and Young, 1992
; Burd, 1994
). Alternatively, recent habitat degradation may have reduced pollinator densities relative to the evolutionary history of the plant species, so that the plant reproductive strategy is no longer matched to the pollinator community (Sih and Baltus, 1987
; Spears, 1987
; Jennersten, 1988
; Sowig, 1989
; Johnston, 1991
; Aizen and Feinsinger, 1994
). Under both explanations, in years of pollinator scarcity the degree of pollination limitation is expected to vary among plant populations according to their quality as a resource for pollinators. The fact that the variation in site quality among the three populations is largely a consequence of recent human activities suggests that habitat degradation is a viable explanation for pollination limitation in O. macrocarpa. On the other hand, the lack of selective abortion of few-seeded fruits may be an adaptation to take advantage of low levels of pollinator activity, suggesting a history of unpredictable pollinator environments. Epilobium canum, another Onagraceae, also matures few-seeded fruits (Snow, 1986
). Furthermore, many Onagraceae, including O. macrocarpa, have viscin threads that hold together a large number of pollen grains (Cruden and Jensen, 1979
), which may be an adaptation to take advantage of infrequent pollination.
Thus, the results of this study are consistent with pollination limitation being either a manifestation of a bet-hedging strategy or a consequence of recent habitat degradation and subsequent pollinator decline or both. Examination of pollination limitation over several years would help to establish the relative importance of these two explanations. At one extreme, a bet-hedging strategy as an exclusive explanation would be suggested if natural pollination levels varied consistently among years, with reproduction not being pollination limited in some years. At the other extreme, a recent reduction in pollinator activity would be suggested if pollination limitation remained consistently high across years, potentially raising conservation concerns about the species. For O. macrocarpa, we hypothesize that reality lies somewhere between these two extremes.
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FOOTNOTES |
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2 Author for reprint requests, current address: Department of Ecology and Evolutionary Biology, University of Kansas, 1200 Sunnyside, Lawrence, Kansas, 66045 USA (jmweis{at}mail.ukans.edu
).
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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