Restoration of Nontarget Species: Bee Communities and Pollination Function in Riparian Forests

Nontarget species such as pollinators may be of great importance to the restoration process and the long‐term functioning of restored habitats, but little is known about how such groups respond to habitat restoration. I surveyed bee communities at five equal‐aged restored sites, paired with five reference sites (riparian remnants) along the Sacramento River, California, United States. Flower availability and bee visitation patterns were also measured to examine the restoration of pollination function. Restoration of structural vegetation allowed diverse and abundant native bee communities to establish at the restoration sites; however, the composition of these important pollinator communities was distinct from that in the remnant riparian sites. Differences did not arise primarily from differences in the composition of the flowering‐plant community; rather there must be other physical characteristics of the restored sites or differences in nesting site availability that led to the different pollinator communities. Because sites were spatially paired, the differences are unlikely to be driven by landscape context. Bee life‐history and other biological traits may partially explain the differences between bee communities at restored and remnant sites. Patterns of visitation to native plant species suggest that pollination function is restored along with pollinator abundance and richness; however, function may be less robust in restored habitats. An examination of interaction networks between bees and plant species found at both restored and remnant riparian sites showed less redundancy of pollinators visiting some plants at restored habitats.     

Plant species roles in pollination networks: an experimental approach

Pollination is an important ecosystem service threatened by current pollinator declines, making flower planting schemes an important strategy to recover pollination function. However, ecologists rarely test the attractiveness of chosen plants to pollinators in the field. Here, we experimentally test whether plant species roles in pollination networks can be used to identify species with the most potential to recover plant–pollinator communities. Using published pollination networks, we calculated each plant's centrality and chose five central and five peripheral plant species for introduction into replicate experimental plots. Flower visitation by pollinators was recorded in each plot and we tested the impact of introduced central and peripheral plant species on the pollinator and resident plant communities and on network structure. We found that the introduction of central plant species attracted a higher richness and abundance of pollinators than the introduction of peripheral species, and that the introduced central plant species occupied the most important network roles. The high attractiveness of central species to pollinators, however, did not negatively affect visitation to resident plant species by pollinators. We also found that the introduction of central plant species did not affect network structure, while networks with introduced peripheral species had lower centralisation and interaction evenness than networks with introduced central species. To our knowledge, this is the first time species network roles have been tested in a field experiment. Given that most restoration projects start at the plant community, being able to identify the plants with the highest potential to restore community structure and functioning should be a key goal for ecological restoration.     

The smallest of all worlds: pollination networks

A pollination network may be either 2-mode, describing trophic and reproductive interactions between communities of flowering plants and pollinator species within a well-defined habitat, or 1-mode, describing interactions between either plants or pollinators. In a 1-mode pollinator network, two pollinator species are linked to each other if they both visit the same plant species, and vice versa for plants. Properties of 2-mode networks and their derived 1-mode networks are highly correlated and so are properties of 1-mode pollinator and 1-mode plant networks. Most network properties are scale-dependent, i.e. they are dependent upon network size. Pollination networks have the strongest small-world properties of any networks yet studied, i.e. all species are close to each other (short average path length) and species are highly clustered. Species in pollination networks are much more densely linked than species in traditional food webs, i.e. they have a higher density of links, a shorter distance between species, and species are more clustered.     

Rapid Shift in Pollinator Communities Following Invasive Species Removal

Ecological restoration is increasingly used to reverse degradation of rare ecosystems and maintain biological diversity. Pollinator communities are critical to maintenance of plant diversity and, in light of recent pollinator loss, we tested whether removal of invasive glossy buckthorn (Frangula alnus L.) from portions of a prairie fen wetland altered plant and pollinator communities. We compared herbaceous plant, bee, and butterfly abundance, diversity, and species composition in buckthorn invaded, buckthorn removal, and uninvaded reference plots. Following restoration, we found striking differences in plant and pollinator abundance and species composition between restored, unrestored, and reference plots. Within 2 years of F. alnus removal, plant species diversity and composition in restored plots were significantly different than invaded plots, but also remained significantly lower than reference plots. In contrast, in the first growing season following restoration, bee and butterfly abundance, diversity, and composition were similar in restored and reference plots and distinct from invaded plots. Our findings indicate that a diverse community of mobile generalist pollinators rapidly re‐colonizes restored areas of prairie fen, while the plant community may take longer to fully recover. This work implies that, in areas with intact pollinator metapopulations, restoration efforts will likely prevent further loss of mobile generalist pollinators and maintain pollination services. On the other hand, targeted restoration efforts will likely be required to restore populations of rare plants and specialist pollinators for which local and regional species pools may be lacking.     

Restored and remnant Banksia woodlands elicit different foraging behavior in avian pollinators

Pollinators and the pollination services they provide are critical for seed set and self‐sustainability of most flowering plants. Despite this, pollinators are rarely assessed in restored plant communities, where their services are largely assumed to re‐establish. Bird–pollinator richness, foraging, and interaction behavior were compared between natural and restored Banksia woodland sites in Western Australia to assess their re‐establishment in restored sites. These parameters were measured for natural communities of varying size and degree of fragmentation, and restored plant communities of high and low complexity for three years, in the summer and winter flowering of Banksia attenuata and B. menziesii, respectively. Bird visitor communities varied in composition, richness, foraging movement distances, and aggression among sites. Bird richness and abundance were lowest in fragmented remnants. Differences in the composition were associated with the size and degree of fragmentation in natural sites, but this did not differ between seasons. Restored sites and their adjacent natural sites had similar species composition, suggesting proximity supports pollinator re‐establishment. Pollinator foraging movements were influenced by the territorial behavior of different species. Using a network analysis approach, we found foraging behavior varied, with more frequent aggressive chases observed in restored sites, resulting in more movements out of the survey areas, than observed in natural sites. Aggressors were larger‐bodied Western Wattlebirds (Anthochaera chrysoptera) and New Holland Honeyeaters (Phylidonyris novaehollandiae) that dominated nectar resources, particularly in winter. Restored sites had re‐established pollination services, albeit with clear differences, as the degree of variability in the composition and behavior of bird pollinators for Banksias in the natural sites created a broad completion target against which restored sites were assessed. The abundance, diversity, and behavior of pollinator services to remnant and restored Banksia woodland sites were impacted by the size and degree of fragmentation, which in turn influenced bird–pollinator composition, and were further influenced by seasonal changes between summer and winter. Consideration of the spatial and temporal landscape context of restored sites, along with plant community diversity, is needed to ensure the maintenance of the effective movement of pollinators between natural remnant woodlands and restored sites.     

Two invasive acacia species secure generalist pollinators in invaded communities

Exotic entomophilous plants need to establish effective pollinator interactions in order to succeed after being introduced into a new community, particularly if they are obligatory outbreeders. By establishing these novel interactions in the new non-native range, invasive plants are hypothesised to drive changes in the composition and functioning of the native pollinator community, with potential impacts on the pollination biology of native co-flowering plants. We used two different sites in Portugal, each invaded by a different acacia species, to assess whether two native Australian trees, Acacia dealbata and Acacia longifolia, were able to recruit pollinators in Portugal, and whether the pollinator community visiting acacia trees differed from the pollinator communities interacting with native co-flowering plants. Our results indicate that in the invaded range of Portugal both acacia species were able to establish novel mutualistic interactions, predominantly with generalist pollinators. For each of the two studied sites, only two other co-occurring native plant species presented partially overlapping phenologies. We observed significant differences in pollinator richness and visitation rates among native and non-native plant species, although the study of β diversity indicated that only the native plant Lithodora fruticosa presented a differentiated set of pollinator species. Acacias experienced a large number of visits by numerous pollinator species, but massive acacia flowering resulted in flower visitation rates frequently lower than those of the native co-flowering species. We conclude that the establishment of mutualisms in Portugal likely contributes to the effective and profuse production of acacia seeds in Portugal. Despite the massive flowering of A. dealbata and A. longifolia, native plant species attained similar or higher visitation rates than acacias.     

Pollination of a bee‐dependent forb in restored prairie: no evidence of pollen limitation in landscapes dominated by row crop agriculture

Restoration is used to conserve biodiversity; however, it is unclear to what extent restoration impacts ecosystem functions. Pollination is an ecosystem function that is critical to plant reproduction and thus restoration success. Few studies have assessed whether pollination is restored within restoration areas themselves. Plant–animal interactions may be affected by factors beyond the scale of the restoration. For example, surrounding landscape context may influence pollinator abundance and consequently the amount of pollen deposited. Decreased pollen receipt might then limit seed set. We hypothesized that in restorations surrounded by more agriculture, pollinator‐dependent forbs would experience greater pollen limitation. This would likely be due to declines in pollinator abundance within the restorations with an increase in surrounding agriculture. We deployed potted Chamaecrista fasciculata (Fabaceae), an obligatorily bee‐pollinated forb, and sampled bee communities in restored prairies in Minnesota, U.S.A. We measured pollen limitation by comparing seed set among open and supplementally pollinated plants. We also sampled native bees in seven of the eight sites. We tested for a relationship between proportion row crop agriculture (corn and soy) surrounding a restoration and pollen limitation, as well as an effect of agriculture on bee abundance. We did not find evidence that increasing proportion of surrounding agriculture negatively affected pollen limitation or bee abundance. Our results indicate that greater surrounding agriculture may not influence pollination of C. fasciculata through declines in pollinator availability, and suggest for some plants that landscape context might not limit pollination in restorations.     

Restoration of riverine inland sand dune complexes: implications for the conservation of wild bees

1.  The evaluation of restoration measures is an important task of conservation biology. Inland sand dunes and dry, oligotrophic grasslands have become rare habitat types in large parts of Central Europe and their restoration and management is of major importance for the preservation of many endangered plant and insect species. Within such habitats, it is important to restore key ecosystem services, such as pollination networks. As wild bees are the most important pollinators in many ecosystems, they represent a suitable key group to evaluate restoration measures. Furthermore, the recent decline of many bee species and the potential ecological and economic consequences are currently topics of strong scientific interest.
2.  We studied the succession of bee communities in response to restoration measures of sand dunes and sand grasslands and compared these communities with those of old sand dune complexes.
3.  Our results show that wild bees respond rapidly to restoration measures indicated by a high species richness and abundance. The community structure of bees at restoration sites converged only slightly to those of the target sites. A higher similarity was found between bee communities at the restoration sites (sand dunes and grasslands), indicating that their close proximity was an important determinant of species overlap. Environmental factors such as the number of entomophilous plant species and moisture had a strong influence on wild bee species composition.
4.   Synthesis and applications . The restoration of inland sand dune complexes provides opportunities for colonization by a diverse wild bee community. Although it is difficult to establish a given target community, restoration measures gave rise to a high pollinator diversity and abundance, suggesting that community function can be re-established.     

Pollinator individual‐based networks reveal the specialized plant–pollinator mutualism in two biodiverse communities

Generalization of pollination systems is widely accepted by ecologists in the studies of plant–pollinator interaction networks at the community level, but the degree of generalization of pollination networks remains largely unknown at the individual pollinator level. Using potential legitimate pollinators that were constantly visiting flowers in two alpine meadow communities, we analyzed the differences in the pollination network structure between the pollinator individual level and species level. The results showed that compared to the pollinator species‐based networks, the linkage density, interaction diversity, interaction evenness, the average plant linkage level, and interaction diversity increased, but connectance, degree of nestedness, the average of pollinator linkage level, and interaction diversity decreased in the pollinator individual‐based networks, indicating that pollinator individuals had a narrower food niche than their counterpart species. Pollination networks at the pollinator individual level were more specialized at the network level (H′₂) and the plant species node level (d′) than at the pollinator species‐level networks, reducing the chance of underestimating levels of specialization in pollination systems. The results emphasize that research into pollinator individual‐based pollination networks will improve our understanding of the pollination networks at the pollinator species level and the coevolution of flowering plants and pollinators.     

Urbanization increases floral specialization of pollinators

Understanding how urbanization alters functional interactions among pollinators and plants is critically important given increasing anthropogenic land use and declines in pollinator populations. Pollinators often exhibit short‐term specialization and visit plants of the same species during one foraging trip. This facilitates plant receipt of conspecific pollen—pollen on a pollinator that is the same species as the plant on which the pollinator was foraging. Conspecific pollen receipt facilitates plant reproductive success and is thus important to plant and pollinator persistence. We investigated how urbanization affects short‐term specialization of insect pollinators by examining pollen loads on insects’ bodies and identifying the number and species of pollen grains on insects caught in urban habitat fragments and natural areas. We assessed possible drivers of differences between urban and natural areas, including frequency dependence in foraging, species richness and diversity of the plant and pollinator communities, floral abundance, and the presence of invasive plant species. Pollinators were more specialized in urban fragments than in natural areas, despite no differences in the species richness of plant communities across site types. These differences were likely driven by higher specialization of common pollinators, which were more abundant in urban sites. In addition, pollinators preferred to forage on invasive plants at urban sites and native plants at natural sites. Our findings reveal indirect effects of urbanization on pollinator fidelity to individual plant species and have implications for the maintenance of plant species diversity in small habitat fragments. Higher preference of pollinators for invasive plants at urban sites suggests that native species may receive fewer visits by pollinators. Therefore, native plant species diversity may decline in urban sites without continued augmentation of urban flora or removal of invasive species.     

Phylogenetic Community Context Influences Pollen Delivery to <Emphasis Type="Italic">Allium cernuum</Emphasis>

Few studies have examined how the number and identity of species in the neighbouring community influences the reproductive success of particular focal species. Pollen delivery, an important component of fitness of sexual plants, is a function of not just the floral traits of any particular individual, but of features of the population and community as it depends on pollinator abundance and preferences. Many pollinators in flowering communities will prefer patches with high floral abundance or diversity yet may exhibit lower floral constancy when more flowering species are present. Thus, pollination efficiency could increase or decrease with increased species richness and this will alter the selection pressures placed upon the floral traits (such as floral colour or reward) of any member of a particular community. Moreover, recent studies have indicated that plant-pollinator networks are phylogenetically structured (pollinators visit related plant species more than expected by chance) and this may be an important factor structuring flowering plant communities. Thus, the sheer number of species within a patch may be less important than the number of closely-related species. We investigate whether species richness or phylogenetic proximity of coflowering species influences the amount and proportion of conspecific pollen delivered to nodding onion, Allium cernuum, in fragment patches of Garry Oak meadows in South Western British Columbia, Canada. We find that pollen delivery depended upon the presence of close relatives far more than on species richness or population density, indicating a central role of the community structure on pollination in flowering plant communities. Insofar as pollen delivery relates to the relative number of seeds produced by members of the community, pollination may in turn determine the community structure of the next generation.     

Factors related to the inter‐annual variation in plants' pollination generalization levels within a community

The number of pollinators of a plant species is considered a measure of its ecological generalization and may have important evolutionary and ecological implications. Many pollination studies report inter‐annual fluctuations in the composition of pollinators to particular species. However, the factors causing such variation are still poorly understood. Here we investigate how flowering duration and plant and pollinator assemblages influenced the inter‐annual changes in the functional generalization level of the 20 most common plant species of a semi‐natural meadow in southern Norway. We also studied the extent to which changes in generalization levels were controlled by flower‐shape and flowering time. Large inter‐annual changes in generalization levels were common and there was no relationship between the generalization level one year and the following. Generalization level of particular plant species increased with flowering duration, sampling effort, and the abundance of managed honeybees in the community. Generalization level decreased with the flowering synchrony between the focal plant species and the rest of the plant community and with the focal species’ own abundance, which we attribute to inter‐specific competition for pollinator attraction and foraging decisions made by pollinators. Plants with different flower‐shapes and flowering times did not differ in the extent of inter‐annual variation in generalization levels. Most studies do not consider the effect of the plant community on the generalization level of particular plant species. We show here that both pollinator and plant assemblages can affect the inter‐annual variation in generalization levels of plant species. Studies like ours will help to understand how pollination interactions are structured at the community level, and the ecological and evolutionary consequences that these inter‐annual changes in generalization levels may have.     

The effects of urbanization on pollinators and pollination: A meta-analysis

Urbanization is increasing worldwide, with major impacts on biodiversity, species interactions and ecosystem functioning. Pollination is an ecosystem function vital for terrestrial ecosystems and food security; however, the processes underlying the patterns of pollinator diversity and the ecosystem services they provide in cities have seldom been quantified. Here, we perform a comprehensive meta-analysis of 133 studies examining the effects of urbanization on pollinators and pollination. Our results confirm the widespread negative impacts of urbanization on pollinator richness and abundance, with Lepidoptera being the most affected group. Furthermore, pollinator responses were found to be trait-specific, with below-ground nesting and solitary Hymenoptera, and spring flyers more severely affected by urbanization. Meanwhile, cities promote non-native pollinators, which may exacerbate conservation risks to native species. Surprisingly, despite the negative effects of urbanization on pollinator diversity, pollination service measured as seed set is enhanced in non-tropical cities likely due to abundant generalists and managed pollinators therein. We emphasize that the richness of local flowering plants could mitigate the negative impacts of urbanization on pollinator diversity. Overall, the results demonstrate the varying magnitudes of multiple moderators on urban pollinators and pollination services and could help guide conservation actions for biodiversity and ecosystem function for a sustainable future.     

Patterns and drivers of wild bee community assembly in a Mediterranean IUCN important plant area

Recent reports of pollinator declines have stirred interest in investigating the impacts of habitat exploitation on the conservation of pollinator and plant communities. An important prerequisite to tailor conservation action is to understand the drivers and patterns of species-rich communities, and how they change in space and time during a whole season. To account for this, we surveyed wild bees and flowering plants using standardized transects in 11 natural habitat fragments of an IUCN important plant area along the coast of Israel. We used phylogeny- and taxon-based methods of community structure analyses to study the assembly processes of bee communities, and investigated the effects of several landscape parameters on bee diversity using generalized linear models (GLMs). Our results illustrate that natural habitat sites comprised significantly higher species richness compared to disturbed habitat sites, and show that even the smallest habitat fragments harbored unique bee assemblages, with significant species replacement (turnover) found in both space and time. Our GLMs indicated that flower diversity, and semi-natural habitat within 500 m of habitat fragments were important drivers of bee diversity, but we found no evidence for a species—area relationship among sites. Finally, we document a case of phylogenetic overdispersion despite low species richness, which highlights the importance of accounting for phylogenetic diversity rather than only species richness to reach a more fine-grained understanding of pollinator diversity. This, in turn, is pivotal to developing conservation actions to protect these essential pollinators and their interaction with rare and endemic plant species in this highly threatened ecosystem.     

Habitat type plays a greater role than livestock grazing in structuring shrubsteppe plant–pollinator communities

Livestock grazing is a widespread grassland disturbance and can negatively impact biodiversity. Pollinators constitute a vital component of grassland ecosystems, but the impact of grazing on pollinator diversity has seldom been evaluated in North America. We assessed vegetation structure, and pollinator and flowering plant abundance, richness, diversity, and community composition in four pairs of spring-grazed/ungrazed sites in south-central British Columbia, Canada. We also investigated whether pollinator or floral communities differed between the two threatened shrubsteppe habitat types we sampled—antelope-brush and big sagebrush shrubsteppe. Pan-trapping surveys captured 5907 bees, flies, beetles, wasps and butterflies constituting 253 species. We found that the percent cover of shrubs and bare soil increased with grazing, while the height of grasses and forbs decreased. In contrast, pollinator and flowering plant abundance, richness, diversity, and community composition were not significantly affected by grazing. Flowering plant and pollinator community composition did differ significantly between shrubsteppe habitats. Our results indicate that grasslands in North America, when managed responsibly, can maintain pollinator and flowering plant diversity under grazing pressure. The continued effort of land managers to balance ecological integrity and economic viability will be important for the conservation of grassland pollination systems.     

Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

相似文献   

Spatial variability in a plant–pollinator community across a continuous habitat: high heterogeneity in the face of apparent uniformity

Large‐scale spatial variability in plant–pollinator communities (e.g. along geographic gradients, across different landscapes) is relatively well understood. However, we know much less about how these communities vary at small scales within a uniform landscape. Plants are sessile and highly sensitive to microhabitat conditions, whereas pollinators are highly mobile and, for the most part, display generalist feeding habits. Therefore, we expect plants to show greater spatial variability than pollinators. We analysed the spatial heterogeneity of a community of flowering plants and their pollinators in 40 plots across a 40‐km² area within an uninterrupted Mediterranean scrubland. We recorded 3577 pollinator visits to 49 plant species. The pollinator community (170 species) was strongly dominated by honey bees (71.8% of the visits recorded). Flower and pollinator communities showed similar beta‐diversity, indicating that spatial variability was similar in the two groups. We used path analysis to establish the direct and indirect effects of flower community distribution and honey bee visitation rate (a measure of the use of floral resources by this species) on the spatial distribution of the pollinator community. Wild pollinator abundance was positively related to flower abundance. Wild pollinator visitation rate was negatively related to flower abundance, suggesting that floral resources were not limiting. Pollinator and flower richness were positively related. Pollinator species composition was weakly related to flower species composition, reflecting the generalist nature of flower–pollinator interactions and the opportunistic nature of pollinator flower choices. Honey bee visitation rate did not affect the distribution of the wild pollinator community. Overall, we show that, in spite of the apparent physiognomic uniformity, both flowers and pollinators display high levels of heterogeneity, resulting in a mosaic of idiosyncratic local communities. Our results provide a measure of the background of intrinsic heterogeneity within a uniform habitat, with potential consequences on low‐scale ecosystem function and microevolutionary patterns.     

Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities

Pollination is exclusively or mainly animal mediated for 70% to 90% of angiosperm species. Thus, pollinators provide an essential ecosystem service to humankind. However, the impact of human-induced biodiversity loss on the functioning of plant–pollinator interactions has not been tested experimentally. To understand how plant communities respond to diversity changes in their pollinating fauna, we manipulated the functional diversity of both plants and pollinators under natural conditions. Increasing the functional diversity of both plants and pollinators led to the recruitment of more diverse plant communities. After two years the plant communities pollinated by the most functionally diverse pollinator assemblage contained about 50% more plant species than did plant communities pollinated by less-diverse pollinator assemblages. Moreover, the positive effect of functional diversity was explained by a complementarity between functional groups of pollinators and plants. Thus, the functional diversity of pollination networks may be critical to ecosystem sustainability.     

Functional Diversity of Plant–Pollinator Interaction Webs Enhances the Persistence of Plant Communities

Pollination is exclusively or mainly animal mediated for 70% to 90% of angiosperm species. Thus, pollinators provide an essential ecosystem service to humankind. However, the impact of human-induced biodiversity loss on the functioning of plant–pollinator interactions has not been tested experimentally. To understand how plant communities respond to diversity changes in their pollinating fauna, we manipulated the functional diversity of both plants and pollinators under natural conditions. Increasing the functional diversity of both plants and pollinators led to the recruitment of more diverse plant communities. After two years the plant communities pollinated by the most functionally diverse pollinator assemblage contained about 50% more plant species than did plant communities pollinated by less-diverse pollinator assemblages. Moreover, the positive effect of functional diversity was explained by a complementarity between functional groups of pollinators and plants. Thus, the functional diversity of pollination networks may be critical to ecosystem sustainability.     

Threats and benefits of invasive alien plant species on pollinators

Invasive alien plant species are usually disliked due to their high pressure on native communities. However, their ecological effects on pollinators are complex: some species provide abundant floral resources, boosting the number of pollinators, while they often disrupt plant-pollinator interactions by outcompeting native plants. Our direct knowledge is mainly based on single-species studies, while understanding the mechanism of these complex ecological interactions needs multi-species field-based approaches. It is also imperative to clarify the pros and cons of invasive plants and drivers of invasion from the perspective of pollinators. We conducted a standard protocol-driven regional study in Central and Eastern Europe, comparing 6-7 invaded and non-invaded sites of 12 herbaceous invasive plant species. We sampled floral resources, bees, and hoverflies before and during the flowering of the invasive plants. We analysed the effects of plant invasion at the invasive plant species level and in combined analyses, and tested whether the life span (perennial vs. annual) and flowering time (early-, middle-, and late-flowering) of invasive plants affect the abundance, species richness, diversity and species composition of native plants and pollinators. The combined analyses showed lower abundance and species richness of flowering plants and pollinators before, and higher abundance of both during the flowering of invasive plants in invaded sites. However, invasive plants had significant species-specific effects. Perennial invasive plants had a stronger negative impact on floral resources and pollinators already before their flowering compared to annuals. Flowering time of invasive plants affected the pollinator guilds differently. We suggest that in certain critical time periods of the year, invasive plants might provide the dominant foraging resources for pollinators in an invaded ecosystem. But, they also often cause significant losses in native floral resources over the year. Instead of simple eradication, careful preparation and consideration might be needed during removal of invasive plants.