Premise
Many animals provide ecosystem services in the form of pollination including honeybees, which have become globally dominant floral visitors. A rich literature documents considerable variation ...in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators.
Methods
We conducted a hierarchical meta‐analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. We paired SVE data with visitation frequency data for 69 of these studies. We used these data to ask three questions: (1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE? (2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors? (3) Is there a correlation between visitation frequency and SVE?
Results
Honeybees were significantly less effective than the most effective non‐honeybee pollinators but were as effective as the average pollinator. The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent.
Conclusions
Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators, and safeguarding pollination will benefit from conservation of non‐honeybee taxa.
Co‐flowering plant species commonly share flower visitors, and thus have the potential to influence each other's pollination. In this study we analysed 750 quantitative plant–pollinator networks from ...28 studies representing diverse biomes worldwide. We show that the potential for one plant species to influence another indirectly via shared pollinators was greater for plants whose resources were more abundant (higher floral unit number and nectar sugar content) and more accessible. The potential indirect influence was also stronger between phylogenetically closer plant species and was independent of plant geographic origin (native vs. non‐native). The positive effect of nectar sugar content and phylogenetic proximity was much more accentuated for bees than for other groups. Consequently, the impact of these factors depends on the pollination mode of plants, e.g. bee or fly pollinated. Our findings may help predict which plant species have the greatest importance in the functioning of plant–pollination networks.
Theoretical models indicate that the structure of plant–pollinator networks has important implications for the reproduction and survival of species. However, despite the growing information on the ...mechanisms underlying such a structure, it is still difficult to predict the functional consequences of species’ structural positions in these networks. From the plant perspective, species position and roles in pollination networks might be related to traits describing flower attractiveness, availability and dependence on pollinators. In turn, both network metrics and plant traits might influence plant species fitness.
During two field seasons, we collected data from the 23 most abundant plant species in a rich coastal community, to evaluate the association between population and floral traits (floral abundance at population level and flowers per individual, flower shape and size, flowering length, nectar volume, pollinator dependence), species‐level network metrics (linkage level, specialization –d′–, weighted closeness centrality, network roles related to modularity) and plant fitness (seeds/flower, seed weight).
Flowering length, flower size, flower abundance and pollinator dependence were positively related to greater generalization, as measured by various indices. More abundant species and those with larger flowers showed higher linkage levels (i.e. higher number of pollinator species), whereas longer flowering periods were negatively related to d′ and positively related to closeness centrality and important roles in the network. Likewise, plants species more dependent on pollinators occupied more central positions in the network. Furthermore, centrality in the networks was significantly associated with plant fitness. Specifically, central species in the network produced more and heavier seeds than the others. However, other plant traits, such as flower size and pollinator dependence had additional direct effects on seed production.
Synthesis. Our study highlights how population and floral traits define the positions and roles of species structuring the pollination communities. Moreover, the relationships between network metrics and plant reproduction indicate, for the first time, the functional implications of these structural positions at the interspecific level of community assembly.
Translated
Resumen
Los modelos teóricos indican que la estructura de las redes planta‐polinizador tiene implicaciones importantes para la reproducción y supervivencia de las especies. Sin embargo, pese a que cada vez existe más información sobre los mecanismos subyacentes a dicha estructura, todavía estamos lejos de poder predecir las consecuencias funcionales de las posiciones estructurales de las especies en las redes. La posición y los roles de las especies de plantas en las redes de polinización pueden estar relacionados con rasgos que describen el atractivo y la disponibilidad de sus flores, así como con la dependencia de los polinizadores para su reproducción. A su vez, tanto las métricas de la red como los rasgos de las especies pueden influir en su éxito reproductivo.
Durante dos temporadas de campo, recolectamos datos de las 23 especies de plantas más abundantes de una comunidad costera rica en especies, para evaluar la asociación entre los rasgos florales y poblacionales de las especies de plantas (abundancia floral a nivel de población y flores/individuo, forma y tamaño de la flor, duración de la floración, volumen de néctar, dependencia de polinizadores), las métricas de red a nivel de especie (nivel de enlace, especialización –d´–, centralidad, roles de red relacionados con la modularidad) y su éxito reproductivo (semillas/flor, peso de semilla).
La duración de la floración, el tamaño de la flor, la abundancia de flores y la dependencia de los polinizadores se relacionaron positivamente con una mayor generalización, medida con diferentes índices. Las especies más abundantes y aquellas con flores más grandes mostraron niveles de enlace más altos (es decir, un mayor número de especies de polinizadores), mientras que los períodos de floración más largos se relacionaron negativamente con d' y positivamente con la centralidad y los roles importantes en la red. Asimismo, las plantas más dependientes de polinizadores ocuparon posiciones más centrales en la red. Además, la centralidad de las especies en las redes se asoció significativamente con el éxito reproductivo de las plantas. Específicamente, las especies centrales en la red produjeron más semillas y más pesadas que las otras especies. Sin embargo, otros rasgos de las plantas, como el tamaño de las flores y la dependencia de los polinizadores tuvieron efectos directos adicionales sobre la producción de semillas.
Síntesis. Nuestro estudio destaca cómo la población y los rasgos florales definen las posiciones y roles de las especies que estructuran las comunidades de polinización. Además, las relaciones entre las métricas de la red y el éxito reproductivo de las plantas indican, por primera vez, las implicaciones funcionales de estas posiciones estructurales al nivel inter‐específico de ensamblaje de comunidades.
Our study highlights how population and floral traits define the positions and roles of species structuring the pollination communities. Moreover, the relationships between network metrics and plant reproduction indicate, for the first time, the functional implications of these structural positions at the interspecific level of community assembly.
Pollinator-mediated selection to a large extent shapes angiosperm floral diversity, but clearly not in isolation. To understand how selection by pollinators interacts with other selective factors and ...depends on environmental context, studies that address multiple selective agents are necessary. Here, I illustrate how antagonistic interactions, community context, and resource availability may influence selection on floral traits. I discuss approaches to quantify the context dependence of pollinator-mediated selection, emphasizing experimental studies that manipulate pollination regime in combination with other putative selective factors. I also discuss how context dependence may differ between floral traits that affect pollinator attraction versus pollination efficiency. Finally, I suggest some areas where important progress can be made. A better understanding of the context dependence of pollinator-mediated selection is essential to predict when, where, and how environmental change will alter selection on floral traits.
Quantifying the benefits of pollinator abundance and diversity for plant reproduction is a critical challenge, especially given recent pollinator declines. Many studies test for pollen limitation ...(PL), but huge gaps remain in our understanding of how often and why plants experience PL. Most studies are limited to a few sites or years. Little existing research mechanistically links pollinator visitation with plant reproduction. Also, buffering against variability in visitation is a key but largely untested potential benefit of pollinator diversity. Long‐term studies pairing visitation data with PL experiments are essential to addressing these gaps, but extremely rare.
I measured pollinator visitation, responses to pollen supplementation, and fruit weights in the generalist plant Scrophularia californica across multiple sites for 8 years. I determined how often S. californica experienced significant PL and tested mechanistic models predicting PL and fruit (capsule) weight from visitation. I then used those models to simulate pollinator loss and evaluate the relative effects of changes in visit quantity and quality. I explored the stabilizing benefits of visitor diversity by quantifying both covariation among pollinators and effects of simulated species loss on variation in PL and capsule weights.
Scrophularia showed significant PL in only 26.9% of patch/year combinations tested. Visitation by the most abundant (Apis mellifera) and effective (Vespula pensylvanica) pollinators strongly predicted PL and capsule weights. Both response curves were highly nonlinear, but PL saturated more with increased visitation. Pollinator loss simulations predicted substantially increased PL and reduced capsule weights, mostly because of lower visit numbers rather than changes in visit quality. Visitation rates of individual pollinators varied substantially and without correlation. Simulated pollinator loss increased the spatial and temporal skew in visitation, resulting in higher predicted coefficients of variation for PL and capsule weights.
Synthesis. Previous work predicts a nonlinear relationship between pollinator visitation and plant reproduction, but this is the first long‐term study I am aware of that quantifies such a pattern. The analysis of covariance in pollinator visitation combined with my simulation results provide novel empirical support for another important hypothesis, that multiple pollinators can provide stabilizing benefits for plant reproduction.
Previous work predicts a nonlinear relationship between pollinator visitation and plant reproduction, but this is the first long‐term study I am aware of that quantifies such a pattern. The analysis of covariance in pollinator visitation combined with my simulation results provide novel empirical support for another important hypothesis, that multiple pollinators can provide stabilizing benefits for plant reproduction.
Abstract
Pollinator insects are declining worldwide, also due to the alteration of their diet with severe implications on their health status. Pollinators diet relies mainly on flower rewards (i.e. ...pollen and nectar), and a precise characterization of their chemical composition is crucial in defining pollinators' nutritional ecology. In this context, the pollen represents a challenging source to investigate, especially due to operative challenges during collection operations and to the small amounts produced per flower.
Here, we designed and tested a novel, easy‐to‐assemble tool for pollen sampling: E‐PoSa (Electronic Pollen Sampler), based on the use of a portable vacuum cleaner. We compared it with some of the most used sampling methods for pollen (i.e. anthers sieving and sampling of the whole anthers) by looking at the differences in their quantitative recovery and nutritional profile. Its applicability in ecological studies was also corroborated by an assessment of its recovery rate obtained from a panel of wildflower species in an operational environment.
The data obtained showed a significantly higher pollen recovery capacity of E‐PoSa compared with the conventional sieving approach and the success in retrieving enough pollen to conduct phytochemical analyses from a broad range of flower morphologies in the field. Our results also demonstrated that high purity pollen can be collected with E‐PoSa and that the device does not introduce any significant variation in the nutritional analysis compared with the conventional sieving.
This new sampling approach represents a cheap and easy‐to‐assemble tool encouraging its future use not only in the field of pollen nutrition but also in a wide variety of other contexts related to pollination ecology. Acknowledging the potential influences of the sampling techniques and moving towards shared standardized field protocols will advance the comprehension of species interactions and foraging patterns of pollinators and their nutritional needs.
Floral resources are known to be important in regulating wild pollinator populations and are therefore an important component of agri‐environment and restoration schemes which aim to support ...pollinators and their associated services. However, the phenology of floral resources is often overlooked in these schemes — a factor which may be limiting their success.
Our study characterizes and quantifies the phenology of nectar resources at the whole‐farm scale on replicate farms in Southwestern UK throughout the flowering season. We quantify the corresponding nectar demands of a subset of common wild pollinators (bumblebees) to compare nectar supply and pollinator demand throughout the year, thereby identifying periods of supply‐demand deficit.
We record strong seasonal fluctuations in farmland nectar supplies, with two main peaks of nectar production (May and July) and a considerable “June Gap” in between. March and August/September are also periods of low nectar availability.
Comparing the phenology of nectar supply with the phenology of bumblebee nectar demand reveals “hunger gaps” during March and much of August/September when supply is unlikely to meet demand.
Permanent pasture and woodland produced the greatest share of farmland nectar because of their large area; however, linear features such as hedgerows and field margins provided the greatest nectar per unit area. Fifty percent of total nectar was supplied by just three species (Allium ursinum, Cirsium arvense and Trifolium repens), but some less productive species (e.g. Hedera helix and Taraxacum agg.) were important in ensuring phenological continuity of nectar supply.
Synthesis and applications. By comparing the phenology of farmland nectar supply with the phenology of pollinator demand, we demonstrate that the timing of nectar supply may be as important as total nectar production in limiting farmland pollinator populations. Considering phenology in the design of agri‐environment or restoration schemes is therefore likely to improve their suitability for pollinators. Plant species which flower during periods of resource deficit (early spring and late summer) should be prioritized in schemes which aim to conserve or restore pollinator populations. Maintaining a range of semi‐natural habitats with complementary flowering phenologies (e.g. woodland, hedgerows and field margins) will ensure a more continuous supply of nectar on farmland, thereby supporting pollinators for their entire flight season.
By comparing the phenology of farmland nectar supply with the phenology of pollinator demand, we demonstrate that the timing of nectar supply may be as important as total nectar production in limiting farmland pollinator populations. Considering phenology in the design of agri‐environment or restoration schemes is therefore likely to improve their suitability for pollinators. Plant species which flower during periods of resource deficit (early spring and late summer) should be prioritized in schemes which aim to conserve or restore pollinator populations. Maintaining a range of semi‐natural habitats with complementary flowering phenologies (e.g. woodland, hedgerows and field margins) will ensure a more continuous supply of nectar on farmland, thereby supporting pollinators for their entire flight season.
Loss of habitats and native species, introduction of invasive species, and changing climate regimes lead to the homogenization of landscapes and communities, affecting the availability of habitats ...and resources for economically important guilds, such as pollinators. Understanding how pollinators and their interactions vary along resource diversity gradients at different scales may help to determine their adaptability to the current diversity loss related to global change. We used data on 20 plant–pollinator communities along gradients of flower richness (local diversity) and landscape heterogeneity (landscape diversity) to understand how the diversity of resources at local and landscape scales affected (1) wild pollinator abundance and richness (accounting also for honey bee abundance), (2) the structure of plant–pollinator networks, (3) the proportion of actively selected interactions (those not occurring by neutral processes), and (4) pollinator diet breadth and species' specialization in networks. Wild pollinator abundance was higher overall in flower‐rich and heterogeneous habitats, while wild pollinator richness increased with flower richness (more strongly for beetles and wild bees) and decreased with honeybee abundance. Network specialization (H2′), modularity, and functional complementarity were all positively related to floral richness and landscape heterogeneity, indicating niche segregation as the diversity of resources increases at both scales. Flower richness also increased the proportion of actively selected interactions (especially for wild bees and flies), whereas landscape heterogeneity had a weak negative effect on this variable. Overall, network‐level metrics responded to larger landscape scales than pollinator‐level metrics did. Higher floral richness resulted in a wider taxonomic and functional diet for all the study guilds, while functional diet increased mainly for beetles. Despite this, specialization in networks (d′) increased with flower richness for all the study guilds, because pollinator species fed on a narrower subset of plants as communities became richer in species. Our study indicates that pollinators are able to adapt their diet to resource changes at local and landscape scales. However, resource homogenization might lead to poor and generalist pollinator communities, where functionally specialized interactions are lost. This study highlights the importance of including different scales to understand the effects of global change on pollination service through changes in resource diversity.
In Veits et al., we showed that flowers respond to a range of pollinator sounds by increased nectar sugar concentration. Here we clarify that (1) our argument is relevant to most pollinators, and not ...limited to bees (2) specifically, bees do access Oenothera Drumondii nectar in this area.
In animal-pollinated plants, the opportunity for selection and the strength of pollinatormediated selection are expected to increase with the degree of pollen limitation. However, whether differences ...in pollen limitation can explain variation in pollinator-mediated and net selection among animal-pollinated species is poorly understood.
In the present study, we quantified pollen limitation, variance in relative fitness and pollinator-mediated selection on five traits important for pollinator attraction (flowering start, plant height, flower number, flower size) and pollination efficiency (spur length) in natural populations of 12 orchid species. Pollinator-mediated selection was quantified by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants.
Mean pollen limitation ranged from zero to 0.96. Opportunity for selection, pollinator-mediated selection and net selection were all positively related to pollen limitation, whereas nonpollinator-mediated selection was not. Opportunity for selection varied five-fold, strength of pollinator-mediated selection varied three-fold and net selection varied 1.5-fold among species. Supplemental hand-pollination reduced both opportunity for selection and selection on floral traits.
The results show that the intensity of biotic interactions is an important determinant of the selection regime, and indicate that the potential for pollinator-mediated selection and divergence in floral traits is particularly high in species that are strongly pollen-limited.
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