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.     

Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach

1.  Habitat fragmentation can affect pollinator and plant population structure in terms of species composition, abundance, area covered and density of flowering plants. This, in turn, may affect pollinator visitation frequency, pollen deposition, seed set and plant fitness.
2.  A reduction in the quantity of flower visits can be coupled with a reduction in the quality of pollination service and hence the plants' overall reproductive success and long-term survival. Understanding the relationship between plant population size and/or isolation and pollination limitation is of fundamental importance for plant conservation.
3.  We examined flower visitation and seed set of 10 different plant species from five European countries to investigate the general effects of plant populations size and density, both within (patch level) and between populations (population level), on seed set and pollination limitation.
4.  We found evidence that the effects of area and density of flowering plant assemblages were generally more pronounced at the patch level than at the population level. We also found that patch and population level together influenced flower visitation and seed set, and the latter increased with increasing patch area and density, but this effect was only apparent in small populations.
5.   Synthesis. By using an extensive pan-European data set on flower visitation and seed set we have identified a general pattern in the interplay between the attractiveness of flowering plant patches for pollinators and density dependence of flower visitation, and also a strong plant species-specific response to habitat fragmentation effects. This can guide efforts to conserve plant–pollinator interactions, ecosystem functioning and plant fitness in fragmented habitats.     

Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae)

Plant-pollinator interactions are one of the most important and variable mutualisms in nature. Multiple pollinators often visit plants and can vary in visitation rates, pollen removal and deposition, and spatial and temporal distribution, altering plant reproduction and patterns of pollinator-mediated selection. Although some visitors may not be effective pollinators, pollinator effectiveness is rarely estimated directly as seed set resulting from a single visit by each taxon visiting generalist plants. For two years, effectiveness of visitors to wild radish, Raphanus raphanistrum, was quantified by counting seeds set and pollen grains removed as a result of a single visit. We calculated a pollinator's importance to plant reproduction as the product of visitation rate and single-visit seed set, and regressed pollinator body size on pollen-removal and on seed set effectiveness. Although pollinators differed in effectiveness and visitation rates, pollinator importance was primarily determined by visitation rates. In contrast to similar 2-yr studies, pollinator assemblage composition varied little, suggesting pollinator-mediated selection can be consistent across years for this generalist. Larger pollinators were more effective than smaller at effecting seed set, but body size was a poor predictor of pollen removal ability. Instead, pollen-removal effectiveness may be more influenced by foraging behavior than size.     

Pollinators shift to nectar robbers when florivory occurs,with effects on reproductive success in Iris bulleyana (Iridaceae)

• Studies have indicated that florivory and nectar robbing may reduce reproductive success of host plants. However, whether and how these effects might interact when plants are simultaneously attacked by both florivores and nectar robbers still needs further investigation.
• We used Iris bulleyana to detect the interactions among florivory, nectar robbing and pollination, and moreover, their effects on plant reproductive success. Field investigations and hand‐pollination treatments were conducted on two experimental plots from a natural population, in which Experimental plot was protected from florivores and Control plot was not manipulated.
• The flower calyx was bitten by sawflies to consume the nectary, and three bumblebee species were pollinators. In addition, the short‐tongued pollinator, Bombus friseanus, was the only robber when there was a hole made by a sawfly. The bumblebee had significantly shortened flower handling time when robbing, as compared to legitimate visits. Pollinator visitation and seed production decreased significantly in damaged flowers. However, seed production per flower after supplementary hand‐pollination did not differ significantly between damaged and undamaged flowers. Compared to the Experimental plot, bumblebees visited fewer flowers per plant in a foraging bout in the Control plot.
• The flowers damaged by florivory allowed B. friseanus to shift to a nectar robber. Florivory and nectar robbing collectively decreased plant reproductive success by consuming nectar resources, which may reduce attractiveness to pollinators of the damaged flowers. However, the changes in pollinator behaviour might be beneficial to the plant by reducing the risk of geitonogamous mating.

     

Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.     

Pollinator Behavior Mediates Negative Interactions between Two Congeneric Invasive Plant Species

Simultaneously flowering plant species may indirectly interact with each other by influencing the quantity of pollinator visitation and/or the quality of pollen that is transferred. These effects on pollination may depend on how pollinators respond to floral resources at multiple levels. In this study, we demonstrate pollinator-mediated negative interactions between two invasive plants, Carduus acanthoides and Carduus nutans. Using constructed arrays of the two species, alone and in mixture, we quantified pollinator visitation at the patch and individual plant levels and measured seed production. We found that co-occurrence of our species led to a shift in pollinator services at both levels. Greater interference occurred when arrays were small and spacings between neighboring plants were large. A spatially explicit movement model suggests that pollinator foraging behavior, which mediates the interactions between plants, was driven by floral display size rather than species identity per se. Pollinator behavior significantly reduced the proportion of seed set for both species relative to that in single-species arrays. Overall, the dependence of pollinator behavior on patch size, spacing between plants, and patch composition can lead to pollinator-mediated plant interactions that range from facilitative to competitive.     

Factors affecting pollinator movement and plant fitness in a specialized pollination system

The rate of pollen exchange within and among flowers may depend on pollinator attraction traits such as floral display size and flowering plant density. Variations in these traits may influence pollinator movements, pollen receipt, and seed number. To assess how floral display size and flowering plant density affect parameters of pollinator visitation rate, pollen receipt per flower, seed number per fruit and the between-plant pollinator movements, we studied the self-incompatible plant, Nierembergia linariifolia. Per-flower pollinator visitation rate and bout length increased linearly with increasing floral display size. Pollen receipt per flower increased linearly with increasing flowering plant density. For seed number per fruit, a polynomial model describing an increased seed number per fruit at low density and a decreased seed number per fruit at high density provided a significant fit. Per-flower pollinator visitation rate was not associated with pollen receipt per flower and seed number per fruit. Bees visited plants located near to the center of the population more frequently than plants located at the periphery. Increases in both floral display size and flowering plant density led to an increased chance of a plant being chosen as the center of the pollinator foraging area. These results suggest that even though large floral displays and high flowering plant density are traits that attract more pollinators, they may also reduce potential mate diversity by restricting pollen movement to conspecific mates that are closely located.     

Plant reproductive strategies vary under low and high pollinator densities

Long‐term variation in the population density of honey bees Apis mellifera across landscapes has been shown to correlate with variation in the floral traits of plant populations in these landscapes, suggesting that variations in pollinator population density and foraging rates can drive floral trait evolution of their host plants. However, it remained to be determined whether this variation in plant traits is associated with adaptive variation in plant reproductive strategies under conditions of high and low pollinator densities. Here we conducted a reciprocal transplant experiment to examine how this variation in floral traits, under conditions of either high and low pollinator density, impacted seed production in the Tibetan lotus Saussurea nigrescens. In 2014 and 2015, we recorded the floral traits, pollinator visitation rates, and seed production of S. nigrescens populations grown in both home sites and foreign sites, where sites varied in honey bee population density. Our results demonstrated that the floral traits reflected those of their original population, regardless of their current location. However, seed production varied with both population origin and transplant site. Seed number was positively correlated with flower abundance in the pollinator‐rich sites, but with nectar production in the pollinator‐poor sites. Pollinator visitation rate was also positively correlated with flower number at pollinator‐rich sites, and with nectar volume at pollinator‐poor sites. Overall, the local genotype had higher seed production than nonlocal genotypes in home sites. However, when pollen is hand‐supplemented, plants from pollinator‐rich populations had higher seed production than plants from pollinator‐poor populations, regardless of whether they were transplanted to pollinator‐rich or ‐poor sites. These results suggest that the plant genotypic differences primarily drive variation in pollinator attraction, and this ultimately drives variation in seed: ovule ratio. Thus, our results suggest that flowering plant species use different reproductive strategies to respond to high or low pollinator densities.     

Edaphic factors and plant–insect interactions: direct and indirect effects of serpentine soil on florivores and pollinators

Edaphic factors can lead to differences in plant morphology and tissue chemistry. However, whether these differences result in altered plant–insect interactions for soil-generalist plants is less understood. We present evidence that soil chemistry can alter plant–insect interactions both directly, through chemical composition of plant tissue, and indirectly, through plant morphology, for serpentine-tolerant Mimulus guttatus (Phrymaceae). First, we scored floral display (corolla width, number of open flowers per inflorescence, and inflorescence height), flower chemistry, pollinator visitation and florivory of M. guttatus growing on natural serpentine and non-serpentine soil over 2 years. Second, we conducted a common garden reciprocal soil transplant experiment to isolate the effect of serpentine soil on floral display traits and flower chemistry. And last, we observed arrays of field-collected inflorescences and potted plants to determine the effect of soil environment in the field on pollinator visitation and florivore damage, respectively. For both natural and experimental plants, serpentine soil caused reductions in floral display and directly altered flower tissue chemistry. Plants in natural serpentine populations received fewer pollinator visits and less damage by florivores relative to non-serpentine plants. In experimental arrays, soil environment did not influence pollinator visitation (though larger flowers were visited more frequently), but did alter florivore damage, with serpentine-grown plants receiving less damage. Our results demonstrate that the soil environment can directly and indirectly affect plant–mutualist and plant–antagonist interactions of serpentine-tolerant plants by altering flower chemistry and floral display.     

Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb

The invasion of exotic species into natural habitats is considered to be a major threat to biodiversity, and many studies have examined how exotic plants directly affect native plant species through competitive interactions for abiotic resources. However, although exotics can have potentially great ecological and evolutionary consequences, very few researchers have studied the effect of exotics on the interactions between plants and their mutualistic partners, such as pollinators, and none have reported on such impacts in logged and undisturbed boreal forest ecosystems. Here we show how experimental introductions of an exotic plant species (Phacelia tanacetifolia Bentham) affect pollinator visitation and female reproductive success of a native plant (Melampyrum pratense L.) in recently disturbed (i.e., logged) and in undisturbed boreal forest habitats. The presence of Phacelia significantly increased the number of bumble bees entering plots in both habitat types. However, the exotic species had a strong negative impact on the visitation rate to the native species in both habitat types. Despite this negative impact on pollinator visitation, the exotic had no effect on female reproductive success of the native species in any habitat. Our results show that seed production may be more robust than pollinator visitation to exotic invasion, irrespective of habitat disturbance history.     

Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in Delphinium barbeyi (Ranunculaceae)

Variation in flowering plant density can have conflicting effects on pollination and seed production. Dense flower patches may attract more pollinators, but flowers in those patches may also compete for pollinator visits and abiotic resources. We examined how natural and experimental conspecific flowering plant density affected pollen receipt and seed production in a protandrous, bumble bee-pollinated wildflower, Delphinium barbeyi (Ranunculaceae). We also compared floral sex ratios, pollinator visitation rates, and pollen limitation of seed set from early to late in the season to determine whether these factors mirrored seasonal changes in pollen receipt and seed production. Pollen receipt increased with natural flowering plant density, while seed production increased across lower densities and decreased across higher flower densities. Experimental manipulation of flowering plant density did not affect pollinator visitation rate, pollen receipt, or seed production. Although pollinator visitation rate increased 10-fold from early to late in the season, pollen receipt and seed set decreased over the season. Seed set was never pollen-limited. Thus, despite widespread effects of flowering plant density on plant reproduction in other species, the effects of conspecific flowering plant density on D. barbeyi pollination and seed production are minor.     

Within-population spatial variation in pollinator visitation rates,pollen limitation on seed set,and flower longevity in an alpine species

Pollen limitation through insufficient pollen deposition on stigmas caused by too infrequent pollinator visitation may influence the reproductive outcome of plants. In this study we investigated how pollinator visitation rate, the degree of pollen limitation, and flower longevity varied spatially among three sites at different altitudes within a population of the dwarf shrub Dryas octopetala L. in alpine southern Norway. Significant pollen limitation on seed set only occurred at the mid-elevation site, while seed set at the other sites appeared to be mainly resource limited, thus indicating a spatial variation in pollen limitation. There was no association between the spatial variation in the extent of pollen limitation and pollinator visitation rate to flowers. However, pollinator visitation rates were related to flower longevity of Dryas; sites with low visitation rates had long-lived flowers and vice versa. Thus, our results suggest within-population spatial co-variation between pollinator visitation rates, pollen limitation, and a developmental response to these factors, flower longevity.     

Plant connectivity underlies plant‐pollinator‐exploiter distributions in Ficus petiolaris and associated pollinating and non‐pollinating fig wasps

Mutualism is ubiquitous in nature, and nursery pollination mutualisms provide a system well suited to quantifying the benefits and costs of symbiotic interactions. In nursery pollination mutualisms, pollinators reproduce within the inflorescence they pollinate, with benefits and costs being measured in the numbers of pollinator offspring and seeds produced. This type of mutualism is also typically exploited by seed‐consuming non‐pollinators that obtain resources from plants without providing pollination services. Theory predicts that the rate at which pollen‐bearing ‘foundresses’ visit a plant will strongly affect the plant's production of pollinator offspring, non‐pollinator offspring, and seeds. Spatially aggregated plants are predicted to have high rates of foundress visitation, increasing pollinator and seed production, and decreasing non‐pollinator production; very high foundress visitation may also decrease seed production indirectly through the production of pollinators. Working with a nursery mutualism comprised of the Sonoran Desert rock fig, Ficus petiolaris, and host‐specific pollinating and non‐pollinating fig wasps, we use linear models to evaluate four hypotheses linking species interactions to benefits and costs: 1) foundress density increases with host‐tree connectivity, 2) pollinator production increases with foundress density, and 3) non‐pollinator production and 4) seed production decrease with pollinator production. We also directly test how tree connectivity affects non‐pollinator production. We find strong support for our four hypotheses, and we conclude that tree connectivity is a key driver of foundress visitation, thereby strongly affecting spatial distributions in the F. petiolaris community. We also find that foundress visitation decreases at the northernmost edge of the F. petiolaris range. Finally, we find species‐specific effects of tree connectivity on non‐pollinators to be strongly correlated with previously estimated non‐pollinator dispersal abilities. We conclude that plant connectivity is highly important for predicting plant‐pollinator‐exploiter dynamics, and discuss the implications of our results for species coexistence and adaptation.     

Does the invasive Lupinus polyphyllus increase pollinator visitation to a native herb through effects on pollinator population sizes?

Invasive plants may compete with native species for abiotic factors as light, space and nutrients, and have also been shown to affect native pollination interactions. Studies have mainly focused on how invasive plants affect pollinator behaviour, i.e. attraction of pollinators to or away from native flowers. However, when an invasive plant provides resources utilized by native pollinators this could increase pollinator population sizes and thereby pollination success in natives. Effects mediated through changes in pollinator population sizes have been largely ignored in previous studies, and the dominance of negative interactions suggested by meta-analyses may therefore be biased. We investigated the impact of the invasive Lupinus polyphyllus on pollination in the native Lotus corniculatus using a study design comparing invaded and uninvaded sites before and after the flowering period of the invasive. We monitored wild bee abundance in transects, and visit rate and seed production of potted Lotus plants. Bumblebee abundance increased 3.9 times in invaded sites during the study period, whereas it was unaltered in uninvaded sites. Total visit rate per Lotus plant increased 2.1 times in invaded sites and decreased 4.4 times in uninvaded sites. No corresponding change in seed production of Lotus was found. The increase in visit rate to Lotus was driven by an increase in solitary bee visitation, whereas mainly bumblebees were observed to visit the invasive Lupinus. The mechanism by which the invasive increases pollinator visit rates to Lotus could be increased availability of other flower resources for solitary bees when bumblebees forage on Lupinus.     

Floral display and pollination success in Achillea ptarmica (Asteraceae)

In a natural population of the self-incompatible Achillea ptarmica , many-headed inflorescences attracted most pollinators (flies), and each pollinator visited more heads on large inflorescences than on smaller ones. The visitation rate did not increase disproportionately with inflorescence size, as would be expected if clusters of heads had a synergetic effect on pollinator attraction. Both the calculated visitation rate per head and the percentage seed set increased slightly as a function of head number. The removal of rays from all heads in the inflorescence reduced the approach rate by 51%, but had only a small negative effect on seed set (12%). Hence, ray removal probably affected male fertility (pollen donation) to a greater extent than female fertility. The decline in pollination success was similar for all inflorescence sizes, suggesting that ray and inflorescence size have independent effects on the total display, and thus represent separate targets for pollinator-mediated selection. Residual variation in seed set was strongly correlated with patch identity, indicating clonal or environmentally induced differences in female reproductive success.     

Experimental reduction of pollinator visitation modifies plant–plant interactions for pollination

The strength of interactions between plants for pollination depends on the abundance of plants and pollinators in the community. The abundance of pollinators may influence plant associations and densities at which individual fitness is maximized. Reduced pollinator visitation may therefore affect the way plant species interact for pollination. We experimentally reduced pollinator visitation to six pollinator‐dependent species (three from an alpine and three from a lowland community in Norway) to study how interactions for pollination were modified by reduced pollinator availability. We related flower visitation, pollen limitation and seed set to density of conspecifics and pollinator‐sharing heterospecifics inside 30 dome‐shaped cages partially covered with fishnet (experimental plots) and in 30 control plots. We expected to find stronger interactions between plants in experimental compared to controls plots. The experiment modified plant–plant interactions for pollination in all the six species; although for two of them neighbourhood interactions did not affect seed set. The pollen limitation and seed set data showed that reduction of pollinator visits most frequently resulted in novel and/or stronger interactions between plants in the experimental plots that did not occur in the controls. Although the responses were species‐specific, there was a tendency for increasing facilitative interactions with conspecific neighbours in experimental plots where pollinator availability was reduced. Heterospecifics only influenced pollination and fecundity in species from the alpine community and in the experimental plots, where they competed with the focal species for pollination. The patterns observed for visitation rates differed from those for fecundity, with more significant interactions between plants in the controls in both communities. This study warns against the exclusive use of visitation data to interpret plant–plant interactions for pollination, and helps to understand how plant aggregations may buffer or intensify the effects of a pollinator loss on plant fitness.     

No evidence for a role of pollinator discrimination in causing selection on flower size through female reproduction

The preference for certain floral phenotypes by flower visiting animals may fuel the evolution of floral traits because variation in flower visitation rates may lead to fitness variation within a population. Here, I examine the importance of flower size for pollinator visitation rate, seed set, and seed mass in two alpine populations of the insect-pollinated herb Ranunculus acris L. during two seasons. There was no pollen limitation of seed set or mass. Pollinators discriminated strongly against flowers experimentally reduced in size. Despite this, there were no signs of any significant impact of flower size on female reproductive success. The results show that although pollinators discriminate strongly among floral phenotypes, this may not always result in female fitness differences within a population because seed set or mass is not limited by pollen availability alone. Probably abiotic environmental constraints prevent plants with high pollinator visitation from capitalizing on the high pollen deposition.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae)

Background and Aims

Few studies have examined the dynamics of specialist plant–pollinator interactions at a geographical scale. This knowledge is crucial for a more general evolutionary and ecological understanding of specialized plant–pollinator systems. In the present study, variations in pollinator activity, assemblage composition and pollen limitation were explored in the oil-producing species Nierembergia linariifolia (Solanaceae).

Methods

Pollen limitation in fruit and seed production was analysed by supplementary hand pollination in five wild populations. Pollinator activity and identity were recorded while carrying out supplementary pollination to assess the effect of pollinators on the degree of pollen limitation. In two populations, pollen limitation was discriminated into quantitative and qualitative components by comparing supplementation and hand cross-pollination in fruit set and seed set. The effect of flower number per plant on the number of flowers pollinated per visitor per visit to a plant was examined in one of these populations as a possible cause of low-quality pollination by increasing geitonogamy.

Results and Conclusions

Although pollen limitation was evident along time and space, differences in magnitude were detected among populations and years that were greatly explained by pollinator activity, which was significantly different across populations. Floral display size had a significant effect on the visitation rate per flower. Limitation by quality clearly affected one population presumably due to a high proportion of geitonogamous pollen. The great inter-population variation in plant–pollinator interaction (both in pollinator assemblages composition and pollinator activity) and fitness consequences, suggests that this system should be viewed as a mosaic of locally selective processes and locally specialized interactions.Key words: Nierembergia linariifolia, Centris, Chalepogenus, pollen limitation, pollen quality, oil-producing flowers, specialized pollination, floral display, assemblage composition, geographic variation, Solanaceae, tests of equivalence     

Pollinator Interactions with Yellow Starthistle (Centaurea solstitialis) across Urban,Agricultural, and Natural Landscapes

Pollinator-plant relationships are found to be particularly vulnerable to land use change. Yet despite extensive research in agricultural and natural systems, less attention has focused on these interactions in neighboring urban areas and its impact on pollination services. We investigated pollinator-plant interactions in a peri-urban landscape on the outskirts of the San Francisco Bay Area, California, where urban, agricultural, and natural land use types interface. We made standardized observations of floral visitation and measured seed set of yellow starthistle (Centaurea solstitialis), a common grassland invasive, to test the hypotheses that increasing urbanization decreases 1) rates of bee visitation, 2) viable seed set, and 3) the efficiency of pollination (relationship between bee visitation and seed set). We unexpectedly found that bee visitation was highest in urban and agricultural land use contexts, but in contrast, seed set rates in these human-altered landscapes were lower than in natural sites. An explanation for the discrepancy between floral visitation and seed set is that higher plant diversity in urban and agricultural areas, as a result of more introduced species, decreases pollinator efficiency. If these patterns are consistent across other plant species, the novel plant communities created in these managed landscapes and the generalist bee species that are favored by human-altered environments will reduce pollination services.