Pollinator Visitation Rates Research Articles

Pollinator Visits to Threatened Species Are Restored Following Invasive Plant Removal

An indirect consequence of plant invasions is the disruption of native plant-pollinator interactions. We examined effects of invasive baby’s breath (Gypsophila paniculata) and spotted knapweed (Centaurea maculosa) on floral visitors to federally threatened Pitcher’s thistle (Cirsium pitcheri) in Lake Michigan dunes. In sweep net surveys, abundances of pollinator taxa were five times higher in invaded than in naturally invader-free sites. However, plot-level G. paniculata removal treatments increased pollinator visits to C. pitcheri relative to invaded plots and restored visitation to levels found in naturally uninvaded plots. Invader removal also increased native plant species richness, which was positively correlated with pollinator visitation to C. pitcheri, suggesting an indirect effect on pollinators mediated through invader-altered plant composition. In temporary floral arrays, the rate of pollinator visitation to C. pitcheri was not affected by neighbor plant species identity. However, compared with native Monarda punctata, invasive C. maculosa attracted more total pollinators to the array but reduced the proportion of total visits that were to C. pitcheri and increased pollinator movements between plant species. While both G. paniculata and C. maculosa appear to act as magnet species by attracting more pollinators at the plot level, these invaders have the potential to reduce reproduction of C. pitcheri by decreasing pollinator visits and increasing interspecific pollen transfer.

Population size, pollination and reproductive success in two endangered Genista species

Habitat fragmentation often leads to small and isolated plant populations as well as decreased habitat quality. These processes can fundamentally disrupt the interactions between plants and pollinators and decrease reproductive success. This concerns especially self-incompatible, non-clonal species that depend on pollination for successful reproduction.In two rare and endangered heathland plant species, Genista anglica and G. pilosa, we examined pollination and reproduction in relation to population size. Eight populations of G. anglica and ten populations of G. pilosa were surveyed in the vicinity of Bremen, NW-Germany. We counted the visits of pollinators (honeybees, bumblebees, and other insects) and determined the reproductive output of the observed shoots.Contrary to our expectation to find increased pollinator visitation rates in larger populations of both Genista species, the number of flower-visiting insects was unrelated to the number of flowering shoots. Increasing shoot length had a positive and increasing temperature a negative impact on the number of visiting honeybees and bumblebees. Despite the general absence of population size effects on pollinator numbers, the number of fruits and seeds in G. anglica increased with increasing population size. Fruit and seed set in G. pilosa were negatively related to the number of ‘other insects’. Our field observations showed that larger populations of both Genista species flowered earlier than smaller populations and much earlier than reported in the literature. Flowering in large populations therefore tends to coincide less well with pollinator abundance, and this may cause a disruption of the temporal coincidence between flowering phenology and pollinator activity.

Does spatial population structure affect seed set in pollen-limited Thymus capitatus?

Plant population size has been shown to affect insect visitation and reproductive success. Small populations are at risk because individuals are more likely to be affected by stochastic processes and inbreeding depression (Allee effect). Additionally, several studies have found that plants in small populations also experience lower pollinator visitation rates, which may further decrease reproduction. In this study, seed set, pollinator visitation and pollen limitation of Thymus capitatus (L.) was assessed in 32 patches in eight populations of various sizes on the island of Lesvos, Greece. All populations except one were significantly pollen-limited. We found that although free-pollinated flowers produced more seeds in larger populations this was not due to higher pollinator visitation rates as flowers which received pollen supplements also produced more seeds in larger populations. We hypothesize that the higher seed set is due to a generally greater genetic variability or better habitat quality. We show that honeybee visitation alone significantly decreases pollen limitation.

Breeding system and factors limiting fruit production in the nectarless orchid Broughtonia lindenii

Low fruit set values in most orchids (especially epiphytic and tropical species) are normally thought to be the consequence of pollination constraints and limited resources. In particular, pollination constraints are modulated by pollinator visitation rates, pollinator visitation behaviour (promoting crossing or selfing), the type and number of pollinia deposited on stigmas (in the case of orchids with subequal pollinia) and the amount of pollen loaded per inflorescence. In order to assess to what extent these factors can affect fruit set in specific orchid-pollinator systems, the repercussions of some of these aspects on reproduction of Broughtonia lindenii were examined in a coastal population in western Cuba. The study focused on plant breeding system, importance of pollen load and type of pollinia on subsequent fruit and seed, limiting factors of seed production and interaction with pollinators. This species presents long-lasting flowers that senesce after all forms of effective visit. Pollinator dependence for fruit production was demonstrated, while hand-pollination experiments revealed self-compatibility and inbreeding depression at seed level. More pollinia on stigmas enhance the proportion of well-developed seeds. In contrast, the pollinia type used in pollination is not important for seed quality of fruits, suggesting that small pollinia are not rudimentary. Natural fruit set in two consecutive years was substantially affected by pollinator activity, and also by systematic depredatory activity of ants and a caterpillar. Considering that this orchid completely lacks nectar and that the local assemblage of pollinators and predators influenced its reproduction, a minor importance of resource constraints in this epiphyte (with long-lasting reserve structures) is confirmed at least for a short time.

Florivores decrease pollinator visitation in a self-incompatible plant

Different biotic interactions may influence one another to produce complex patterns of direct and indirect effects, which together influence plant reproductive success. However, so far most studies on plant-animal interactions have focused on single interactions in isolation. In this study, we studied the effect of florivory by the weevil Cionus nigritarsis on pollinator visitation rate in the self-incompatible perennial herb Verbascum nigrum by combining observations of florivory and pollination in natural populations with records of pollinator visitation to plants with different levels of experimentally inflicted damage. Increasing levels of damage through either natural or simulated florivory resulted in fewer pollinator visits per plant and per flower. As expected, the magnitude of the indirect effect of florivory on pollinator visitation was proportional to the intensity of florivory. Our results indicate that biotic non-pollinating agents, such as florivores, may induce substantial changes in pollinator availability. Therefore, studies addressing different plant-animal interactions in parallel are necessary to better comprehend the factors influencing the reproductive performance and demography of flowering plants.

Change in floral orientation in Anisodus luridus (Solanaceae) protects pollen grains and facilitates development of fertilized ovules

Some floral traits could be selected by pollinators and nonpollinator agents, and studying the floral traits shaped by physical agents could reveal adaptive mechanisms to the environment. We explored the adaptive significance of the change in floral orientation, from pendulous flowers to erect fruits that have a persistent calyx, in Anisodus luridus, a perennial native to the Qinghai-Tibet Plateau (QTP). • We examined the effect of flower orientation on pollinator visitation rates, pollen deposition efficiency, pollen quantity, and pollen viability to estimate whether pendulous flowers have improved male fitness. We then measured seed production and seed germination rate to assess whether erect fruits have enhanced female fitness. • Pendulous flowers did not have any preferred pollinators or increased pollen deposition. In artificially erected flowers, the number of pollen grains greatly decreased after rainwash. Pollen germination experiments indicated that pollen damage by water and exposure to solar radiation is serious. In the persistent calyx that holds water within it, the temperature inside the calyx changed slower than in the calyx that had the water removed. After supplemental pollination, the seed number, seed set, and seed mass of fruits that had water removed from the calyx were reduced greatly in both years. • We conclude that the change in floral orientation could enhance male and female fitness of A. luridus and is effectively adaptive to the alpine environments, indicating a strong selection by the combined pressure from various abiotic nonpollinator agents in shaping the floral traits of this alpine plant.

Relationship between reproductive assurance and mixed mating in perennial Kosteletzkya virginica

Recent works have shown that mixed mating systems often evolve despite strong inbreeding depression and reproductive assurance, which is one of the widely accepted explanations for the evolution of selfing. However, there have been few empirical studies on the relationship between mixed mating and reproductive assurance in perennial plants. In the herbaceous perennial, Kosteletzkya virginica, delayed selfing induced from context-dependent style curvature offers reproductive assurance, and adverse weather conditions significantly reduce pollinator visitation rates. In this study, our goals were (i) to experimentally evaluate pollinator failure rate, reproductive assurance, selfing rate and the relationships between them, and (ii) to measure inbreeding depression across multiple growth seasons. Results indicate that both population selfing rates and reproductive assurance are significantly and positively correlated with field estimates of pollinator failure rates, and there is a strong relationship between selfing rates and reproductive assurance. Inbreeding depression across multiple growth seasons ranged from 0.621 to 0.665, and there were no significant differences among different seasons. Our data demonstrates that a mixed mating system is beneficial because frequent pollinator failure has allowed reproductive assurance to evolve through delayed selfing which minimizes the risk of seed discounting and is still advantageous despite high inbreeding depression.

The role of volatile organic compounds, morphology and pigments of globeflowers in the attraction of their specific pollinating flies

• Floral scents and visual cues of the globeflower Trollius europaeus may play a key role in the attraction of Chiastocheta flies, involved in a highly specific nursery pollination mutualism. • Here, headspace collection and GC-MS were used to identify and quantify the volatile organic compounds emitted by the globeflower. • Scents are produced in three different floral parts by four structures: secretory glands and flat epidermis cells in the abaxial sepal epidermis, conical cells in the adaxial sepal epidermis, and pollen. The blend is made up of 16 compounds commonly found in floral scents. Geographical variation among populations is low compared with variation amongst individuals within populations. Electroantenno-graphic analyses revealed that six compounds emitted by both anthers and sepals are detected by Chiastocheta flies. Removing the anthers hidden inside the globe from flowers in the field decreased the number of fly visits to globeflowers. • A multivariate analysis of the effect of several floral traits on pollinator visitation rate conducted in the field showed that both floral scents and visual flower cues play a role in pollinator attraction. However, their relative roles and the intensity of the selective pressures exerted on floral traits by pollinators appear to vary in time and space.

Reproduction of Echinacea angustifolia in fragmented prairie is pollen‐limited but not pollinator‐limited

Pollen limitation of plant reproduction occurs in many plant species, particularly those in fragmented habitat; however, causes of pollen limitation are often unknown. We investigated the relationship between pollen limitation and pollinator visitation in the purple coneflower, Echinacea angustifolia (Asteraceae), which grows in the extremely fragmented tall grass prairie of North America. Previous investigations showed that pollen limitation of E. angustifolia increases with plant isolation and decreases with population size. We observed insect visitation to E. angustifolia over two flowering seasons and estimated pollen limitation of observed plants, using seed set as a proxy measure in 2004 and persistence of receptive style rows in 2005. We analyzed spatial patterns of bee visitation and pollination at two spatial scales: individual isolation, as measured by the distance to their kth nearest flowering neighbors (k = 1 - 15), and population size. Our results indicate that E. angustifolia is pollinated by over 26 species of native bees, with 70-75% of visits by halictid bees. Surprisingly, in both years, bee visitation increased with isolation of individual plants and did not vary significantly with population size. As expected, plant isolation increased pollen limitation and lowered seed set. There was no effect of population size on seed set in 2004, and pollen limitation decreased nonsignificantly with population size in 2005. We conclude that pollen receipt limits reproduction in E. angustifolia, but pollinator visitation does not. Remarkably, isolated plants simultaneously have increased rates of pollinator visitation by pollinators and decreased reproduction. We discuss alternative explanations of pollen limitation that are consistent with this apparent discrepancy, including a decline in the availability of compatible conspecific pollen with increased plant isolation.

Pollen dispersal in an insect-pollinated wet meadow herb along an urban river

Abstract Urban sprawl has led over wide areas to alteration and fragmentation of so many ecosystem types that it becomes essential to consider biodiversity conservation in urban planning. As the urbanisation is usually irreversible, the urban context has to be taken into account when defining appropriate management measures to sustain viable populations. Connectivity through pollen flow appears to be a key-factor for the long-term persistence of populations of insect-pollinated plant species. We investigated pollen dispersal using fluorescent dye as pollen analogue in Lychnis flos-cuculi , an insect-pollinated wetland herb, along the Woluwe River, in Brussels urban zone (Belgium). Dye dispersal showed an exponential decay distribution, with particles mainly deposited on neighbouring individuals and populations. The mean distance of dye transfer was 133.6 m, with a maximal distance of 523.7 m. Dye deposition was positively related to the number of potential recipient plants when distance to dye source was held constant. This may be associated with a higher flowering plant density across the flying distance that increases attractiveness and visitation rate of pollinators, and/or with secondary dye transfer. When connected, small and large populations only differed in response to the number of potential recipients. The small isolated population received little immigrant pollen flow, but remained a dye donor. Our study demonstrates that small populations of L. flos-cuculi along an urban river may still exchange pollen thanks to pollinator movements, and might therefore be regarded in management planning as potential connecting components between populations.

Shading by invasive shrub reduces seed production and pollinator services in a native herb

Plant invasions disrupt native plant reproduction directly via competition for light and other resources and indirectly via competition for pollination. Furthermore, shading by an invasive plant may reduce pollinator visitation and therefore reproduction in native plants. Our study quantifies and identifies mechanisms of these direct and indirect effects of an invasive shrub on pollination and reproductive success of a native herb. We measured pollinator visitation rate, pollen deposition, and female reproductive success in potted arrays of native Geranium maculatum in deciduous forest plots invaded by the non-native shrub Lonicera maackii and in two removal treatments: removal of aboveground L. maackii biomass and removal of flowers. We compared fruit and seed production between open-pollinated and pollen-supplemented plants to test for pollen and light limitation of reproduction. Plots with L. maackii had significantly lower light, pollinator visitation rate, and conspecific pollen deposition to G. maculatum than biomass removal plots. Loniceramaackii flower removal did not increase pollinator visitation or pollen deposition compared to unmanipulated invaded plots, refuting the hypothesis of competition for pollinators. Thus, pollinator-mediated impacts of invasive plants are not limited to periods of co-flowering or pollinator sharing between potential competitors. Geranium maculatum plants produced significantly fewer seeds in plots containing L. maackii than in plant removal plots. Seed set was similar between pollen-supplemented and open-pollinated plants, but pollen-supplemented plants exhibited higher seed set in plant removal plots compared to invaded plots. Therefore, we conclude that the mechanism of impact of L. maackii on G. maculatum reproduction was increased understory shade.

The structure and roles of sterile flowers in Viburnum macrocephalum f. keteleeri (Adoxaceae)

The formation and ecological roles of sterile flowers in flowering plants are interesting issues in floral biology and evolution. Here, we investigated the morphological and anatomical characteristics of both fertile and sterile flowers of Viburnum macrocephalum f. keteleeri, a self-incompatible and insect-pollinated shrub, during different developmental stages of flowers. In addition, pollinator visitation rates and fruit set were determined in intact inflorescences and those with sterile flowers removed. The results indicate that sterile and fertile flowers were developmentally similar during early developmental stages, and that development of the flower types diverged about 15 days before flowering. In addition, pollinator visitation rates, number of pollen grains on stigmas and fruit set were significantly higher in inflorescences with sterile flowers than those without sterile flowers. The results suggest that sterile flowers of this species evolved from fertile flowers under long-term selective pressure, and play a crucial role in enhancing reproductive success through effectively attracting pollinators to the plant and thus enhancing fruit set.

The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks

Striking changes in food web structure occur with alterations in resource supply. Like predator–prey interactions, many mutualisms are also consumer–resource interactions. However, no studies have explored how the structure of plant–pollinator networks may be affected by nutrient enrichment. For three years, we enriched plots of subalpine plant communities with nitrogen and observed subsequent effects on plant–pollinator network structure. Although nitrogen enrichment affects floral abundance and rates of pollinator visitation, we found no effects of nitrogen enrichment on the core group of generalist plants and pollinators or on plant–pollinator network structure parameters, such as network topology (the identity and frequency of interactions) and the degree of nestedness. However, individual plant and pollinator taxa were packed into the nested networks differently among nitrogen treatments. In particular, pollinators visited different numbers and types of plants in the nested networks, suggesting weak, widespread effects of nitrogen addition on individual taxa. Independent of nitrogen enrichment, there were large interannual differences in network structure and interactions, due to species turnover among years and flexibility in interacting with new partners. These data suggest that the community structure of small‐scale mutualistic networks may be relatively robust to short‐term bottom–up changes in the resource supply, but sensitive to variation in the opportunistic behavior and turnover of plant and pollinator species among years.

SELECTION ON VARIANCE IN FLOWERING TIME WITHIN AND AMONG INDIVIDUALS

We model the impact of pollinator visitation rate and behavior on the short-term evolution of population flowering phenologies determined by the distributions of flowering times within and among individual plants. Evolution of population flowering phenologies depends on the phenotypic variances and heritabilities of the within-individual mean and variance of flowering time. In the ecological scenarios we investigate selection does not produce a correlation of the mean and variance of individual flowering time. Self-incompatibility causes weak stabilizing selection on flowering time that acts to reduce the within-individual variance in flowering time. Disruptive selection due to pollinator limitation acts mostly to increase the among-individual variance in flowering time. Stabilizing selection due to pollinator attraction, or short reproductive season, acts mostly to decrease the within-individual variance in flowering time. Temporal autocorrelation of environmental stochasticity in pollinator visitation rate strongly selects to increase the within-individual variance in flowering time. These predictions can be tested by measuring the causal factors described above, partitioning the variance in population phenology within and among individuals, and estimating the inheritance of, and selection on, within-individual mean and variance of flowering time.

Variation in Pollination: Causes and Consequences for Plant Reproduction

Pollen dispersal by animals varies extensively because of differences in pollinator visitation rates among plants, dissimilar pollination by the various pollinators that visit individual plants, and stochastic variation in deposition as an individual pollinator disperses a plant's pollen to subsequently visited recipient flowers. Such variation reduces expected female and male success if seed production decelerates with increasing pollen receipt, because less than average receipt diminishes mean seed production more than copious pollination increases it (Jensen's inequality). We report empirical studies of the nature and magnitude of pollen dispersal variance, which provide the basis for a numerical model of the consequences of dispersal for expected seed production. Model fitting revealed that dispersal of Brassica napus pollen by bumblebees and especially butterflies exhibited much more variation than is expected of a binomial process and was best modeled as a beta-binomial process with a constant mean. Overdispersion arose primarily during pollen dispersal by individual insects, since differences between individuals of the same pollinator type were limited. Our model revealed variance limitation as a previously unrecognized, substantial, and ubiquitous component of pollen limitation of seed production. Variance limitation should select for floral traits that increase pollinator visitation, reduce dispersal variance, or reduce the postpollination nonlinearities that cause Jensen's inequality.

On the roles of colour and scent in a specialized floral mimicry system

Sexually deceptive orchids achieve cross-pollination by mimicking the mating signals of female insects, generally hymenopterans. This pollination mechanism is often highly specific as it is based primarily on the mimicry of mating signals, especially the female sex pheromones of the targeted pollinator. Like many deceptive orchids, the Mediterranean species Ophrys arachnitiformis shows high levels of floral trait variation, especially in the colour of the perianth, which is either green or white/pinkinsh within populations. The adaptive significance of perianth colour polymorphism and its influence on pollinator visitation rates in sexually deceptive orchids remain obscure. The relative importance of floral scent versus perianth colour in pollinator attraction in this orchid pollinator mimicry system was evaluated by performing floral scent analyses by gas chromatography-mass spectrometry (GC-MS) and behavioural bioassays with the pollinators under natural conditions were performed. The relative and absolute amounts of behaviourally active compounds are identical in the two colour morphs of O. arachnitiformis. Neither presence/absence nor the colour of the perianth (green versus white) influence attractiveness of the flowers to Colletes cunicularius males, the main pollinator of O. arachnitiformis. Chemical signals alone can mediate the interactions in highly specialized mimicry systems. Floral colour polymorphism in O. arachnitiformis is not subjected to selection imposed by C. cunicularius males, and an interplay between different non-adaptive processes may be responsible for the maintenance of floral colour polymorphism both within and among populations.

Breeding system and pollination ecology of introduced plants compared to their native relatives

Identifying how plant-enemy interactions contribute to the success of introduced species has been a subject of much research, while the role of plant-pollinator interactions has received less attention. The ability to reproduce in new environments is essential for the successful establishment and spread of introduced species. Introduced plant species that are not capable of autonomous self-fertilization and are unable to attract resident pollinators may suffer from pollen limitation. Our study quantifies the degree of autogamy and pollination ecology of 10 closely related pairs of native and introduced plant species at a single site near St. Louis, Missouri, USA. Most of these species pairs had similar capacities for autogamy; however, of those that differed, the introduced species were more autogamous than their native congeners. Most introduced plants have pollinator visitation rates similar to those of their native congeners. Of the 20 species studied, only three had significant pollen limitation. We suggest that the success of most introduced plant species is because they are highly autogamous or because their pollinator visitation rates are similar to those of their native relatives. Understanding and identifying traits related to pollination success that are key in successful introductions may allow better understanding and prediction of biological invasions.

Contrasting effects of plant population size on florivory and pollination

Abstract Changes in plant population size, induced by various forms of habitat degradation, can affect the performance of plants by altering their interactions with other organisms such as pollinators and herbivores. However, studies on plant reproductive response to variation in population size that simultaneously consider different interactions are rare. In this study, we examined (1) how levels of pollinator visitation and florivory vary with population size of a self-incompatible herb, Verbascum nigrum (Scrophulariaceae), (2) the relative effect of these two interactions on host seed set, and (3) whether the intensity of florivory influences pollinator visitation rate. The intensity of florivory increased, whereas pollinator visitation rate decreased with host population size. Although average seed production was negatively affected by the intensity of florivory, seed production was independent of population size. The direct negative effect of florivores on plant seed set was indirectly enforced by their negative effect on pollinator visitation rate. Our results emphasize the complexity of responses of different plant–animal interactions to plant population size. However, interactions involving specialized organisms are likely to disrupt first as plant population size decreases.

Changes in Sexual Expression as Result of Defoliation and Environment in a Monoecious Shrub in Mexico: Implications for Pollination

ABSTRACTFolivory may indirectly impact plant reproduction through changes in sexual expression (i.e., number or proportion of male and female flowers produced), which influence plant–pollinator interactions via changes in pollinator preference or efficiency. This study is an experimental evaluation of the effect that defoliation has on sex expression in the monoecious shrubCnidoscolus aconitifolius, how such effect varies across sites, as well as how such changes indirectly affect pollinator visitation rates. The present study used three populations ofC. aconitifolius, each one located in a different site in Yucatán (México): pasture, deciduous forest and subdeciduous medium height forest and three levels of defoliation: 50 percent, 100 percent, and a control (no damage). Results showed that defoliation reduced significantly the total number of male flowers produced in two of the sites. Defoliation did not impact female flower production or the proportion of female flowers produced. Finally, floral visit rates were not affected by defoliation via changes in sexual expression and neither by site or by the interaction site × defoliation. Findings showed that defoliation had an effect on sex expression inC. aconitifolius, although apparently this change did not affect the plant–pollinator interactions.

Displacement of flowering phenologies among plant species by competition for generalist pollinators

We model the evolution of allochronic isolation between sympatric animal-pollinated plant species via displacement of their flowering times. The plant species share generalist pollinators and either produce inviable hybrid seeds or do not hybridize at all. Displacement of flowering times between reproductively isolated species reduces competition for pollinators and the formation of inviable hybrid seeds. Under strong pollen limitation, competition for pollinators causes rapid evolution of allochronic isolation both for hybridizing and nonhybridizing species. Under weak pollen limitation, allochronic isolation evolves rapidly for hybridizing species but more slowly for nonhybridizing species. Positive density-dependent pollinator visitation rate at low flower densities facilitates allochronic isolation under weak pollen limitation. Allochronic isolation among sympatric species sharing generalist pollinators could be common under any intensity of pollen limitation if the flowering season is sufficiently long.