Diane R. Campbell

POLLEN LIMITATION OF PLANT REPRODUCTION: ECOLOGICAL AND EVOLUTIONARY CAUSES AND CONSEQUENCES

Determining whether seed production is pollen limited has been an area of intensive empirical study over the last two decades. Yet current evidence does not allow satisfactory assessment of the causes or consequences of pollen limitation. Here, we critically evaluate existing theory and issues concerning pollen limitation. Our main conclusion is that a change in approach is needed to determine whether pollen limitation reflects random fluctuations around a pollen–resource equilibrium, an adaptation to stochastic pollination environments, or a chronic syndrome caused by an environmental perturbation. We formalize and extend D. Haig and M. Westobys conceptual model, and illustrate its use in guiding research on the evolutionary consequences of pollen limitation, i.e., whether plants evolve or have evolved to ameliorate pollen limitation. This synthesis also reveals that we are only beginning to understand when and how pollen limitation at the plant level translates into effects on plant population dynamics...

Landscape approaches to historical and contemporary gene flow in plants.

Growing interest in metapopulation dynamics and dispersal at a landscape level is promoting new approaches to the study of contemporary gene flow. These approaches have been fostered by the development of new genetic markers and statistical methods, as well as an awareness that contemporary gene flow cannot be reliably estimated by conventional methods based on genetic structure. Estimation of the spatial and temporal dynamics of pollen and seed movement with respect to extant landscape features can aid evolutionary and conservation biologists in predicting the demographic and genetic responses of species to naturally occurring or human-mediated population subdivision.

Resource and Pollen Limitations to Lifetime Seed Production in a Natural Plant Population

Using experimental manipulations, we examined pollen and resource limitations to seed production and their interaction in a natural population of a monocarpic plant, Ipomopsis aggregata. Our design cross two factors, pollen level (hand—pollinated or control) and resource level (water added, water and fertilizer added, or control). Both hand—pollination and fertilizing during the blooming season increased total seed production, while watering alone has no effect on any component of reproductive success. Hand—pollination boosted number of seeds per flower, with no effect on flower number. In contrasts, fertilizing had its primary effect on the number of flowers produced, while also increasing the number of seeds per mature fruit in hand—pollinated plants. Fertilizing increased nectar volume, but path analysis detected no indirect effect of this increased reward rate on seed production, suggesting instead that fertilizing has a slight, but direct, effect on seeds per flower. These results argue against a strict dichotomy between pollen limitation and resource limitation of female reproductive success in plants.

Components of phenotypic selection : pollen export and flower corolla width in Ipomopsis aggregata

In the hummingbird‐pollinated herb Ipomopsis aggregata, selection through male function during pollination favors wide corolla tubes. We explored the mechanisms behind this selection, using phenotypic selection analysis to compare effects of corolla width on two components of male pollination success, pollinator visit rate and pollen exported per visit. During single visits by captive hummingbirds, flowers with wider corollas exported more pollen, and more dye used as a pollen analogue, to stigmas of recipient flowers. Corolla width was less strongly related to visit rate in the field, and had no direct effect on visit rate after nectar production and corolla length were controlled for. Moreover, the phenotypic selection differential was 80% higher for the effect on pollen exported per visit, suggesting that this is the more important mechanism of selection.

The Mechanism of Competition for Pollination between Two Forest Herbs

The primary mechanism of competition for pollination between the two forest herbs Stellaria pubera and Claytonia virginica in piedmont North Carolina is interspecific pollen movement. The most common visitor, the bee fly Bombylius major, forages indiscriminately among flowers of the two species. In only one of five experiments did the presence of C. virginica reduce the pollinator visit rate per S. pubera flower, and in other experiments addition of C. virginica enhanced visit rate. Thus these plant species exhibit little or no competition through pollinator preference. In some natural populations, however, visits to S. pubera are frequently immediately preceded by a visit to C. virginica, and a flower receives less conspecific pollen and produces fewer seeds following such an interspecific visit than if the visitor has arrived directly from a conspecific flower. Interspecific pollen movement is responsible for most, if not all, of the reductions in seed set of S. pubera due to pollinator sharing. Although insects deposit a substantial amount of S. pubera pollen on stigmas of C. virginica, little C. virginica pollen is found on S. pubera stigmas. Moreover, application of foreign pollen to the stigma does not influence seed production of S. pubera. The effect of interspecific pollen movement is due to loss of conspecific pollen, not stigmatic interference.

THE CONSEQUENCES OF FLORAL HERBIVORY FOR POLLINATOR SERVICE TO ISOMERIS ARBOREA

Flower-feeding insects may reduce the reproductive success of their host plant in subtle ways that go beyond a direct reduction in gametes. Pollinators may respond to floral damage by visiting damaged plants at lower rates. Fewer visitations to the plant may result in fewer flowers that receive pollinator service and as a consequence lead to lower male and/or female reproductive success. In a two-year study, we examined the direct effect of flower predation by Meligethes rufimanus on the floral display of Isomeris arborea, and the indirect effect of herbivory on pollinator behavior. Plants exposed to herbivore attack produced fewer functional inflorescences than plants protected from herbivory. Undamaged flowers produced three times as much nectar per flower as damaged flowers. Likewise, protected plants had over twice as many anthers per flower as exposed plants. Pollinators responded by visiting damaged flowers less, and exposed plants had lower flower visitation rates than protected plants. Pollinators also visited patches of protected plants more frequently than exposed patches. These results show that floral herbivory reduces pollinator service and thus may reduce reproductive success indirectly, as well as through the direct consumption of viable gametes.

Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica

We measured the pollination effectiveness and visitation rates of major insect visitors of Claytonia virginica, an obligately insect-pollinated spring wildflower, in a North Carolina deciduous forest. Seed set in the population was not pollinator-limited except during rainy weather and very early in the flowering season. The solitary bee Andrena erigeniae and the bee fly Bombylius major were responsible for more than 75% of the visits to C. virginica. Andrena erigeniae is a specialist on C. virginica, while B. major is a common visitor to many plant species. We measured the effectiveness of a pollinator by the probability that a visit resulted in fruit (capsule) formation. For those flowers that were successfully pollinated and thus produced a capsule, number of seeds did not vary with visitor identity or the total number of visits received. Although B. major and female A. erigeniae differ greatly in morphology and foraging behavior, a visit by either insect results in equally high seed set. As B. major is about two-thirds as abundant as A. erigeniae females on C. virginica, both insects contribute substantially to seed set in our population. With the visitation frequency and pollination effectiveness we measured, the generalist B. major alone has the potential to pollinate three-quarters of the flowers.

Analyzing Pollinator-Mediated Selection in a Plant Hybrid Zone: Hummingbird Visitation Patterns on Three Spatial Scales

Clines across hybrid zones can be produced by several forms of natural selection. We illustrate an approach to studying pollinator-mediated selection in plant hybrid zones, using two species of Ipomopsis (Polemoniaceae) as a model system. We measured visitation to flowers in natural and experimental populations by two major types of pollinators, hummingbirds and hawkmoths, at up to three different spatial scales. Using measures of pollinator visitation, we calculated phenotypic selection gradients and characterized the form of selection in the hybrid zone. Hummingbirds overvisited Ipomopsis aggregata compared with Ipomopsis tenuituba and morphological hybrids at all spatial scales, especially the largest scale of kilometers. These responses may depend in part on the presence of other hummingbird-visited plants in the community. Hummingbird behavior produced directional selection favoring wide corolla tubes and intense red coloration. Hawkmoths, in contrast, overvisited plants with narrow corolla tubes. When both types of pollinators were present, corolla width experienced disruptive selection, consistent with a model of hybrid disadvantage. In the natural hybrid zone, however, hawkmoths are rare participants. In most years plants experience visitation from hummingbirds alone. Thus, selection by pollinators usually fits an advancing wave model in which traits characteristic of I. aggregata are favored everywhere. Modeling the evolution of clines in response to such pollinator-mediated selection will require further theoretical development that allows for selection intensity to vary with spatial scale and with the abundance of unrelated plants visited by the same pollinators.

Pollinator Sharing and Seed Set of Stellaria pubera: Competition for Pollination

I used field experiments to examine the effect of pollinator sharing on seed set in the understory herb Stellaria pubera. In piedmont North Carolina the solitary bee and fly pollinators of this species are also frequent visitors to Claytonia virginica. Removals of nearby flowers of C. virginica increased seed set of S. pubera. Examination of seed set in populations of potted plants indicated that the effect was due to the change in species composition rather than plant density. Variation in seed production was high, however, and even when flowers were provided with excess pollen through supplemental hand pollinations, only 20% of ovules produced seeds. Competition for pollination appears to be one of several selective forces that act on blooming time of S. pubera. Stellaria pubera blooms slightly later than C. virginica. Whereas the seed set of early flowers was increased 13% by removal of C. virginica and 19% by hand pollination, seed set of late flowers was unaffected. Plants forced to bloom early also tended to be more pollinator-limited than control plants. Removal of C. virginica did not, however, increase the seed set of S. pubera plants forced to bloom early significantly more than that of control plants. Other forces are probably also involved in the maintenance of blooming time.

Effects of Floral Traits on Sequential Components of Fitness in Ipomopsis aggregata

The total number of viable, undamaged seeds released by a plant provides an estimate of female reproductive success (RS). I outline a method for analyzing pollinator-mediated selection based on partitioning female RS into four multiplicative components: number of flowers, pollen received per flower, number of seeds set per grain of pollen received, and number of undamaged seeds per seed set. I measured these fitness components for individual plants in several populations of Ipomopsis aggregata and estimated the life-cycle components of selection differentials. Plants whose flowers had highly exserted stigmata and spent a high proportion of time in the pistillate phase received more pollen per flower, as estimated by tracking dye. Experimental hand-pollinations showed that female RS was strongly limited by low levels of pollen, confirming the results of other studies. In spite of this pollen limitation, within natural populations female RS did not increase with mean pollen received per flower. Of the four multiplicative fitness components, only number of flowers and number of seeds set per grain of pollen correlated positively with female RS. As a result, even though hummingbirds exerted significant selection through female function, net selection was not predictable from pollination success alone. Instead, selection was modified by events during flower production, seed formation, and predispersal seed predation. Net selection on proportion pistillate was stabilizing. Selection on flowering date reversed direction over the life cycle, but net selection strongly favored early blooming. Selection on corolla length varied from year to year, which may help explain the high level of phenotypic variation. The relationships between fitness components differed depending on whether I compared flowers within plants, plants within populations, or population means. Failure to take plant and population identity into account can lead to false detection of selection when none is present.