Article

A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors

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Abstract

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: 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?; and 3) Is there a correlation between visitation frequency and SVE? Key results: Honeybees were significantly less effective than the most effective non-honeybee pollinators but 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. This article is protected by copyright. All rights reserved.

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... Though the terms used vary among authors, the "effectiveness" of each pollinator species has been predominantly evaluated as number of pollen grains deposited, or seeds or fruits set, following a single visit to a flower, and the "importance" of each pollinator usually evaluated as the product of its relative effectiveness and its relative frequency of visitation (reviewed in Ne'eman et al. 2010). Across a wide range of both crop and natural plant species in both its native and introduced range, two recent meta-analyses have shown that the pervisit effectiveness of honey bees does not differ from the average non-honey bee floral visitor (Hung et al. 2019, Page et al. 2021. ...
... First, we conducted a "Web of Science" (WoS) literature search to collect relevant manuscripts. Due to the extremely variable language used to describe insect visitation to flowers, we constructed the following WoS query (modified from Page et al. 2021): "A* mellifera" AND "pollinat* effectiveness" OR "pollinat* efficacy" OR "pollinat* efficiency" OR "pollinat* intensity" OR "pollinat* importance" OR "pollinat* level" OR "flower visits per plant" OR "visits per plant*". We then employed a similar query in Google Scholar. ...
... After removing duplicates and erroneous results, we had 522 published manuscripts. Lastly, an additional 30 papers were added after examining literature that was collected and analysed in two previous meta-analyses likely to include pertinent visitation data (Herrera 2020; Page et al. 2021). ...
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Geitonogamy, the transfer of pollen from one flower to another on the same plant, is often the primary means of self-pollination in flowering plants. For self-compatible plants, self-fertilization may lead to greatly reduced offspring fitness via inbreeding depression. For self-incompatible plants, geitonogamous pollen transfer can result in low seed set, even when stigmatic pollen loads are substantial. For multiple self-compatible, native California plants, we found that honey bees visited more flowers per plant than native insects, and that offspring resulting from pollination by honey bees had reduced fitness relative to those resulting from native insect pollination. Here we investigate whether honey bees generally make more geitonogamous visits than other pollinators using data from a global survey of 41 manuscripts that reported floral visitation data. Compared to the average of all non-honey bee visitors in a plants pollinator assemblage, honey bees visit significantly more flowers per plant, though they do not differ from the non-honey bee visitor with the highest rate of geitonogamous visitation. However, the disparity between rates of geitonogamous visitation by honey bees and non-honey bee visitors is a function of the frequency of honey bees relative to non-honey bee visitors. As honey bees become increasingly numerically dominant, there is a trend for their rates of geitonogamous visitation to increase, accompanied by a significant decline in flowers visited per plant by non-honey bee visitors. While we found that honey bees visited more flowers per plant compared to the average of other visitors, large or eusocial pollinators were as likely as honey bees to be the most geitonogamous visitor.
... Le préalable à l'étude des communautés d'abeilles et des interactions plantes-pollinisateurs passe bien souvent par un travail de connaissance faunistique poussé. Ainsi, lors de toutes mes expériences de recherche, (Jannersten, 1984 ;Howllet et al. 2017 ;Ollerton, 2017 ;Sayers et al. 2019 ;Vanderplanck et al. 2020 ;Page et al. 2021, Requier et al. 2022. Pourtant, ils sont encore peu étudiés (Rader et al. 2009 ;, Bartholomée & Lavorel, 2019, où même en ce qui concerne les diptères non-syrphidés largement oublié dans les études relatives à la pollinisation (Orford et al. 2015 ;Grass et al. 2016). ...
... Pourtant, ils sont encore peu étudiés (Rader et al. 2009 ;, Bartholomée & Lavorel, 2019, où même en ce qui concerne les diptères non-syrphidés largement oublié dans les études relatives à la pollinisation (Orford et al. 2015 ;Grass et al. 2016). Bien que les abeilles soient souvent citées comme étant les pollinisateurs les plus efficaces à l'échelle d'une visite de fleurs, notamment grâce à leurs poils branchus et leurs organes spécifiques de récolte de pollen (Barrios et al. 2016 ;Willmer et al. 2017 ;Page et al. 2021), l'abondance et la diversité des diptères en font des pollinisateurs très importants notamment dans les paysages agricoles (Rader et al. 2009 ; et les écosystèmes alpins (Lefebvre et al. 2019). Fig. 6). ...
... 2016Osterman et al. 2021). D'une manière générale, pour de nombreuses cultures, les abeilles domestiques ne peuvent pas compenser l'absence de pollinisateurs sauvages ou se substituer à eux (e.g.Garibaldi et al. 2013 ;Nicholson et al. 2019 ;Page et al. 2021 ;Senapathi et al. 2021). Ainsi, les abeilles domestiques ne sont pas des pollinisateurs efficients pour le coton, les fraises, les courgettes, ou encore les tomates (entre autres) en comparaison des pollinisateurs sauvages(Garibaldi et al. 2013 ;Willmer et al. 2017 ;Page et al. 2021). ...
Thesis
Chapitre 1 : Les abeilles dans leur diversité. Chapitre 2 : Paysages agricoles, pollinisateurs et services de pollinisation. Chapitre 3 : La ville et ses effets sur les communautés d’abeilles sauvages. Chapitre 4 : La compétition Apis vs non Apis. Chapitre 5 : Les abeilles exotiques envahissantes.
... Bees that visit flowers solely for nectar can still contribute to pollination, however, as pollen can still be transferred by the bee's external setae. The difference in pollination service between bees visiting flowers for pollen and nectar, versus bees visiting for nectar alone, is poorly studied [92,93]. There is evidence that most pollen transfer occurs via these external hairs, because pollen carried in scopa is often moistened, thus decreasing the chance for pollen transfer [94]. ...
... To build on this complexity, bee species have different structures of hairs, in varying densities, on different parts of their bodies. Megachilid bees carry pollen on scopae formed on the underside of their abdomen, whereas other bees have scopae on their hind-femora or hind-tibiae [92]. The thickness and body position of bee scopae and external body hairs, as well as the shape and pollen structures of flowers can all impact the efficiency of pollen transfer [95]. ...
... Specialist bees tend to feed within a certain genus of plants, as within the genus, flower structures are often similar [92]. There are many specialist behaviors that have been documented, with some bees visiting a single species, and others feeding on several species or genera within a family of plants. ...
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Different species of bees provide essential ecosystem services by pollinating various agricultural crops, including tree fruits. Many fruits and nuts depend on insect pollination, primarily by wild and managed bees. In different geographical regions where orchard crops are grown, fruit growers rely on wild bees in the farmscape and use orchard bees as alternative pollinators. Orchard crops such as apples, pears, plums, apricots, etc., are mass-flowering crops and attract many different bee species during their bloom period. Many bee species found in orchards emerge from overwintering as the fruit trees start flowering in spring, and the active duration of these bees aligns very closely with the blooming time of fruit trees. In addition, most of the bees in orchards are short-range foragers and tend to stay close to the fruit crops. However, the importance of orchard bee communities is not well understood, and many challenges in maintaining their populations remain. This comprehensive review paper summarizes the different types of bees commonly found in tree fruit orchards in the fruit-growing regions of the United States, their bio-ecology, and genetic diversity. Additionally, recommendations for the management of orchard bees, different strategies for protecting them from multiple stressors, and providing suitable on-farm nesting and floral resource habitats for propagation and conservation are discussed.
... The western honeybee, Apis mellifera L., is native to Europe, Africa, and the Middle East, but due to beekeeping it is now distributed around the world (Han et al., 2012). Honeybees are also the most widely used and economically valuable pollinator of crops in monoculture worldwide (Klein et al., 2007), but there is increasing evidence that they are not particularly effective pollinators in either agricultural or in natural environments (Garibaldi et al., 2014;Hung et al., 2018;Page et al., 2021). Just over 50 years ago, Free (1966a) published an important, but often overlooked, paper that used mark-recapture data to show that honeybees tend to confine their activities to single apple trees, even during subsequent foraging bouts. ...
... Recent meta-analyses showed that honeybees are generally less efficient when compared to the most efficient non-Apis pollinators for various plant species (Hung et al., 2018;Page et al., 2021), and this is particularly true for when honeybees are compared to birds (Page et al., 2021). It also applies both where honeybees are native (e.g., Brown et al., 2009) and where they are introduced (e.g., Celebrezze and Paton, 2004). ...
... Recent meta-analyses showed that honeybees are generally less efficient when compared to the most efficient non-Apis pollinators for various plant species (Hung et al., 2018;Page et al., 2021), and this is particularly true for when honeybees are compared to birds (Page et al., 2021). It also applies both where honeybees are native (e.g., Brown et al., 2009) and where they are introduced (e.g., Celebrezze and Paton, 2004). ...
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Premise: Honeybees dominate the flower-visitor assemblages of many plant species, yet their efficiency in terms of the quality of pollen delivered to stigmas is largely unknown. We investigated why honeybees are poor pollinators of Aloe ferox, a self-incompatible succulent treelet with large numbers of flowers. Honeybees are very frequent visitors to flowers of this species, yet contribute very little to seed production. Methods: We assessed pollen loads on honeybees, studied their visitation behavior, selectively excluded birds from plants to determine direct effects of bees on pollen deposition, seed set, and ovule abortion, and used a novel "split-pollinator" method to test whether honeybees deposit mainly low-quality self pollen. For the latter, we captured honeybees, and with their existing pollen loads, used them to either pollinate virgin flowers on the plant on which they were caught or to pollinate virgin flowers on different plants. Results: Honeybees cumulatively deposit as much pollen on stigmas as do birds, but our experiments showed that the pollen deposited by honeybees is mostly low-quality self pollen that leads to substantial ovule discounting and depressed seed set. Conclusions: Lack of movement among A. ferox plants during individual honeybee foraging bouts is the most likely explanation for their deposition of low-quality self pollen on stigmas. The "split-pollinator" method is a simple and cost-effective technique to test the quality of pollination.
... Interaction turnover is important to assess as different groups of pollinators are known to have different functions in terms of pollination effectiveness. For instance, native bees are generally more effective pollinators than native flies (Page et al., 2021). It is critical to understand how interactions change respective to both components of interaction turnover to determine how subsets of species respond to changes in resource availability or the loss of a keystone species. ...
... Likewise, bumblebees that had high interaction frequency (namely Bombus impatiens) with C. pitcheri in 2016 drastically decreased with the decline of C. pitcheri in our networks. These larger pollinators were replaced by flies, such as Caliphoridae sp., that may forage with higher incidences of nectar robbing or are less effective at pollinating due to traits that result in lower conspecific pollen transfer (Herrera, 1987;Adler and Irwin, 2006;Földesi et al., 2021;Page et al., 2021). Solitary bees, specifically halictids such as Dialictus sp., rewired to a greater extent than other functional groups and are known to be effective pollinators (Batra, 1984;Bischoff et al., 2013;Marshall J. M., 2017;Willmer et al., 2017). ...
Article
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Ecological communities are maintained through species interactions, and the resilience of species interactions is critical to the persistence of natural communities. Keystone species play outsized roles in maintaining species interaction networks, and within plant-pollinator communities are high priorities for conservation. The loss of a keystone plant from a plant-pollinator network is expected to cause changes to network structure and composition of pollinator species, with the potential to cause secondary losses of plants and pollinators. To understand how the unmanipulated decline of a keystone plant affects the structure and composition of its network, we studied the plant-pollinator interactions of a Lake Michigan dune plant community where the population of the keystone plant, Cirsium pitcheri , is in rapid decline. The network prior to C. pitcheri decline (2016) was compared to the network as C. pitcheri continued to decline (2021 and 2022) in response to habitat loss. We find evidence that the loss of C. pitcheri altered network structure such that the community may be more sensitive to perturbations. Furthermore, changes in the composition of pollinators were explained by species turnover to a greater extent than by interaction rewiring, including the loss of bumblebees. Short-term negative consequences based on the changes to network structure and composition might lead to long-term effects on the persistence of the dune community. Our study exemplifies that the decline of a keystone plant can have negative implications for conservation of a plant-pollinator community. Using an interaction network framework to assess plant-pollinator communities has potential to develop strategies for best conservation and restoration practices in habitats vulnerable to habitat loss and disturbance.
... Several management strategies are being followed to mitigate pollination deficits, such as increasing the abundance of domesticated bee species or managing the habitat to preserve wild pollinators (Garibaldi et al., 2017). However, quite often management strategies aimed at closing yield gaps are applied blindly (Garibaldi et al., 2016), as the pollination effectiveness of each single species of the pollinator assemblage for a target crop species is usually unknown (Page et al., 2021). For example, one of the more common practices in crop pollination is to increase the number of honeybee hives, yet the honeybee is not always an effective pollinator (Garibaldi et al., 2013;Page et al., 2021;Sáez et al., 2022). ...
... However, quite often management strategies aimed at closing yield gaps are applied blindly (Garibaldi et al., 2016), as the pollination effectiveness of each single species of the pollinator assemblage for a target crop species is usually unknown (Page et al., 2021). For example, one of the more common practices in crop pollination is to increase the number of honeybee hives, yet the honeybee is not always an effective pollinator (Garibaldi et al., 2013;Page et al., 2021;Sáez et al., 2022). In fact, high abundances (Sáez et al., 2014) and/or inefficient management (Haedo et al., 2022b) of honeybees could be detrimental for certain crops. ...
Article
There is a growing consensus that the world is facing a pollination crisis. To mitigate crop pollination deficits, some management strategies include the massive introduction of managed bee species, yet quite often they are applied blindly, as information on crop pollination effectiveness for each single pollinator species of assemblages is usually not available. Therefore, the introduction on managed species is not always the best option to improve crop yields. Here, by using the highly pollinator-dependent alfalfa crop (Medicago sativa L.) as a case study, we propose the use of the effectiveness landscape framework to identify key crop pollinator species. According to this framework, in a mutualistic interaction, each species´effectiveness is represented by the product of a quantitative component and a qualitative one, these being measures of the outcomes of this interaction. We applied this framework for two managed and four wild bee species that visit alfalfa in fields southwest of Buenos Aires province, Argentina. We dissected the quantity components of the pollinator effectiveness landscape by estimating two quantitative subcomponents: visitation rate and flower tripping rate. Also, we estimate pod set as a qualitative component without dissecting it in subcomponents. Our results showed that the contribution of both components and the resulting pollinator effectiveness varied among pollinator species, indicating a contrasting effectiveness of different bee species on alfalfa pollination. For example, pollinator effectiveness was higher for managed than for wild bees, as consequence of their very high visitation rate, however, wild bee flower tripping rate and pod set were as high as managed ones. In fact, wild bees were more effective in promoting flower tripping than one of the managed bees (A. mellifera). This approach allowed us to assess which effectiveness components and subcomponents make pollinator species more or less effective, thus providing valuable information to identify key species to be enhanced to help in closing yield gaps. We suggest that the application of the effectiveness landscape framework would be useful to develop strategies to improve crop pollination service in pollinator-dependent crop systems.
... Several management strategies are being followed to mitigate pollination deficits, such as increasing the abundance of domesticated bee species or managing the habitat to preserve wild pollinators (Garibaldi et al., 2017). However, quite often management strategies aimed at closing yield gaps are applied blindly (Garibaldi et al., 2016), as the pollination effectiveness of each single species of the pollinator assemblage for a target crop species is usually unknown (Page et al., 2021). For example, one of the more common practices in crop pollination is to increase the number of honeybee hives, yet the honeybee is not always an effective pollinator (Garibaldi et al., 2013;Page et al., 2021;Sáez et al., 2022). ...
... However, quite often management strategies aimed at closing yield gaps are applied blindly (Garibaldi et al., 2016), as the pollination effectiveness of each single species of the pollinator assemblage for a target crop species is usually unknown (Page et al., 2021). For example, one of the more common practices in crop pollination is to increase the number of honeybee hives, yet the honeybee is not always an effective pollinator (Garibaldi et al., 2013;Page et al., 2021;Sáez et al., 2022). In fact, high abundances (Sáez et al., 2014) and/or inefficient management (Haedo et al., 2022b) of honeybees could be detrimental for certain crops. ...
... Indeed, this species is managed by beekeepers who place beehives in close proximity to crops to ensure the pollination service is provided [7]. However, wild insect pollinators provide significant contributions to crop pollination in synergy with managed pollinators [8][9][10]. Since the 19th century, wild insect pollinators have suffered an important decline, and beekeepers have registered increased mortality rates in managed honey bee colonies [11][12][13]. ...
Article
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Simple Summary Urban agriculture is a sustainable form of crop production for city-dwellers that requires insect pollinators to produce fruits and vegetables. However, few studies have tested whether urban pollinators are able to support the production of these urban crops. We carried out a study in an urban area near Paris (France) to test whether pollinators present in an urban environment contributed to the production of strawberries. From observational pollinator surveys, we found only wild pollinators visiting strawberry flowers, i.e., no honey bees were observed despite the presence of beehives nearby. We found that fruits were larger when pollinators could visit the flowers. Our results suggest that wild pollinators present in this urban environment are able to support strawberry production in an urban agricultural context. Abstract Pollination services provided by a diversity of pollinators are critical in agriculture because they enhance the yield of many crops. However, few studies have assessed pollination services in urban agricultural systems. We performed flower–visitor observations and pollination experiments on strawberries (Fragaria × ananassa) in an urban area near Paris, France, in order to assess the effects of (i) insect-mediated pollination service and (ii) potential pollination deficit on fruit set, seed set, and fruit quality (size, weight, and malformation). Flower–visitor observations revealed that the pollinator community solely comprised unmanaged pollinators, despite the presence of beehives in the surrounding landscape. Based on the pollination experiments, we found that the pollination service mediated by wild insects improved the fruit size as a qualitative value of production, but not the fruit set. We also found no evidence of pollination deficit in our urban environment. These results suggest that the local community of wild urban pollinators is able to support strawberry crop production and thus plays an important role in providing high-quality, local, and sustainable crops in urban areas.
... By competing with native pollinators for oral resources and nesting sites (Goulson 2003 European honeybees (Apis mellifera) have become principal oral visitors of plant species of ecosystems around the world (Herrera 2020), but their effect on plant reproductive success is complex to detect (Page and Williams 2023) and to assess (Agüero et al. 2020). Honeybees are generalist pollinators and frequent plant visitors but may not necessarily bene t plant reproduction of all species (Ollerton et al. 2012), especially when they competitively replace native pollinators and become ineffective surrogates (Page et al. 2021). Conversely, in cases where native pollinators are rare or locally extinct, honeybees often boost pollination (Lomov et al. 2010;Hanna et al. 2013) or can even recover plant tness from reproductive collapse in fragmented habitat (Dick 2001). ...
Preprint
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Biological invasion is one of the leading threats to global biodiversity. Invasive species can change the structure and dynamics of landscapes, communities, and ecosystems, and even alter mutualistic relationships across species such as pollination. Orchids are one of the most threatened plant families globally and known to have established specialised pollination mechanism to reproduce, yet the impact of invasive bees on orchid reproduction has not been comprehensively assessed. We conduct a literature survey to document global patterns of the impact of invasive honeybees on orchids’ pollination. We then present a study case from Australian orchids, testing the extent to which introduced honeybees can successfully pollinate orchids across different degrees of habitat alteration, using Diuris brumalis and D. magnifica (Orchidaceae). Globally, Apis mellifera is the principal alien bee potentially involved in orchid pollination. We show that pollinator efficiency and fruit set in D. brumalis is higher in wild habitats in which both native bees and invasive honeybees are present, relative to altered habitat with introduced honeybees only. Pollen removal and fruit set of D. magnifica rise with native bees’ abundance whilst pollinator efficiency decreases with honeybee abundance and increases with habitat size. Complementarily to our findings, our literature survey suggests that the presence of introduced honeybees adversely impacts orchid pollination, likely via inefficient pollen transfer. Given the worldwide occurrence of introduced honeybees, we warn that some orchids may be negatively impacted by these alien pollinators, especially in altered and highly fragmented habitats where natural pollination networks are compromised.
... data are resource-intensive to collect and, therefore, remain rare (see Page et al., 2021 for a meta-analysis of available studies). ...
Article
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Despite the importance of insect pollination to produce marketable fruits, insect pollination management is limited by insufficient knowledge about key crop pollinator species. This lack of knowledge is due in part to (1) the extensive labour involved in collecting direct observations of pollen transport, (2) the variability of insect assemblages over space and time and (3) the possibility that pollinators may need access to wild plants as well as crop floral resources. We address these problems using strawberry in the United Kingdom as a case study. First, we compare two proxies for estimating pollinator importance: flower visits and pollen transport. Pollen‐transport data might provide a closer approximation of pollination service, but visitation data are less time‐consuming to collect. Second, we identify insect parameters that are associated with high importance as pollinators, estimated using each of the proxies above. Third, we estimated insects' use of wild plants as well as the strawberry crop. Overall, pollinator importances estimated based on easier‐to‐collect visitation data were strongly correlated with importances estimated based on pollen loads. Both frameworks suggest that bees (Apis and Bombus) and hoverflies (Eristalis) are likely to be key pollinators of strawberries, although visitation data underestimate the importance of bees. Moving beyond species identities, abundant, relatively specialised insects with long active periods are likely to provide more pollination services. Most insects visiting strawberry plants also carried pollen from wild plants, suggesting that pollinators need diverse floral resources. Identifying essential pollinators or pollinator parameters based on visitation data will reach the same general conclusions as those using pollen transport data, at least in monoculture crop systems. Managers may be able to enhance pollination service by preserving habitats surrounding crop fields to complement pollinators' diets and provide habitats for diverse life stages of wild pollinators.
... Some go further and refine these estimates of importance by multiplying them by single visit pollinator effectiveness, measured as pollen grains delivered, seeds set or probability of fruit set [16,32,33]. While measures of single-visit effectiveness of honeybees vary across plant species, meta-analyses have shown that, on average, their effectiveness is not different than the mean of other pollinators visiting the same species [25,34]. But if pollinators deliver pollen of different quality (e.g. ...
Article
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Most flowering plants require animal pollination and are visited by multiple pollinator species. Historically, the effects of pollinators on plant fitness have been compared using the number of pollen grains they deposit, and the number of seeds or fruits produced following a visit to a virgin flower. While useful, these methods fail to consider differences in pollen quality and the fitness of zygotes resulting from pollination by different floral visitors. Here we show that, for three common native self-compatible plants in Southern California, super-abundant, non-native honeybees (Apis mellifera L.) visit more flowers on an individual before moving to the next plant compared with the suite of native insect visitors. This probably increases the transfer of self-pollen. Offspring produced after honeybee pollination have similar fitness to those resulting from hand self-pollination and both are far less fit than those produced after pollination by native insects or by cross-pollination. Because honeybees often forage methodically, visiting many flowers on each plant, low offspring fitness may commonly result from honeybee pollination of self-compatible plants. To our knowledge, this is the first study to directly compare the fitness of offspring resulting from honeybee pollination to that of other floral visitors.
... As highlighted in discussions above, a major limitation of the plant-insect visitor data is that we only recorded flower visitation, which does not accurately indicate whether a particular insect visitor was actually contributing to the pollination of the flower, or if so, how effective it is as a pollinator compared with other visitors. However, previous pollination research has shown that the more frequent insect visitors are also typically the predominant pollinators (Ballantyne et al., 2017;Vazquez et al., 2012) and though our results should be interpreted with caution, particularly given the dominance of honeybees in our interactions (Page et al., 2021), such visitation data still serve as a useful first step in identifying the most common insect visitors to food crops grown in urban areas in the United Kingdom. The current study was part of a larger project that aimed to develop a simple citizen-science methodology to facilitate the participation of urban growers across different regions of the world in data collection on insect visitation to crops grown in urban areas. ...
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Societal Impact Statement Urban food production could contribute towards sustainable food provision and would also deliver benefits to biodiversity and the health of urban residents. Many crops rely on insect pollination, but urban pollinator populations are under‐studied. In this study, crop–pollinator interactions and pollination quality were quantified in urban allotments in the United Kingdom. A diversity of insects was observed visiting the flowers of food crops, with squash, cucumber and fruit trees attracting the most flower visitors. However, strawberry plants pollinated naturally by insects produced lower quality fruit than those receiving supplemental hand‐pollination. Urban crop pollination could therefore be improved through the provision of food and nesting habitats for insects. Summary Growing food in and around cities could be a partial solution to sustainably increasing food production in an urbanised world. Recent studies have shown that small‐scale urban farms can be as productive, if not more so, than large‐scale conventional farms. However, the question of which insects visit fruit and vegetable crops in urban areas and whether there are sufficiently large and diverse populations to provide adequate pollination to food crops has been little explored. Here we quantified plant–pollinator visitation networks in urban allotments in the city of Brighton and Hove, UK, to determine which insect groups visit commonly grown fruit and vegetable crops. We also conducted pollinator deficit experiments to determine whether there are sufficient pollinators in urban allotments to adequately pollinate two commonly grown insect‐pollinated crops, strawberries (Fragaria x ananassa) and runner beans (Phaseolus coccineus). A broad range of insect‐pollinated fruit and vegetable crops were grown in allotments and were visited by a diversity of insects spanning many taxonomic groups. We found little evidence that runner bean crop yields were limited by a lack of pollination; however, open‐pollinated strawberry plants produced more ‘unmarketable’ fruit suggesting there is potential for improving the delivery of pollination to strawberries grown in urban areas. Our results suggest there are potential opportunities for expanding urban food production to the benefit of both people and biodiversity. We recommend that future work should also consider the effectiveness of different insect groups in pollinating the various crops grown in urban areas.
... Some go further and refine these estimates of importance by multiplying them by single visit pollinator effectiveness, measured as pollen grains delivered, seeds set, or probability of fruit set [16,32,33]. While measures of single-visit effectiveness of honey bees vary across plant species, meta-analyses have shown that, on average, their effectiveness is not different than the mean of other pollinators visiting the same species [24,34]. But if pollinators deliver pollen of different quality that leads to strong differences in the fitness of the offspring produced, this will impact the importance of different pollinators to a plant's reproductive success. ...
Preprint
Most flowering plants require animal pollination and are visited by multiple pollinator species. Historically, the effects of pollinators on plant fitness have been compared using the number of pollen grains they deposit, and the number of seeds or fruits produced following a visit to a virgin flower. While useful, these methods fail to consider differences in pollen quality and the fitness of zygotes resulting from pollination by different floral visitors. Here we show that, for three common native self-compatible plants in Southern California, super-abundant, non-native honey bees ( Apis mellifera L.) visit more flowers on an individual before moving to the next plant compared to the suite of native insect visitors. This likely increases the transfer of self-pollen. Offspring produced after honey bee pollination have similar fitness to those resulting from hand self-pollination and both are far less fit than those produced after pollination by native insects or by cross-pollination. Because honey bees often forage methodically, visiting many flowers on each plant, low offspring fitness may commonly result from honey bee pollination of self-compatible plants. To our knowledge, this is the first study to directly compare the fitness of offspring resulting from honey bee pollination to that of other floral visitors.
... However, honeybees are an average pollinator in most crops [12][13][14][15][16]. When compared to their wild counterparts, they often fall short in terms of both pollen deposition and fruit set [17]. While wild bees are known to contribute to marketable yields, growers are hesitant to rely on their free services [18][19][20][21]. ...
Article
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Insect pests and pollinators can interact directly and indirectly to affect crop production; however, impacts of these interactions on marketable yield are little known. Thus, the evaluation of interactions between pests and pollinators are needed to best prioritize management efforts. Over 2 years, we evaluated the impact of pollinator visitation and/or beetle ( Acalymma vittatum ) infestation on fruit set and yield in seedless watermelon production. In 2020, we tested the main effect of pollinator visitation: two or eight honeybee visits, two wild bee visits, hand pollinated and open pollinated. In 2021, we crossed wild and managed pollinator visitation (two or four honeybee visits, two or four wild bee visits, hand pollinated and open pollinated) with varying beetle infestation levels (0, 3, 6 and 9 beetles/plant). In both years, wild bees contributed significantly to high fruit yields, and exclusive visitation from wild bees increased yield by a factor of 1.5–3 compared to honeybees. In 2021, pollination was the only significant factor for fruit set and marketable yield even when compared to the varying beetle infestation levels. These data advocate for a reprioritization of management, to conserve and protect wild bee pollination, which could be more critical than avoiding pest damage for ensuring high yields.
... Some meta-analyses conclude that honey bees are "average" pollinators of crop and wild flowers, but their pollinating contribution is usually enhanced by their numerical dominance (Hung et. al 2018, Page et al. 2021. ...
Article
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Differences in pollination effectiveness (PE) among pollinators have been widely documented. However, the morphological and behavioural traits underlying these differences have been less investigated. We used single-visit pollen deposition to apple flowers to explore the relationship between pollinator traits and PE. Our objectives were to determine which morphological and behavioural traits promote PE and to establish whether effective pollinators shared similar traits. For each flower visit we recorded duration, flower handling behaviour (top-working vs. side-working: flower visited from the top or from the side, respectively) and resource collected (pollen vs. nectar). For each pollinator species we measured body size, tongue length, hair density and hair length. PE depended on flower handling behaviour (top visitors were more effective than side visitors) and was positively correlated with body size and visit duration, but not with hairiness. We found large differences in PE among 11 pollinator species. The mean number of pollen grains deposited per visit ranged from 201.5 (Apis mellifera) to 833.7 (Andrena flavipes). In general, solitary bees (Andrena, Eucera, Osmia) were more effective than social bees (Bombus, Apis). Dipterans and beetles (Eristalis, muscoid flies, Tropinota, Oxythyrea) showed high to intermediate levels of PE. All effective pollinators were top-workers, but otherwise did not necessarily share similar traits. We conclude that there are different ways to be an effective pollinator. Our results provide a mechanism to explain the positive relationship between pollinator diversity and pollination service and can be used to predict PE in bowl-shaped flowers. Our approach can be easily adapted to other flower-pollinator systems.
... Previous studies showed that ecosystem service delivery is positively influenced by the richness of serviceproviding organisms like flower visitors (Dainese et al. 2019). Although honeybees (mainly the European honeybee Apis mellifera L.) are kept worldwide to provide crop pollination, other insects (such as wild bees, flies, beetles, wasps) contribute a lot more to total pollination than previously thought (Rader et al. 2016;Page et al. 2021). Floral abundance and richness are important for crop pollination services from unmanaged flower visitors Garibaldi et al. 2014), thus wild pollinator communities should be supported by increasing the floral abundance and richness in their environment. ...
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Recent biodiversity declines require action across sectors such as agriculture. The situation is particularly acute for arthropods, a species-rich taxon providing important ecosystem services. To counteract negative consequences of agricultural intensification, creating a less hostile agricultural “matrix” through growing crop mixtures can reduce harm for arthropods without yield losses. While grassland biodiversity experiments showed positive plant biodiversity effects on arthropods, experiments manipulating crop diversity and management intensity to study arthropods are lacking. Here, we experimentally manipulated crop diversity (1-3 species, fallows), crop species (wheat, faba bean, linseed, oilseed rape) and agrochemical input (high vs. low) and studied responses of arthropod biodiversity. Increasing crop diversity increased arthropod diversity and arthropod numbers. Mass-flowering crops attracted more arthropods than legumes or cereals. Integrating intercropping into agricultural systems could lead to a massive increase in flower visits (up to 15 million visits/ha), indicating benefits of intercropping for insect biodiversity and associated ecosystem services.
... In contrast, it is probable that the short time of secretion of I. sibirica nectaries may decrease pollinator frequency (i.e. number of visits), which may lead to a decrease in the quantity of pollen deposited onto the stigma (Földesi et al., 2021;Page et al., 2021) and reduce fruit and seed set (Kendall et al., 2020;Stavert et al., 2020). As highlighted by many researchers, insufficient pollinator visitation is the main and most important limitation of fruit and seed production, which is common and ubiquitous across angiosperms Negi et al., 2020;Meroi Arcerito et al., 2021). ...
Article
The insufficient pollinator visitation is the most important limitation of fruit and seed production, which is common and ubiquitous in entomophilous angiosperms. The scent and attractive colours with flower guides and such floral rewards as nectar, pollen, and oil are important attractants for insects visiting and pollinating flowers in the family Iridaceae. The aim of this study was to investigate the morphology of flowers and the micromorphology, anatomy, and ultrastructure of floral nectaries in the rare and endangered species Iris sibirica with the use of light, scanning, and transmission electron microscopes and histochemical assays. Osmophores in the form of papillae were located on the adaxial surface of outer tepals and on the abaxial surface of the stylodium channel. The nectaries were located on the inner surface of the perianth tube and were composed of a single-layered epidermis with papillae and several layers of glandular parenchyma with vascular bundles. I. sibirica nectaries represent the presecretory starch-accumulating type, where nectar is released for a short time immediately after flower opening. Nectar was produced throughout the flower lifespan in both male and female stages. It was secreted in the granulocrine mode and released through microchannels in the reticulate cuticle of nectary papillae. Transport of pre-nectar components proceeded via symplastic and apoplastic pathways. The nectary epidermal cells with papillae and glandular parenchyma cells contained total lipids, acidic lipids, and polysaccharides, whereas the epidermal cells with papillae additionally contained neutral lipids and polyphenol compounds. The nectaries and nectar production in I. sibirica flowers share the common location and follow several secretion patterns characteristic for the nectaries in some members of the family Iridaceae and the subfamily Iridoideae. Nevertheless, the mode of nectar release through the cuticle of epidermal papillae has been described in Iridaceae family for the first time. The visual, aromatic, and food attractants characteristic of I. sibirica flowers probably stimulate potential visits by pollinators, but the short nectar secretion period may limit the effectiveness of pollinators and sexual reproductive success.
... Approximately 75% of crop species benefit from pollinators, contributing to an estimated 9.5% of the value of the world agriculture production devoted to human food [1,147]. Other studies conducting meta-analysis have also shown the benefits of insect pollination for plant reproduction and yield in crops in general [148][149][150], in the plant species of particular natural habitats [151], and in particular crops, such as fava bean [152], oilseed rape [34], and tomato [153]. This review and meta-analysis shows that, overall, the yield parameters of crops in the family Brassicaceae benefit from insect pollination. ...
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This paper reviewed the effects of insect pollination on the yield parameters of plants from the family Brassicaceae presenting different breeding systems. Meta-analysis indicates that in both self-compatible and self-incompatible crop species, meta-analysis indicates that seed yield (Y), silique set (SQS), number of siliquae/plant (NSQ), and the number of seeds/silique (NSSQ) increase when plants are insect-pollinated compared to when there is no insect pollination. The weight of seeds (WS), however, increased in self-incompatible species but not in self-compatible ones as a result of insect pollination. Overall, the percentage of studies showing a positive effect of insect pollination on yield parameters was higher in self-incompatible than in self-compatible species. It was shown that the ability of self-compatible species to reproduce does not fully compensate for the loss of yield benefits in the absence of insect pollination. Cultivated Brassicaceae attract a wide variety of pollinators, with honeybees (Apis spp.) such as A. mellifera L., A. cerana F., A. dorsata F., and A. florea F. (Hymenoptera: Apidae); other Apidae, such as bumblebees (Bombus spp.) (Hymenoptera: Apidae); mining bees (Hymenoptera: Andrenidae); sweat bees (Hymenoptera: Halictidae); and hoverflies (Diptera: Syrphidae) constituting the most common ones. The benefits of insect pollination imply that pollinator conservation programs play a key role in maximizing yield in cruciferous crops.
... In contrast, when honeybees are the initial visitor or the only visitor in a visitation sequence, the effect of additional visits is additive; the cumulative effect of longer total visitation sequences, including those involving both bee species, is heavier fruit. Honeybees are, in general, less effective pollinators than wild bee species (Page et al., 2021). As such, an initial visit by a honeybee does not have the same limiting effect as a stingless bee, and the effect of subsequent floral visitation is likely more reflective of patterns in decreasing floral resource availability. ...
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Priority effects occur when the order of species arrival affects subsequent ecological processes. The order that pollinator species visit flowers may affect pollination through a priority effect, whereby the first visitor reduces or modifies the contribution of subsequent visits. We observed floral visitation to blueberry flowers from honeybees, stingless bees or a mixture of both species and investigated how (i) the initial visits differed in duration to later visits; and (ii) how the visit sequences from different pollinator taxa influenced fruit weight. Stingless bees visited blueberry flowers for significantly longer than honeybees and maintained their floral visit duration, irrespective of the number of preceding visits. In contrast, honeybee visit duration declined significantly with an increasing number of preceding visits. Fruit weight was positively associated with longer floral visit duration by honeybees but not from stingless bee or mixed species visitation. Fruit from mixed species visits were heavier overall than single species visits, because of a strong priority effect. An initial visit by a stingless bee fully pollinated the flower, limiting the pollination contribution of future visitors. However, after an initial honeybee visit, flowers were not fully pollinated and additional visitation had an additive effect upon fruit weight. Blueberries from flowers visited first by stingless bees were 60% heavier than those visited first by honeybees when total floral visitation was short (∼1 min). However, when total visitation time was long (∼ 8 min), blueberry fruit were 24% heavier when initial visits were from honeybees. Our findings highlight that the initial floral visit can have a disproportionate effect on pollination outcomes. Considering priority effects alongside traditional measures of pollinator effectiveness will provide a greater mechanistic understanding of how pollinator communities influence plant reproductive success.
... Beekeeping intensification in the Mediterranean Basin has led to a gradual replacement of wild bees by honey bees at wild and cultivated flowers in this region (Herrera 2020). This replacement is alarming because honey bees can only complement, and never fully substitute, the pollination services provided by wild insects (Ollerton et al. 2012, Garibaldi et al. 2013, Page et al. 2021. From a conservation perspective it is essential to understand whether the pollination benefit of introducing honey bees is counteracted by negative effects on wild pollinators. ...
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Maintaining the diversity of wild bees is a priority for preserving ecosystem function and promoting stability and productivity of agroecosystems. However, wild bee communities face many threats and beekeeping could be one of them, because honey bees may have a strong potential to outcompete wild pollinators when placed at high densities. Yet, we still know little about how beekeeping intensity affects wild bee diversity and their pollinator interactions. Here, we explore how honey bee density relates to wild bee diversity and the structure of their pollination networks in 41 sites on 13 Cycladic Islands (Greece) with similar landscapes but differing in beekeeping intensity. Our large‐scale study shows that increasing honey bee visitation rate had a negative effect on wild bee species richness and abundance, although the latter effect was relatively weak compared to the effect of other landscape variables. Competition for flowering resources (as indicated by a resource sharing index) increased with the abundance of honey bees, but the effect was more moderate for wild bees in family Apidae than for bees in other families, suggesting a stronger niche segregation in Apidae in response to honey bees. Honey bees also influenced the structure of wild bee pollination networks indirectly, through changes in wild bee richness. Low richness of wild bees in sites with high honey bee abundance resulted in wild bee networks with fewer links and lower linkage density. Our results warn against beekeeping intensification in these islands and similar hotspots of bee diversity, and shed light on how benefits to pollination services of introducing honey bees may be counterbalanced by detriments to wild bees and their ecosystem services.
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As pollinator-dependent crops continue to expand globally, management strategies are needed to meet the current demand for pollination services. Improving the efficiency of pollinators depends on knowledge about crop plant biology as well as pollinator behavior. In this sense, we will review the scope and challenges of implementing a targeted pollination strategy based on the behavioral individual and social plasticity of the honey bee Apis mellifera. Here we summarize current knowledge on the bees´ ability to perceive, learn and generalize floral odors, the bias of their foraging preferences after in-hive experiences and the transfer of food source information within the social context of the colony, all aspects that impact on foraging decisions and can be used to direct pollinators to target crops. We focused on describing how key olfactory cues that mimic crop floral scents are acquired in the hive and propagate among colony mates to guide foraging to specific crops. Knowledge gaps, including volatiles variability between flowers of the same or different crop varieties, alternative managed pollinators, and potential impact on food industry are discussed.
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Recent biodiversity declines require action across sectors such as agriculture. The situation is particularly acute for arthropods, a species‐rich taxon providing important ecosystem services. To counteract the negative consequences of agricultural intensification, creating a less hostile agricultural ‘matrix’ through growing crop mixtures can reduce harm for arthropods without yield losses. While grassland biodiversity experiments showed positive plant biodiversity effects on arthropods, experiments manipulating crop diversity and agrochemical input used to study arthropods are lacking. Here, we experimentally manipulated crop diversity (1–3 species, fallows), crop species (wheat, faba bean, linseed and oilseed rape) and agrochemical input (high vs. low) and studied responses of arthropod biodiversity. We tested whether arthropod responses were affected by crop diversity, mixtures and management. Additionally, we measured crop biomass. Crop biomass increased with crop diversity under high‐input management, while under low management intensity, biomass was highest in two‐species mixtures. Increasing crop diversity positively affected arthropod abundance and diversity, under both low‐ and high‐input management. Crop mixtures containing faba bean, linseed or oilseed rape had particularly high arthropod diversity. Mass‐flowering crops attracted more arthropods than legumes or cereals. Integrating intercropping into agricultural systems could increase flower visits by insects up to 1.5 million per hectare, thus likely also supporting pollination and pest‐control ecosystem services. Flower visitor network complexity increased in mixtures containing linseed and faba bean and under low‐input management. Intercropping can counteract insect declines in farmland by creating beneficial matrix habitat without compromising crop yield.
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Human‐mediated species introductions provide real‐time experiments in how communities respond to interspecific competition. For example, managed honey bees Apis mellifera (L.) have been widely introduced outside their native range and may compete with native bees for pollen and nectar. Indeed, multiple studies suggest that honey bees and native bees overlap in their use of floral resources. However, for resource overlap to negatively impact resource collection by native bees, resource availability must also decline, and few studies investigate impacts of honey bee competition on native bee floral visits and floral resource availability simultaneously. In this study, we investigate impacts of increasing honey bee abundance on native bee visitation patterns, pollen diets, and nectar and pollen resource availability in two Californian landscapes: wildflower plantings in the Central Valley and montane meadows in the Sierra. We collected data on bee visits to flowers, pollen and nectar availability, and pollen carried on bee bodies across multiple sites in the Sierra and Central Valley. We then constructed plant‐pollinator visitation networks to assess how increasing honey bee abundance impacted perceived apparent competition (PAC), a measure of niche overlap, and pollinator specialization (d'). We also compared PAC values against null expectations to address whether observed changes in niche overlap were greater or less than what we would expect given the relative abundances of interacting partners. We find clear evidence of exploitative competition in both ecosystems based on the following results: (1) honey bee competition increased niche overlap between honey bees and native bees, (2) increased honey bee abundance led to decreased pollen and nectar availability in flowers, and (3) native bee communities responded to competition by shifting their floral visits, with some becoming more specialized and others becoming more generalized depending on the ecosystem and bee taxon considered. Although native bees can adapt to honey bee competition by shifting their floral visits, the coexistence of honey bees and native bees is tenuous and will depend on floral resource availability. Preserving and augmenting floral resources is therefore essential in mitigating negative impacts of honey bee competition. In two California ecosystems, honey bee competition decreases pollen and nectar resource availability in flowers and alters native bee diets with potential implications for bee conservation and wildlands management.
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Insect pollinators, such as bees, butterflies, and flies, play a critical role in plant reproduction and the functioning of ecosystems. Their diversity is vital for efficient pollination, genetic variability in plants, and maintaining ecosystem resilience. However, these pollinators are under threat due to habitat loss, climate change, and pesticide use, resulting in population declines. To safeguard pollinators, it is imperative to take actions like creating pollinator-friendly gardens, avoiding pesticides, and promoting sustainable agriculture practices. The diversity of insect pollinators contributes to ecosystem resilience by preserving plant diversity and productivity. It also plays a significant role in global food security by enhancing crop yield, quality, and diversity. Challenges faced in pollinator-dependent agriculture include habitat loss, pesticide use, climate change, invasive species, and diseases. The decline in pollinator diversity has far-reaching consequences, including reduced crop yields and compromised ecosystem resilience. Conservation strategies focus on preserving diverse habitats, implementing agroecological practices, and raising public awareness about the importance of pollinators. Protecting and enhancing insect pollinator diversity is crucial for the overall health of ecosystems, agricultural systems, and the well-being of humans and the planet. Introduction Insect pollinators, including bees, butterflies, flies, beetles, and moths, play a fundamental role in plant reproduction and the functioning of ecosystems. The diversity of insect pollinators is essential for maintaining ecosystem resilience, promoting genetic diversity in plants, and ensuring global food security. Each type of pollinator has its own unique way of transferring pollen. For example, bees use their fuzzy bodies to collect pollen, while butterflies use their long tongues to reach into the depths of flowers. Insect pollinators are essential for the health of ecosystems and agriculture. Without them, many plants would not be able to reproduce, and we would have a much smaller variety of fruits, vegetables, and seeds to eat. However, insect pollinators are facing a number of threats, including habitat loss, climate change, and pesticide use. These threats are causing the populations of many insect pollinators to decline. It is important to take steps to protect insect pollinators. We can do this by planting pollinator-friendly gardens, avoiding the use of pesticides, and supporting sustainable agriculture practices. This article explores the significance of insect pollinator diversity, its drivers, and the potential consequences of its decline.
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Introduced species can have cascading effects on ecological communities, but indirect effects of species introductions are rarely the focus of ecological studies. For example, managed honey bees (Apis mellifera) have been widely introduced outside their native range and are increasingly dominant floral visitors. Multiple studies have documented how honey bees impact native bee communities through floral resource competition, but few have quantified how these competitive interactions indirectly affect pollination and plant reproduction. Such indirect effects are hard to detect because honey bees are themselves pollinators and may directly impact pollination through their own floral visits. The potentially huge but poorly understood impacts that non‐native honey bees have on native plant populations combined with increased pressure from beekeepers to place hives in U.S. National Parks and Forests makes exploring impacts of honey bee introductions on native plant pollination of pressing concern. In this study, we used experimental hive additions, field observations, as well as single‐visit and multiple‐visit pollination effectiveness trials across multiple years to untangle the direct and indirect impacts of increasing honey bee abundance on the pollination of an ecologically important wildflower, Camassia quamash. We found compelling evidence that honey bee introductions indirectly decrease pollination by reducing nectar and pollen availability and competitively excluding visits from more effective native bees. In contrast, the direct impact of honey bee visits on pollination was negligible, and, if anything, negative. Honey bees were ineffective pollinators and increasing visit quantity could not compensate for inferior visit quality. Indeed, although the effect was not statistically significant, increased honey bee visits had a marginally negative impact on seed production. Thus, honey bee introductions may erode longstanding plant‐pollinator mutualisms, with negative consequences for plant reproduction. Our study calls for a more thorough understanding of the indirect effects of species introductions and more careful coordination of hive placements.
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The productivity of approximately 75% of crops worldwide depends to some extent on insect pollination. However, while global agriculture is becoming more dependent on pollinators, wild populations of pollinators are declining. For this reason, hives of Apis mellifera (honeybees), the most widely used pollinator, are commonly placed in the fields; in recent years, alternative managed pollinators (AMPs) such as Bombus spp. or Osmia spp. have also been used. Thus, for evidence-based pollination management, we need to know whether the pollination service provided by AMPs can replace, complement or synergistically interact with that provided by honeybees. We asked: Does crop productivity differ between fields with honeybees and those with AMPs? Does productivity increase by incorporating AMPs in addition to managed honeybees? Do the effects of managed honeybees and AMPs interact? We performed a meta-analysis based on 28 studies on 20 crops. We estimated effect sizes (ln(R)) for crop productivity (fruit/seed set, fruit/seed quality and yield) from 73 comparisons between honeybees and an AMP, and 21 comparisons between honeybees alone and honeybees plus an AMP. Overall, we found no evidence of difference in crop productivity between honeybees and AMPs when managed separately. However, the productivity of crops pollinated by honeybees together with AMPs was 22% ± 6 (SE) higher than that of crops pollinated only by honeybees. Moreover, we found a weak evidence of a positive effect of beehive density on crop productivity when an AMP was added, suggesting a synergistic interaction between honeybees and AMPs. We conclude that, on average, honeybee performance is similar to that of AMPs, and that increasing the number of managed pollinator species can improve crop productivity in the short-term, particularly in systems with impoverished pollinator faunas. More generally, this review confirms the positive effect of pollinator diversity on pollination service, suggesting this can be partly recreated using a suite of managed pollinators.
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Background The spatial structure and size of plant populations affect foraging choices of pollinators and, consequently, pollen transfer within and between populations. Aims To understand pollination patterns in relation to population size and pollinator selectivity we quantified patch size and pollen flow in natural populations of Richardia grandiflora, a neotropical perennial herb. Methods We assessed the composition of flower visitors, the number of flowers visited, and the frequency of visits in patches of different sizes. In addition, we measured the inter- and intra-patch-size pollen transfer (pollen from patches of different sizes and from the same patch/same patch size, respectively) using fluorescent dyes as pollen analogues. Results We recorded 22 species of insects, mainly bees, with Apis mellifera standing out as the major visitor in medium and large size patches. Large patches received a greater richness and abundance of flower visitors, had more flowers visited, and greater pollen flow overall (62%), representing 62% of the total intra-patch-size and 64% of inter-patch-size pollen flow. Alternatively, small patches represented 16% of the total intra-patch-size and 5% of the inter-patch-size pollen flow. Native bee species were found almost exclusively in small patches. Conclusion Small patches are important for sustaining rare floral visitors while large patches are more relevant for diverse pollination events.
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1. Many insect species provide essential pollination services. However, the amount of pollen deposited onto a stigma when visiting a flower (“single visit pollen deposition”, SVD) can vary greatly among taxa depending on morphological traits of pollinators. Further, SVD is commonly measured using one of two methods (‘static’: waiting for an insect to visit a flower present on plant, and ‘active’: removing the flower and presenting it to a flower visitor) that may also differ in their effectiveness. 2. To gain a more comprehensive understanding of how SVD compares among pollinators, we conducted a hierarchical meta-analysis using data from 28 studies identified by a systematic review. These contained SVD data for 94 bee and 33 fly taxa (hereafter “wild pollinators”), across 30 plant species from which we included 127 observations. In the analysis of each study, we used the western honey bee (Apis mellifera) as a comparator species. 3. Wild pollinators deposited more pollen onto stigmas per single visit than honeybees, and those with larger body deposited significantly more pollen than smaller ones. Of the two methodological approaches to assess SVD, ‘static’ versus ‘active’, we found no significant difference regarding the amount of deposited pollen. 4. Synthesis and applications. Our meta-analysis highlights the breadth of wild pollinators that contribute to pollination effectiveness via their delivery of pollen to many crop and non-crop plant species. However, just 25% of the observations assessed the amount of pollen deposited by fly species. Our findings point to the need to further quantify the pollination effectiveness of non-bee pollinators as studies have largely focused on managed and wild bee species.
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Evidence for pollinator declines largely originates from mid-latitude regions in North America and Europe. Geographical heterogeneity in pollinator trends combined with geographical biases in pollinator studies can produce distorted extrapolations and limit understanding of pollinator responses to environmental changes. In contrast with the declines experienced in some well-investigated European and North American regions, honeybees seem to have increased recently in some areas of the Mediterranean Basin. Because honeybees can have negative impacts on wild bees, it was hypothesized that a biome-wide alteration in bee pollinator assemblages may be underway in the Mediterranean Basin involving a reduction in the relative number of wild bees. This hypothesis was tested using published quantitative data on bee pollinators of wild and cultivated plants from studies conducted between 1963 and 2017 in 13 countries from the European, African and Asian shores of the Mediterranean Sea. The density of honeybee colonies increased exponentially and wild bees were gradually replaced by honeybees in flowers of wild and cultivated plants. The proportion of wild bees at flowers was four times greater than that of honeybees at the beginning of the period, the proportions of both groups becoming roughly similar 50 years later. The Mediterranean Basin is a world biodiversity hotspot for wild bees and wild bee-pollinated plants, and the ubiquitous rise of honeybees to dominance as pollinators could in the long run undermine the diversity of plants and wild bees in the region.
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How insects promote crop pollination remains poorly understood in terms of the contribution of functional trait differences between species. We used meta-analyses to test for correlations between community abundance, species richness and functional trait metrics with oilseed rape yield, a globally important crop. While overall abundance is consistently important in predicting yield, functional divergence between species traits also showed a positive correlation. This result supports the complementarity hypothesis that pollination function is maintained by non-overlapping trait distributions. In artificially constructed communities (mesocosms), species richness is positively correlated with yield, although this effect is not seen under field conditions. As traits of the dominant species do not predict yield above that attributed to the effect of abundance alone, we find no evidence in support of the mass ratio hypothesis. Management practices increasing not just pollinator abundance, but also functional divergence, could benefit oilseed rape agriculture.
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The honeybee is the primary managed species worldwide for both crop pollination and honey production. Owing to beekeeping activity, its high relative abundance potentially affects the structure and functioning of pollination networks in natural ecosystems. Given that evidences about beekeeping impacts are restricted to observational studies of specific species and theoretical simulations, we still lack experimental data to test for their larger-scale impacts on biodiversity. Here we used a three-year field experiment in a natural ecosystem to compare the effects of pre- and post-establishment stages of beehives on the pollination network structure and plant reproductive success. Our results show that beekeeping reduces the diversity of wild pollinators and interaction links in the pollination networks. It disrupts their hierarchical structural organization causing the loss of interactions by generalist species, and also impairs pollination services by wild pollinators through reducing the reproductive success of those plant species highly visited by honeybees. High-density beekeeping in natural areas appears to have lasting, more serious negative impacts on biodiversity than was previously assumed.
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We present V.PhyloMaker, a freely available package for R designed to generate phylogenies for vascular plants. The mega‐tree implemented in V.PhyloMaker (i.e., GBOTB.extended.tre), which was derived from two recently published mega‐trees and includes 74,533 species and all families of extant vascular plants, is the largest dated phylogeny for vascular plants. V.PhyloMaker can generate phylogenies for very large species lists (the largest species list that we tested included 314,686 species). V.PhyloMaker generates phylogenies at a fast speed, much faster than other phylogeny‐generating packages. Our tests of V.PhyloMaker show that generating a phylogeny for 60,000 species requires less than six hours. V.PhyloMaker includes an approach to attach genera or species to their close relatives in a phylogeny. We provide a simple example in this paper to show how to use V.PhyloMaker to generate phylogenies. This article is protected by copyright. All rights reserved.
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The pollination effectiveness of a flower visitor has traditionally been measured as the product of a quantity component that depends on the frequency of interaction and a quality component that measures the per‐visit effects on plant reproduction. We propose that this could be complemented with a genetic component informing about each pollinator's contribution to the genetic diversity and composition of the plant progeny. We measured the quantity and quality components of effectiveness of most pollinator functional groups of the generalist herb Erysimum mediohispanicum . We used 10 microsatellite markers to calculate the genetic component as the diversity of sires among siblings and included it into the calculation of the pollination effectiveness. Functional groups varied in the quantity and quality components, which were shown to be decoupled. Functional groups also differed in the genetic component. This component changed the estimates of pollination effectiveness, increasing the differences between some functional groups and modifying the pollination effectiveness landscape. We demonstrate that including the genetic component in the calculation of the pollination effectiveness may allow a more complete quantification of the contribution of each pollinator to the reproductive success of a plant, providing information on its mating patterns and long‐term fitness.
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REVIEW The male fitness pathway, from pollen production to ovule fertilization, is thought to strongly influence reproductive trait evolution in animal-pollinated plants. This pathway is characterized by multiple avenues of pollen loss which may lead to reductions in male fitness. However, empirical data on the mechanistic processes leading to pollen loss during transport are limited, and we therefore lack a comprehensive understanding of how male fitness is influenced by each step in the pollination process. This review assesses the history of studying male function in plants and identifies critical gaps in our understanding of the ecology and evolution of pollen transport. We explore male reproductive function along the steps of the pathway to paternity and discuss evolutionary options to overcome barriers to siring success. In particular, we present a newly emerging idea that bodies of pollinators function as a dynamic arena facilitating intense male–male competition, where pollen of rival males is constantly covered or displaced by competitors. This perspective extends the pollen-competitive arena beyond the confines of the stigma and style, and highlights the opportunity for important new breakthroughs in the study of male reproductive strategies and floral evolution. **** FREE PDF available at journal website:**** doi.org/10.1093/aob/mcy167
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Premise of the Study: Large phylogenies can help shed light on macroevolutionary patterns that inform our understanding of fundamental processes that shape the tree of life. These phylogenies also serve as tools that facilitate other systematic, evolutionary, and ecological analyses. Here we combine genetic data from public repositories (GenBank) with phylogenetic data (Open Tree of Life project) to construct a dated phylogeny for seed plants. Methods: We conducted a hierarchical clustering analysis of publicly available molecular data for major clades within the Spermatophyta. We constructed phylogenies of major clades, estimated divergence times, and incorporated data from the Open Tree of Life project, resulting in a seed plant phylogeny. We estimated diversification rates, excluding those taxa without molecular data. We also summarized topological uncertainty and data overlap for each major clade. Key Results: The trees constructed for Spermatophyta consisted of 79,881 and 353,185 terminal taxa; the latter included the Open Tree of Life taxa for which we could not include molecular data from GenBank. The diversification analyses demonstrated nested patterns of rate shifts throughout the phylogeny. Data overlap and inference uncertainty show significant variation throughout and demonstrate the continued need for data collection across seed plants. Conclusions: This study demonstrates a means for combining available resources to construct a dated phylogeny for plants. However, this approach is an early step and more developments are needed to add data, better incorporating underlying uncertainty, and improve resolution. The methods discussed here can also be applied to other major clades in the tree of life.
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The western honey bee (Apis mellifera) is the most frequent floral visitor of crops worldwide, but quantitative knowledge of its role as a pollinator outside of managed habitats is largely lacking. Here we use a global dataset of 80 published plant-pollinator interaction networks as well as pollinator effectiveness measures from 34 plant species to assess the importance of A. mellifera in natural habitats. Apis mellifera is the most frequent floral visitor in natural habitats worldwide, averaging 13% of floral visits across all networks (range 0-85%), with 5% of plant species recorded as being exclusively visited by A. mellifera For 33% of the networks and 49% of plant species, however, A. mellifera visitation was never observed, illustrating that many flowering plant taxa and assemblages remain dependent on non-A. mellifera visitors for pollination. Apis mellifera visitation was higher in warmer, less variable climates and on mainland rather than island sites, but did not differ between its native and introduced ranges. With respect to single-visit pollination effectiveness, A. mellifera did not differ from the average non-A. mellifera floral visitor, though it was generally less effective than the most effective non-A. mellifera visitor. Our results argue for a deeper understanding of how A. mellifera, and potential future changes in its range and abundance, shape the ecology, evolution, and conservation of plants, pollinators, and their interactions in natural habitats.
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Flower-visiting bees collect large quantities of pollen to feed their offspring. Pollen deposited in the bees’ transport organs is lost for the flowers’ pollination. It has been hypothesised that specific body areas, bees cannot groom, serve as ‘safe sites’ for pollen transfer between flowers. For the first time, we experimentally demonstrated the position, area and pollen amount of safe sites at the examples of Apis mellifera and Bombus terrestris by combining artificial contamination of the bees’ body with pine or sunflower pollen and the subsequent bees’ incomplete grooming. We found safe sites on the forehead, the dorsal thorax and waist, and on the dorsal and ventral abdomen of the bees. These areas were less groomed by the bees’ legs. The largest amount of pollen was found on the waist, followed by the dorsal areas of thorax and abdomen. At the example of Salvia pratensis, S. officinalis and Borago officinalis, we experimentally demonstrated with fluorescent dye that the flowers’ pollen-sacs and stigma contact identical safe sites. These results confirm that pollen deposition on the bees’ safe sites improves pollen transfer to stigmas of conspecific flowers sti. Future research will demonstrate the importance of safe sites for plant pollination under field conditions.
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Accurate predictions of pollination service delivery require a comprehensive understanding of the interactions between plants and flower visitors. To improve measurements of pollinator performance underlying such predictions, we surveyed visitation frequency, pollinator effectiveness (pollen deposition ability) and pollinator importance (the product of visitation frequency and effectiveness) of flower visitors in a diverse Mediterranean flower meadow. With these data we constructed the largest pollinator importance network to date and compared it with the corresponding visitation network to estimate the specialisation of the community with greater precision. Visitation frequencies at the community level were positively correlated with the amount of pollen deposited during individual visits, though rarely correlated at lower taxonomic resolution. Bees had the highest levels of pollinator effectiveness, with Apis, Andrena, Lasioglossum and Osmiini bees being the most effective visitors to a number of plant species. Bomblyiid flies were the most effective non-bee flower visitors. Predictions of community specialisation (H2′) were higher in the pollinator importance network than the visitation network, mirroring previous studies. Our results increase confidence in existing measures of pollinator redundancy at the community level using visitation data, while also providing detailed information on interaction quality at the plant species level.
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Our growing human population will be increasingly dependent on bees and other pollinators that provide the essential delivery of pollen to crop flowers during bloom. Within the context of challenges to crop pollinators and crop production, farm managers require strategies that can reliably provide sufficient pollination to ensure maximum economic return from their pollinator-dependent crops. There are unexploited opportunities to increase yields by managing insect pollination, especially for crops that are dependent on insect pollination for fruit set. We introduce the concept of Integrated Crop Pollination as a unifying theme under which various strategies supporting crop pollination can be developed, coordinated, and delivered to growers and their advisors. We emphasize combining tactics that are appropriate for the crop’s dependence on insect-mediated pollination, including the use of wild and managed bee species, and enhancing the farm environment for these insects through directed habitat management and pesticide stewardship. This should be done within the economic constraints of the specific farm situation, and so we highlight the need for flexible strategies that can help growers make economically-based ICP decisions using support tools that consider crop value, yield benefits from adoption of ICP components, and the cost of the practices. Finally, education and technology transfer programs will be essential for helping land managers decide on the most efficient way to apply ICP to their unique situations. Building on experiences in North America and beyond, we aim to provide a broad framework for how crop pollination can help secure future food production and support society’s increasing need for nutritious diets.
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Pollinators that collect pollen – and specifically, pollen-specialist bees – are often considered to be the best pollinators of a (host) plant. Although pollen collectors and pollen specialists often benefit host plants, especially in the pollen that they deliver (their pollination “effectiveness”), they can also exact substantial costs because they are motivated to collect as much pollen as possible, reducing the proportion of pollen removed that is subsequently delivered to stigmas (their pollination “efficiency”). From the plant perspective, pollen grains that do not pollinate conspecific stigmas are “wasted”, and potentially costly. We measured costs and benefits of nectar-collecting, pollen-collecting, and pollen-specialist pollinator visitation to the spring ephemeral Claytonia virginica. Visits by the pollen-specialist bee Andrena erigeniae depleted pollen quickly and thoroughly. Although all pollinators delivered roughly the same number of grains, the pollen specialist contributed most to C. virginica pollen delivery because of high visitation rates. However, the pollen specialist also removed a large number of grains; this removal may be especially costly because it resulted in the depletion of pollen grains in C. virginica populations. While C. virginica appears to rely on pollen transfer by the pollen specialist in these populations, nectar-collecting visitors could provide the same benefit at a lower cost if their visitation rates increased. Pollen depletion affects a pollinator's value to plants, but is frequently overlooked. If they lower the effectiveness of future floral visitors, visits by A. erigeniae females to C. virginica may be more detrimental than beneficial compared to other pollinators and may, in some circumstances, reduce plant fitness rather than increase it. Therefore, A. erigeniae and C. virginica may vary in their degree of mutualism depending on the ecological context.
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Systematic reviews and meta-analyses have become increasingly important in health care. Clinicians read them to keep up to date with their field [1],[2], and they are often used as a starting point for developing clinical practice guidelines. Granting agencies may require a systematic review to ensure there is justification for further research [3], and some health care journals are moving in this direction [4]. As with all research, the value of a systematic review depends on what was done, what was found, and the clarity of reporting. As with other publications, the reporting quality of systematic reviews varies, limiting readers' ability to assess the strengths and weaknesses of those reviews. Several early studies evaluated the quality of review reports. In 1987, Mulrow examined 50 review articles published in four leading medical journals in 1985 and 1986 and found that none met all eight explicit scientific criteria, such as a quality assessment of included studies [5]. In 1987, Sacks and colleagues [6] evaluated the adequacy of reporting of 83 meta-analyses on 23 characteristics in six domains. Reporting was generally poor; between one and 14 characteristics were adequately reported (mean = 7.7; standard deviation = 2.7). A 1996 update of this study found little improvement [7]. In 1996, to address the suboptimal reporting of meta-analyses, an international group developed a guidance called the QUOROM Statement (QUality Of Reporting Of Meta-analyses), which focused on the reporting of meta-analyses of randomized controlled trials [8]. In this article, we summarize a revision of these guidelines, renamed PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses), which have been updated to address several conceptual and practical advances in the science of systematic reviews (Box 1). Box 1: Conceptual Issues in the Evolution from QUOROM to PRISMA Completing a Systematic Review Is an Iterative Process The conduct of a systematic review depends heavily on the scope and quality of included studies: thus systematic reviewers may need to modify their original review protocol during its conduct. Any systematic review reporting guideline should recommend that such changes can be reported and explained without suggesting that they are inappropriate. The PRISMA Statement (Items 5, 11, 16, and 23) acknowledges this iterative process. Aside from Cochrane reviews, all of which should have a protocol, only about 10% of systematic reviewers report working from a protocol [22]. Without a protocol that is publicly accessible, it is difficult to judge between appropriate and inappropriate modifications.
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Interaction networks are widely used as tools to understand plant–pollinator communities, and to examine potential threats to plant diversity and food security if the ecosystem service provided by pollinating animals declines. However, most networks to date are based on recording visits to flowers, rather than recording clearly defined effective pollination events. Here we provide the first networks that explicitly incorporate measures of pollinator effectiveness (PE) from pollen deposition on stigmas per visit, and pollinator importance (PI) as the product of PE and visit frequency. These more informative networks, here produced for a low diversity heathland habitat, reveal that plant–pollinator interactions are more specialized than shown in most previous studies. At the studied site, the specialization index H 0 2 was lower for the visitation network than the PE network, which was in turn lower than H 0 2 for the PI network. Our study shows that collecting PE data is feasible for community-level studies in low diversity communities and that including information about PE can change the structure of interaction networks. This could have important consequences for our understanding of threats to pollination systems.
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There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.
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Peach Prunus persica (L.) Batsch is self-compatible and largely self-fertile, but under greenhouse conditions pollinators must be introduced to achieve good fruit set and quality. Because little work has been done to assess the effectiveness of different pollinators on peach trees under greenhouse conditions, we studied 'Okubo' peach in greenhouse tunnels near Beijing between 2012 and 2014. We measured pollen deposition, pollen-tube growth rates, ovary development, and initial fruit set after the flowers were visited by either of two managed pollinators: bumblebees, Bombus patagiatus Nylander, and honeybees, Apis mellifera L. The results show that B. patagiatus is more effective than A. mellifera as a pollinator of peach in greenhouses because of differences in two processes. First, B. patagiatus deposits more pollen grains on peach stigmas than A. mellifera, both during a single visit and during a whole day of open pollination. Second, there are differences in the fertilization performance of the pollen deposited. Half of the flowers visited by B. patagiatus are fertilized 9–11 days after bee visits, while for flowers visited by A. mellifera, half are fertilized 13–15 days after bee visits. Consequently, fruit development is also accelerated by bumblebees, showing that the different pollinators have not only different pollination efficiency, but also influence the subsequent time course of fertilization and fruit set. Flowers visited by B. pata-giatus show faster ovary growth and ultimately these flowers produce more fruit. Our work shows that pollinators may influence fruit production beyond the amount of pollen delivered. We show that managed indigenous bumblebees significantly outperform introduced honey-bees in increasing peach initial fruit set under greenhouse conditions.
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Bees, hoverflies and butterflies are taxa frequently studied as pollinators in agricultural and conservation contexts. Although there are many records of non-syrphid Diptera visiting flowers, they are generally not regarded as important pollinators. We use data from 30 pollen-transport networks and 71 pollinator-visitation networks to compare the importance of various flower-visiting taxa as pollen-vectors. We specifically compare non-syrphid Diptera and Syrphidae to determine whether neglect of the former in the literature is justified. We found no significant difference in pollen-loads between the syrphid and non-syrphid Diptera. Moreover, there was no significant difference in the level of specialization between the two groups in the pollen-transport networks, though the Syrphidae had significantly greater visitation evenness. Flower visitation data from 33 farms showed that non-syrphid Diptera made up the majority of the flower-visiting Diptera in the agricultural studies (on average 82% abundance and 73% species richness), and we estimate that non-syrphid Diptera carry 84% of total pollen carried by farmland Diptera. As important pollinators, such as bees, have suffered serious declines, it would be prudent to improve our understanding of the role of non-syrphid Diptera as pollinators.
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The foraging behavior and pollinating efficacy of Osmia cornuta (Latreille) and Apis mellifera L. were studied in an orchard of ‘Delicious’ apple, Malus domestica Borkh, in northeastern Spain. Yields after one single visit were more than five times higher in flowers visited by O. cornuta than in those visited by A. mellifera nectar gatherers. This is attributed to the lower rate of stigma contact in A. mellifera visits, rather than to insufficient deposition of compatible pollen when the stigmas are contacted. A. mellifera pollen collectors had very high rates of stigma contact, but they were very scarce (3%) on ‘Delicious’ flowers despite the presence of abundant brood in their hives. One single visit per flower by O. cornuta produced commercial fruit set (27.4%) and fruit size (>70 mm diameter). Based on cell production, average number of trips required to provision a male and a female cell, and flower visiting rates, it is estimated that a mean of 22,252 apple flower visits per female O. cornuta were made during the 15-d flowering period. This result indicates that 530 nesting O. cornuta females per hectare are enough to provide adequate apple pollination.
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Native, wild bees are important pollinators for both crop and wild plants. With concerns over the availability and cost of managed honeybees, attention has turned to native, wild bees as crop pollinators. However, the ability of native, wild bees to provide sufficient pollination may depend on their populations at local scales. Therefore, at the farm scale, we examined the pollination contribution of both native, wild bees and managed honeybees to apples and assessed the relative importance of bee abundance vs. species richness. Over three growing seasons, apple fruit set, bee abundance and bee species richness were measured at orchards in Wisconsin, half of which used managed honeybees, thus allowing us to independently examine the contribution of native, wild bees to fruit set. We additionally conducted observations of honeybees and wild bees foraging on apple blossoms in order to examine functional complementarity. We found that apples are highly dependent on animal pollinators. However, fruit set was not significantly higher at orchards with managed honeybees, nor did it increase with the number of honeybees per orchard. Instead, fruit set significantly increased with the species richness of native, wild bees during bloom. Honeybees and wild bees showed different foraging preferences: honeybees more frequently visited apple flowers on densely blooming trees, while wild bees showed no preference for floral density, thereby evenly visiting trees throughout the orchard. Synthesis and applications . Our results show that native, wild bees play a significant and unique role in apple pollination within our region and cannot therefore be replaced by managed bees. Moreover, our findings suggest that bee conservation efforts should focus specifically on maintaining or increasing bee species richness in order to improve pollination and crop yields.
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The relative importance of specialized and generalized plant‐pollinator relationships is contentious, yet analyses usually avoid direct measures of pollinator quality (effectiveness), citing difficulties in collecting such data in the field and so relying on visitation data alone. We demonstrate that single‐visit deposition ( SVD ) of pollen on virgin stigmas is a practical measure of pollinator effectiveness, using 13 temperate and tropical plant species. For each flower the most effective pollinator measured from SVD was as predicted from its pollination syndrome based on traditional advertisement and reward traits. Overall, c . 40% of visitors were not effective pollinators (range 0–78% for different flowers); thus, flower–pollinator relationships are substantially more specialized than visitation alone can reveal. Analyses at species level are crucial, as significant variation in SVD occurred within both higher‐level taxonomic groups (genus, family) and within functional groups. Other measures sometimes used to distinguish visitors from pollinators (visit duration, frequency, or feeding behaviour in flowers) did not prove to be suitable proxies. Distinguishing between ‘pollinators’ and ‘visitors’ is therefore crucial, and true ‘pollination networks’ should include SVD to reveal pollinator effectiveness ( PE ). Generating such networks, now underway, could avoid potential misinterpretations of the conservation values of flower visitors, and of possible extinction threats as modelled in existing networks.
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Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.
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Introduced honeybees have had a large impact on native ecosystems by disrupting native plant–pollinator interactions. However, little is known of the effect of honeybees on reproduction of bumblebee-pollinated plants. Seasonal displacement of native bumblebees by introduced honeybees (Apis mellifera and A. cerana) was observed in Pedicularis densispica, endemic to Hengduan Mountains, China, providing an opportunity for honeybee presence/absence comparisons. Five-year field surveys were conducted in one frequently disturbed population at Yila Pasture (YP). We compared pollination effectiveness (combinations of visitation rate, efficiency in pollen transfer, and potential geitonogamy) between native and introduced managed bees. The total visitation rate of native bees and subsequent reproductive output decreased progressively, but honeybee introduction resulted in at least twofold increase in visitation and 70 % increase in seed set. In general, native bumblebees, which have larger bodies and longer proboscises and spent more time probing single flowers, were more efficient than honeybees in terms of pollen removal and pollen deposition during first visits to virgin flowers. Compared with bumblebees, honeybees visited markedly fewer flowers in sequence within individual plants, potentially reducing geitonogamous pollination. Our data highlight that introduced honeybees can provide pollination service in terms of both quantity and quality for P. densispica. We suggest honeybee introduction as an effective way to augment pollination of P. densispica at disturbed and isolated sites.
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Understanding the functional impacts of pollinator species losses on plant populations is critical given ongoing pollinator declines. Simulation models of pollination networks suggest that plant communities will be resilient to losing many or even most of the pollinator species in an ecosystem. These predictions, however, have not been tested empirically and implicitly assume that pollination efficacy is unaffected by interactions with interspecific competitors. By contrast, ecological theory and data from a wide range of ecosystems show that interspecific competition can drive variation in ecological specialization over short timescales via behavioral or morphological plasticity, although the potential implications of such changes in specialization for ecosystem functioning remain unexplored. We conducted manipulative field experiments in which we temporarily removed single pollinator species from study plots in subalpine meadows, to test the hypothesis that interactions between pollinator species can shape individual species' functional roles via changes in foraging specialization. We show that loss of a single pollinator species reduces floral fidelity (short-term specialization) in the remaining pollinators, with significant implications for ecosystem functioning in terms of reduced plant reproduction, even when potentially effective pollinators remained in the system. Our results suggest that ongoing pollinator declines may have more serious negative implications for plant communities than is currently assumed. More broadly, we show that the individual functional contributions of species can be dynamic and shaped by the community of interspecific competitors, thereby documenting a distinct mechanism for how biodiversity can drive ecosystem functioning, with potential relevance to a wide range of taxa and systems.
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On average, nectar-collecting bumble bees Bombus deposited 0.6% of the pollen removed from the flowers of Erythronium grandiflorum (Liliaceae) onto the stigmas of subsequently visited flowers. Because the proportion deposited declined as the amount removed increased, an individual plant would maximise its total pollen dispersal by relying on many pollen-removing visits while limiting the pollen removed by each pollinator. This restriction of pollen removal could be achieved by a plant presenting only a small portion of its pollen at one time (packaging) and/or by limiting the amount of presented pollen that a pollinator removes during a single visit (dispensing). The restriction of pollen removal required to maximize the expected total deposition on stigmas depends on the number of pollinator visits a plant receives, variation in the frequency of visits, and the pattern of pollen removal during a series of visits. Many aspects of floral biology contribute to a plant's ability to restrict pollen removal, including inflorescence size, flower morphology, anthesis patterns, nectar production, and dichogamy. Selection increasing paternal fitness of animal-pollinated plants could therefore elicit one of a variety of evolutionary responses; the specific response will depend on characteristics of both the plant and the pollinator. -Authors
Article
Species that persist in small populations isolated by habitat destruction may experience reproductive failure. Self‐incompatible plants face dual threats of mate‐limitation and competition with co‐flowering plants for pollination services. Such competition may lower pollinator visitation, increase heterospecific pollen transfer and reduce the likelihood that a visit results in successful pollination. To understand how isolation from mates and competition with co‐flowering species contribute to reproductive failure in fragmented habitat, we conducted an observational study of a tallgrass prairie perennial Echinacea angustifolia . We quantified the isolation of focal individuals from mates, characterized species richness and counted inflorescences within 1 m radius, observed pollinator visitation, collected pollinators, quantified pollen loads on pollinators and on Echinacea stigmas, and measured pollination success. Throughout the season, we sampled 223 focal plants across 10 remnant prairie sites. We present evidence that both co‐flowering species and isolation from mates substantially limit reproduction in Echinacea . As the flowering season progressed, the probability of pollinator visitation to focal plants decreased and evidence for pollen‐limited reproduction increased. Pollinators were most likely to visit Echinacea plants from low‐richness floral neighbourhoods with close potential mates, or plants from high‐richness neighbourhoods with distant potential mates. Frequent visitation only increased pollination success in the former case, likely because Echinacea in high‐richness floral neighbourhoods received low‐quality visits. Synthesis . In Echinacea, reproduction was limited by isolation from potential mates and the richness of co‐flowering species. These aspects of the floral neighbourhood influenced pollinator visitation and pollination success, although conditions that predicted high visitation did not always lead to high pollination success. These results reveal how habitat modification and destruction, which influence floral neighbourhood and isolation from conspecific mates, can differentially affect various stages of reproductive biology in self‐incompatible plants. Our results suggest that prairie conservation and restoration efforts that promote patches of greater floral diversity may improve reproductive outcomes in fragmented habitats.
Article
The alarming loss of pollinator diversity world‐wide can reduce the productivity of pollinator‐dependent crops, which could have economic impacts. However, it is unclear to what extent the loss of a key native pollinator species affects crop production and farmer's profits. By experimentally manipulating the presence of colonies of a native bumblebee species Bombus pauloensis in eight apple orchards in South Argentina, we evaluated the impact of losing natural populations of a key native pollinator group on (a) crop yield, (b) pollination quality, and (c) farmer's profit. To do so, we performed a factorial experiment of pollinator exclusion (yes/no) and hand pollination (yes/no). Our results showed that biotic pollination increased ripe fruit set by 13% when compared to non‐biotic pollination. Additionally, fruit set and the number of fruits per apple tree was reduced by less than a half in those orchards where bumblebees were absent, even when honeybees were present at high densities. Consequently, farmer's profit was 2.4‐fold lower in farms lacking bumblebees than in farms hosting both pollinator species. The pollination experiment further suggested that the benefits of bumblebees could be mediated by improved pollen quality rather than quantity. Synthesis and applications . This study highlights the pervasive consequences of losing key pollinator functional groups, such as bumblebees, for apple production and local economies. Adopting pollinator‐friendly practices such as minimizing the use of synthetic inputs or restoring/maintaining semi‐natural habitats at farm and landscape scales, will have the double advantage of promoting biodiversity conservation, and increasing crop productivity and profitability for local farmers. Yet because the implementation of these practices can take time to deliver results, the management of native pollinator species can be a provisional complementary strategy to increase economic profitability of apple growers in the short term.
Article
Premise: Variation in pollinator effectiveness may contribute to pollen limitation in fragmented plant populations. In plants with multiovulate ovaries, the number of conspecific pollen grains per stigma often predicts seed set and is used to quantify pollinator effectiveness. In the Asteraceae, however, florets are uniovulate, which suggests that the total amount of pollen deposited per floret may not measure pollinator effectiveness. We examined two aspects of pollinator effectiveness-effective pollen deposition and effective pollen movement-for insects visiting Echinacea angustifolia, a composite that is pollen limited in small, isolated populations. Methods: We filmed insect visits to Echinacea in two prairie restorations and used these videos to quantify behavior that might predict effectiveness. To quantify effective pollen deposition, we used the number of styles shriveled per visit. To quantify effective pollen movement, we conducted paternity analysis on a subset of offspring and measured the pollen movement distance between mates. Results: Effective pollen deposition varied among taxa. Andrena helianthiformis, a Heliantheae oligolege, was the most effective taxon, shriveling more than twice the proportion of styles as all other visitors. Differences in visitor behavior on a flowering head did not explain variation in effective pollen deposition, nor did flowering phenology. On average, visitors moved pollen 16 m between plants, and this distance did not vary among taxa. Conclusions: Andrena helianthiformis is an important pollinator of Echinacea. Variation in reproductive fitness of Echinacea in fragmented habitat may result, in part, from the abundance of this species.
Article
Insects other than bees (i.e., non-bees) have been acknowledged as important crop pollinators, but our understanding of which crop plants they visit and how effective they are as crop pollinators is limited. To compare visitation and efficiency of crop-pollinating bees and non-bees at a global scale, we review the literature published from 1950 to 2018 concerning the visitors and pollinators of 105 global food crops that are known to benefit from animal pollinators. Of the 105 animal-pollinated crops, a significant proportion are visited by both bee and non-bee taxa (n = 82; 77%), with a total gross domestic product (GDP) value of US$780.8 billion. For crops with a narrower range of visitors, those that favor non-bees (n = 8) have a value of US$1.2 billion, compared to those that favor bees (n = 15), with a value of US$19.0 billion. Limited pollinator efficiency data were available for one or more taxa in only half of the crops (n = 61; 58%). Among the non-bees, some families were recorded visiting a wide range of crops (>12), including six families of flies (Syrphidae, Calliphoridae, Muscidae, Sarcophagidae, Tachinidae, and Bombyliidae), two beetle families (Coccinelidae and Nitidulidae), ants (Formicidae), wasps (Vespidae), and four families of moths and butterflies (Hesperiidae, Lycaenidae, Nymphalidae, and Pieridae). Among the non-bees, taxa within the dipteran families Syrphidae and Calliphoridae were the most common visitors to the most crops, but this may be an artifact of the limited data available. The diversity of species and life histories in these groups of lesser-known pollinators indicates that diet, larval requirements, and other reproductive needs will require alternative habitat management practices to bees. Expected final online publication date for the Annual Review of Entomology, Volume 65 is January 7, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Article
Many, many more pollinators needed Numerous studies have shown that biodiversity is necessary for ecosystem function. The majority of these, however, have taken place at relatively small experimental scales. Winfree et al. looked across more than 3000 square kilometers for relationships between biodiversity and crop pollination (see the Perspective by Kremen). The number of wild bee species required for successful pollination rapidly increased with spatial scale, largely owing to variation in the species present across sites and the degree to which the most abundant species played a role. In the end, more than an order of magnitude more species than predicted by smaller-scale experiments were required for full ecosystem functioning. Science , this issue p. 791 ; see also p. 741
Article
As pollination biology undergoes unprecedented growth as a discipline, confusion in the use of terms has become increasingly common. The need for a flexible yet unambiguous terminology has become urgent. As an example we discuss how the term “pollination efficiency” is used differently by 18 studies, and “pollinator effectiveness” by seven others. Here we present flowcharts of two general models of pollination systems (biotic and abiotic) that trace all the events from pollen production to development of seed or fruit, and we develop a lexicon for the quantities of pollen, processes of transfers (to a vector, to a stigma), and ratios of quantities that are of interest in studies of pollination and mating systems. An appendix includes a glossary of the definitions we suggest.
Article
During the past decades, managed honeybee stocks have increased globally. Managed honeybees are particularly used within mass-flowering crops and often spill over to adjacent natural habitats after crop blooming. Here, we uniquely show the simultaneous impact that honeybee spillover has on wild plant and animal communities in flower-rich woodlands via changes in plant-pollinator network structure that translate into a direct negative effect on the reproductive success of a dominant wild plant. Honeybee spillover leads to a re-assembly of plant-pollinator interactions through increased competition with other pollinator species. Moreover, honeybee preference for the most abundant plant species reduces its seed set, driven by high honeybee visitation rates that prevent pollen tube growth. Our study therefore calls for an adequate understanding of the trade-offs between providing pollination services to crops and the effects that managed pollinators might have on wild plants and pollinators.
Article
Effective pollination is a complex phenomenon determined by both species-level and community-level factors. While pollinator communities are constituted by interacting organisms in a shared environment, these factors are often simplified or overlooked when quantifying species-level pollinator effectiveness alone. Here, we review the recent literature on pollinator effectiveness to identify the pros and cons of existing methods and outline three important areas for future research: plant-pollinator interactions, heterospecific pollen transfer and the variation in pollination outcomes. We conclude that there is a need to acknowledge a new, additional community level property of pollination effectiveness (i.e. pollinator community effectiveness) in order to account for the suite of plant, pollinator and environmental factors known to influence different stages of successful pollination.
Article
Phylogenetic comparative methods (PCMs) enable us to study the history of organismal evolution and diversification. PCMs comprise a collection of statistical methods for inferring history from piecemeal information, primarily combining two types of data: first, an estimate of species relatedness, usually based on their genes, and second, contemporary trait values of extant organisms. Some PCMs also incorporate information from geological records, especially fossils, but also other gradual and episodic events in the Earth’s history (for example, trait data from fossils or the global oxygen concentration as an independent variable). It is important to note at the outset that PCMs are not concerned with reconstructing the evolutionary relationships among species; this has to do with estimating the phylogeny from genetic, fossil and other data, and a separate set of methods for this process makes up the field of phylogenetics. PCMs as a set of methods are distinct from, but are not completely independent of, phylogenetics. PCMs are used to address the questions: how did the characteristics of organisms evolve through time and what factors influenced speciation and extinction?
Article
Experimental demonstration of direct exploitative competition between foraging honey bees and native bees in wildlands has proven elusive, due to problems of experimental design, scale, and context-dependence. We propose a different approach that translates floral resources collected by a honey bee colony into progeny equivalents of an average solitary bee. Such a metric is needed by public land managers confronting migratory beekeeper demands for insecticide-free, convenient, resource-rich habitats for summering. We calculate that, from June-August, a strong colony gathers as much pollen as could produce 100,000 progeny of an average solitary bee. Analogous to the animal unit month (AUM) for livestock, a hive unit month (HUM) is therefore 33,000 native bee progeny. By this calculation, a 40-hive apiary residing on wildlands for 3 months collects the pollen equivalent of four million wild bees. We introduce a rapid assessment metric to gauge stocking of honey bees, and briefly highlight alternative strategies to provide quality pasture for honey bees with minimal impact on native bees.
Article
Biodiversity-ecosystem functioning experiments have established that species richness and composition are both important determinants of ecosystem function in an experimental context. Determining whether this result holds for real-world ecosystem services has remained elusive, however, largely due to the lack of analytical methods appropriate for large-scale, associational data. Here, we use a novel analytical approach, the Price equation, to partition the contribution to ecosystem services made by species richness, composition and abundance in four large-scale data sets on crop pollination by native bees. We found that abundance fluctuations of dominant species drove ecosystem service delivery, whereas richness changes were relatively unimportant because they primarily involved rare species that contributed little to function. Thus, the mechanism behind our results was the skewed species-abundance distribution. Our finding that a few common species, not species richness, drive ecosystem service delivery could have broad generality given the ubiquity of skewed species-abundance distributions in nature. © 2015 John Wiley & Sons Ltd/CNRS.
Article
(1) Nearly all bees collected pollen on some trips and nectar only on others; most of the exceptions were observed for a few trips only. (2) Only a few of the local species were visited extensively for pollen. Bees foraging on these showed a greater constancy per trip than bees foraging on other species. The most popular pollen often occurred as a minor constituent of loads that were predominantly of other pollens. (3) Bombus lucorum foragers visited fewer species and had purer loads than B. agrorum foragers. Pollen-gatherers from two B. lucorum colonies made different use of the surrounding flora, suggesting that the colony somehow influences an individual bee's choice of forage. (4) B. lucorum foragers showed day-to-day constancy and about 70% collected their original pollen type on the tenth day after the first observation. Inconstant bees sometimes collected the same combination of pollens on successive trips.
Article
(1) The transport of pollen from donor flowers by bumble bees was measured by examining deposition on stigmata of sequences of recipient flowers. The rate of decay of grain deposition was estimated as a measure of pollen carryover. (2) Bombus bifarius was a much less effective pollinator of Erythronium grandiflorum than was the larger Bombus occidentalis. (3) The numbers of pollen grains deposited by bumble bees on the stigmata of Erythronium americanum vary greatly from flower to flower. (4) The time spent by a bee on a flower is positively related to the nectar concentration and volume. (5) Flowers with large volumes of nectar receive more pollen grains per visit than those with small volumes, presumably because the visits are longer. The results are insufficient to show a parallel increase in deposition with nectar concentration. (6) Measures of pollen carryover are presented. Most deposition of grains from a particular donor flower occurs on the first several recipient flowers subsequently visited by the bee, but a few grains travel much farther. (7) Pollen carryover in E. grandiflorum is reduced by bee grooming. (8) The negative effect of grooming on carryover is increased when the recipient flowers have undehisced anthers. (9) Erythronium americanum and E. grandiflorum were similar in carryover, but Linaria vulgaris showed much higher carryover. The reasons for this are discussed.
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Production of many flowering crops often benefits from elevated pollinator diversity and abundance. Nevertheless, the opposite relationship may arise if bees impair fruit or seed production and/or quality by damaging flowers during visitation, despite transferring pollen. We assessed pollination and drupelet set (i.e. the number of drupelets per fruit) in 16 raspberry Rubus idaeus fields along a gradient of bee abundance in north‐west Patagonia, Argentina. Using pollen supplementation, we also tested whether drupelet set was pollen limited in a subset of six fields. Managed Apis mellifera and the invasive bumblebee Bombus terrestris accounted for 50% and 45% of all bee visits, respectively, to raspberry flowers. Pollen loads on stigmas increased with visit frequency of all bees combined and particularly with visitation by A. mellifera, but not by B. terrestris . Drupelet set was not pollen limited along the gradient of bee abundance. Instead, drupelet set decreased with the proportion of damaged styles, which varied more strongly with the frequency of visits by B. terrestris than by A. mellifera . In fields with the highest bee frequency of visits (~300 visits flower −1 day ⁻¹ ), ~80% of styles were damaged in flowers and these developed into fruits with ~30% fewer drupelets compared to flowers in fields with the lowest bee visitation rates (~4 visits flower −1 day ⁻¹ ). Synthesis and applications . Extreme bee visitation, particularly by Bombus terrestris , damaged the styles of raspberry flowers, precluding ovule fertilization by deposited pollen and limiting crop production by reducing drupelet set. Only a few bee visits are required to maximize fruit production in raspberry plants, therefore, pollinator management in north‐west Patagonia should focus principally on reducing the abundance of the invasive bumblebee B. terrestris and secondarily controlling the number of honeybee hives in nearby cultivated fields. Although mainstream pollinator management relies on the assumption that more visits enhance fruit set, high bee visitation rates can be detrimental for fruit development and, consequently, for crop yield.
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Invasive, alien plants and pollinators have varying effects on their interaction partners, ranging from highly beneficial to strongly detrimental. To understand these contrasting impacts, we review the benefits and costs associated with plant–pollinator interactions and enquire as to how the presence of abundant invaders affects the benefit–cost balance. We provide a conceptual framework that predicts that mutualism shifts to antagonism when invaders increase disproportionally in abundance relative to their interaction partners. This outcome is illustrated by an empirical example of a crop in which flower damage and an associated reduction in fruit quality represent interaction costs of intense visitation by invasive bees. More generally, the extremely high density of invasive flower visitors, such as Apis mellifera and Bombus terrestris, might have population- and community-level consequences by hampering reproduction of native plants while promoting reproduction of alien plants. Furthermore, modification of the structure of pollination networks resulting from intense visitation of native plants by superabundant alien flower visitors in highly invaded communities could predict accentuated interaction costs for many native plants. Owing to their high density and the exclusion of native pollinators, invasive bees, originally introduced for honey production and crop pollination, may negatively impact both the native biota and agriculture.
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Inflorescences (heads or capitula) of the putative self-incompatible species, purple coneflower (Echinacea angustifolia (DC) Cronq. (Asteraceae)), were visited by insects representing the Coleoptera, Diptera, Hymenoptera, and Lepidoptera, in accordance with a generalist pollination syndrome. Measurement of the effectiveness of insect species as pollinators was accomplished by permitting solitary visits to receptive, central disc florets of virgin (previously bagged) heads. Four parameters were quantified: total stigmatic pollen load and proportion of pollen grains germinated, numbers of pollen tubes at style bases, and percentages of total receptive florets that had retracted (shrivelled) styles. Quantifying total and germinated pollen grains proved ineffective, partly owing to the tendency of self-pollen to initiate pollen tubes. The most effective pollinators were Apidae, especially bumble bees (Bombus spp.) and the European honey bee (Apis mellifera L.) (mean: 39 - 61% of styles retracted). Other noteworthy pollinators were cloudless sulfur butterflies (Phoebis sennae L.--Pieridae; mean 47% of style bases with pollen tubes), golden blister beetles (Epicauta ferruginea Say--Meloidae; 44%), and grasshopper bee flies (Systoechus vulgaris Loew--Bombyliidae; 22%). Sunflower leafcutter bees (Megachile pugnata Say) were less effective (4% of styles retracted). Promisingly, analysis of the proportion of retracted styles provided similar results to the established technique of pollen-tube quantification, but had the significant advantages of being completed more rapidly, without a microscope, and in the field. The quantitative technique of retracted-style analysis appears well suited for prompt measurement of inflorescence-visiting insects as pollinators of many asteraceans.
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A total of 34 floral visitors of Lavandula latifolia (Labiatae) at a S Spanish locality were examined from the perspective of their 'quality' as pollinators, considering frequency of pollen transfer, number of pollen grains deposited on the stigma, selection of floral sexual stage (flowers are markedly protandrous), and patterns of flight distance between flowers. Hymenoptera deposited more pollen and more often than Lepidoptera or Diptera. The latter 2 groups did not differ in this respect. Interspecific variation in frequency of pollen delivery depended on differences in proportional visitation to female-stage (receptive) flowers as well as total pollen delivery to these flowers. Lepidoptera tended to fly longer distances between consecutive flowers than Hymenoptera. Variation among floral visitors in reproductive services rendered may translate into differential fitness of lavender plants. Nevertheless, the potential for plant specialization on specific insects is constrained by counterbalancing variation in components of pollination quality. -from Author