Plant-pollinator Communities Research Articles

Experimental field test of the influence of generalist stingless bees (Meliponini) on the topology of a bee–flower mutualistic network in the tropics

1. Generalists are assumed to play a key role in structuring and stabilising animal–plant mutualistic networks. Until now, analyses on the effects of generalists have been based on empirical field data or simulations. The present natural field experiment manipulated the abundance of a generalist and abundant stingless bee [Melipona (Eomelipona) marginata] to determine the effects on the mutualistic network.2. Networks were generated, and associated metrics were used for comparing replicate plots with and without the insertion of stingless bee nests.3. Unweighted metrics and the basic qualitative structural pattern of networks (high nestedness, very low modularity and specialisation) was not affected by experimental variation in stingless bee abundance because they exert strong basal effects on the plant–pollinator community under natural conditions of abundance. Still, increased abundance caused significant variation in weighted nestedness and modularity and community‐level specialisation.4. Supporting predictions of neutral models, increased abundance of the stingless bee led to an increase in most of its specific metrics, expressing the expansion of its realised trophic niche.5. During this process, specialist and other generalist bees were affected in different ways. More plant species became even more dependent on this stingless bee (increased asymmetry).6. Long‐term effects could not be inferred directly from instantaneous values of network metrics. Nonetheless, the increased abundance of the generalist stingless bee may both reduce the local level of ecological specialisation in the short term and affect the spatial distribution of less abundant and/or specialist bee species and plants in the long term.

Plant–pollinator interactions along an urbanization gradient from cities and villages to farmland landscapes

AbstractUrbanization affects pollinator diversity and plant–pollinator networks by changing resource availability locally and in the surrounding landscape. We experimentally established (N = 12) standardized plant communities in farmland, villages, and cities to identify the relative role of local and landscape effects on plant–pollinator communities along this urbanization gradient. We found that the number of flower visits by solitary bees, but not bumblebees, was highest in cities and lowest in farmland, with villages being intermediate, whereas syrphid flies exhibited lowest numbers in cities. Villages supported the richest pollinator communities, as they appeared to benefit from both farmland and city communities. Plant–pollinator network metrics such as robustness, interaction evenness, and interaction diversity decreased with increasing urbanization, although local plant richness increased toward urban areas. In conclusion, pollinator communities were most diverse and stable in farmland and village sites, despite the high plant richness in cities. The different composition of pollinator communities along the urbanization gradient suggests considering all three landscape types for conservation schemes.

Seasonal variation of a plant-pollinator network in the Brazilian Cerrado: Implications for community structure and robustness.

Seasonal variation in the availability of floral hosts or pollinators is a key factor influencing diversity in plant-pollinator communities. In seasonally dry Neotropical habitats, where month-long periods of extreme drought are followed by a long rainy season, flowering is often synchronized with the beginning of precipitation, when environmental conditions are most beneficial for plant reproduction. In the Brazilian Cerrado, a seasonally dry ecosystem considered one of the world’s biodiversity hotspots for angiosperms, plants with shallow root systems flower predominantly during the rainy season. Foraging activity in social bees however, the major pollinators in this biome, is not restricted to any particular season because a constant supply of resources is necessary to sustain their perennial colonies. Despite the Cerrado’s importance as a center of plant diversity, the influence of its extreme cycles of drought and precipitation on the dynamics and stability of plant-pollinator communities is not well understood. We sampled plant-pollinator interactions of a Cerrado community weekly for one year and used network analyses to characterize intra-annual seasonal variation in community structure. We also compared seasonal differences in community robustness to species loss by simulating extinctions of plants and pollinators. We find that the community shrinks significantly in size during the dry season, becoming more vulnerable to disturbance due to the smaller pool of floral hosts available to pollinators during this period. Major changes in plant species composition but not in pollinators has led to high levels of turnover in plant-pollinator associations across seasons, indicated by in interaction dissimilarity (<3% of shared interactions). Aseasonal pollinators, which mainly include social bees and some solitary specialized bees, functioned as keystone species, maintaining robustness during periods of drastic changes in climatic conditions.

The role of alien species on plant-floral visitor network structure in invaded communities.

The interactions between pairs of native and alien plants via shared use of pollinators have been widely studied. Community level studies however, are necessary in order to fully understand the factors and mechanisms that facilitate successful plant invasion, but these are still scarce. Specifically, few community level studies have considered how differences in invasion level (alien flower abundance), and degree of floral trait similarity between native and invasive species, mediate effects on native plant-pollinator communities. Here, we evaluated the role of alien species on overall plant-floral visitor network structure, and on species-level network parameters, across nine invaded coastal communities distributed along 205 km in Yucatán, México that vary in alien species richness and flower abundance. We further assessed the potential the role of alien plant species on plant-floral visitor network structure and robustness via computational simulation of native and invasive plant extinction scenarios. We did not find significant differences between native and alien species in their functional floral phenotypes or in their visitation rate and pollinator community composition in these invaded sites. Variation in the proportion of alien plant species and flower abundance across sites did not influence plant-pollinator network structure. Species-level network parameters (i.e., normalized degree and nestedness contribution) did not differ between native and alien species. Furthermore, our simulation analyses revealed that alien species are functionally equivalent to native species and contribute equally to network structure and robustness. Overall, our results suggest that high levels of floral trait similarity and pollinator use overlap may help facilitate the integration of alien species into native plant-pollinator networks. As a result, alien species may also play a similar role than that of natives in the structure and stability of native plant and pollinator communities in the studied coastal sand dune ecosystem.

Interconnectedness of the Grinnellian and Eltonian Niche in Regional and Local Plant-Pollinator Communities.

Understanding the causes and consequences of coexistence and thus biodiversity is one of the most fundamental endeavors of ecology, which has been addressed by studying species’ requirements and impacts – conceptualized as their Grinnellian and Eltonian niches. However, different niche types have been mostly studied in isolation and thus potential covariation between them remains unknown. Here we quantified the realized Grinnellian niche (environmental requirements), the fundamental (morphological phenotype) and realized Eltonian niche (role in networks) of plant and pollinator taxa at a local and regional scale to investigate the interconnectedness of these niche types. We found a strong and scale-independent co-variation of niche types suggesting that taxa specialized in environmental factors are also specialized in their position in trait spaces and their role in bipartite networks. The integration of niche types thus will help to detect the true causes for species distributions, interaction networks, as well as the taxonomic and functional diversity of communities.

Network modelling, citizen science and targeted interventions to predict, monitor and reverse bee decline

Societal Impact StatementThe global decline in pollinating insect populations has rightly received widespread news coverage as it imperils ecosystem function and human food security. Reversing and addressing this decline is an urgent global priority. However, in many locations we do not know what species are present, how large or small species populations are, or what types of specific resources the populations require. By adopting novel network analyses approaches and by working with monitoring programs, such as Oxford Plan Bee, we may be able to dramatically improve our ability to predict species extinctions and facilitate targeted conservation action to maintain abundant, diverse and stable pollinator communities. Summary Pollination is fundamentally important to ecosystem function and human food security. Recent reports of dramatic insect declines, and pollinator decline in particular, have increased public awareness and political motivation to act to protect pollinators. This article maps commonly proposed management interventions onto known drivers of bee decline, and identifies forage and nest site provision as a tractable management intervention that can simultaneously address multiple drivers of decline. However, it is recognized that there are gaps in the knowledge of exactly how much and which types of forage resources are necessary to support wild pollinator populations. A novel network analysis approach based on quantified floral resources and pollination services is proposed, which would illuminate the types and quantities of floral resources and pollinators necessary to maintain a diverse and abundant plant–pollinator community. The approach would also facilitate the prediction of species extinctions in plant–pollinator communities and help target conservation interventions. Finally, Oxford Plan Bee is introduced as a new, citizen‐science‐based project to monitor solitary bee populations, and provide empirical data to validate predictions from the proposed network approach. The over‐arching aim of the described network analysis approach and the Oxford Plan Bee project is to facilitate effective, evidence‐based conservation action to protect pollinators and the plants they pollinate into the future.

Patterns and effects of heterospecific pollen transfer between an invasive and two native plant species: the importance of pollen arrival time to the stigma.

Invasive plant species can integrate into native plant-pollinator communities, but the underlying mechanisms are poorly understood. Competitive interactions between invasive and native plants via heterospecific pollen (HP) and differential invasive HP effects depending on HP arrival time to the stigma may mediate invasion success, but these have been little studied. We evaluated patterns and effects of HP receipt on pollen tube growth in two native and one invasive species in the field. We also used hand-pollination experiments to evaluate the effect of invasive HP pollen and its arrival time on native reproductive success. Native species receive smaller and less-diverse HP loads (5-7 species) compared to invasive species (10 species). The load size of HP had a negative effect on the proportion of pollen tubes in both native species but not in the invasive, suggesting higher HP tolerance in the latter. Invasive HP arrival time differentially affected pollen tube success in native species. Our results highlight the need to study reciprocal HP effects between invasive and native species and the factors that determine differential responses to HP receipt to fully understand the mechanisms facilitating invasive species integration into native plant-pollinator communities.

Forest proximity and lowland mosaic increase robustness of tropical pollination networks in mixed fruit orchards

More than 30% of global crop plants rely on pollinators to set fruit or seed. While several studies have documented the negative effects of habitat degradation and distance from natural habitats on pollinator diversity in tropical areas, such studies have focused on single crops in particular areas without examining entire plant-pollinator communities. Here, we compared the plant-pollinator network structure between mixed fruit orchards that were near to (<1 km) and far from (>7 km) tropical forests and further investigated the effect of landscape composition in surrounding areas on plant-pollinator network structure. Our ten pairs of orchards were in Thailand and grew a range of tropical fruits pollinated by insects, birds and bats. The average number of visitor-flower interactions was higher at sites near the forest. Similarly, network robustness (the resistance of the network to losing species as a result of primary species removal) and interaction evenness (evenness of interactions among species) were higher at the sites closer to the forest. Robustness was strongly positively influenced by the proportion of lowland mosaic within a 1 km radius, while interaction evenness was positively affected by the proportion of urban area and montane mosaic within a 4 km radius of each site. Conservation of (semi-) natural habitats is therefore important for maintaining the diversity of wild pollinators and agricultural production.

Experimental species introduction shapes network interactions in a plant-pollinator community

Invasive species that form mutualistic interactions can perturb resident communities by creating new interactions, or weakening the strength of existing interactions via competition. We hypothesized that introducing a super-generalist plant species to bee-plant networks would lead to (1) increases in the weighted and unweighted average degree, nestedness, and connectance and (2) decreases in the modularity. We constructed visitation networks of bees to five native plant species in experimental research plots, in the presence and absence of an invasive thistle and while varying thistle abundance and time/duration of introduction. Species introduction did not change the visitation rate of bees to co-occurring native plants, or the interaction structure between the native plant species and bee visitors; seed set of a focal native plant species was also unaffected. We found the number of bee species with which the introduced species interacted (generality) correlated with significant increases in unweighted and weighted average degree, nestedness, and connectance, but not modularity. When comparing the impact of the introduced species either early or late in the season, we found similar relationships between introduced species generality and weighted and unweighted average degree and connectance; there was a significant negative relationship between introduced species generality and modularity early in the season, and a significant positive relationship with nestedness late in the season, suggesting introduction timing within a season may affect some measures differently. Overall, the native community was robust to the introduction of the super-generalist; our experimental test of network theory predictions demonstrates an improving mechanistic understanding of how mutualistic networks respond to ecological perturbations.

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‐km2area 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.

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.

Specialist foragers in forest bee communities are small, social or emerge early.

Individual pollinators that specialize on one plant species within a foraging bout transfer more conspecific and less heterospecific pollen, positively affecting plant reproduction. However, we know much less about pollinator specialization at the scale of a foraging bout compared to specialization by pollinator species. In this study, we measured the diversity of pollen carried by individual bees foraging in forest plant communities in the mid-Atlantic United States. We found that individuals frequently carried low-diversity pollen loads, suggesting that specialization at the scale of the foraging bout is common. Individuals of solitary bee species carried higher diversity pollen loads than did individuals of social bee species; the latter have been better studied with respect to foraging bout specialization, but account for a small minority of the world's bee species. Bee body size was positively correlated with pollen load diversity, and individuals of polylectic (but not oligolectic) species carried increasingly diverse pollen loads as the season progressed, likely reflecting an increase in the diversity of flowers in bloom. Furthermore, the seasonal increase in pollen load diversity was stronger for bees visiting trees and shrubs than for bees visiting herbaceous plants. Overall, our results showed that both plant and pollinator species' traits as well as community-level patterns of flowering phenology are likely to be important determinants of individual-level interactions in plant-pollinator communities.

Bmotif: A package for motif analyses of bipartite networks

Abstract Bipartite networks are widely used to represent a diverse range of species interactions, such as pollination, herbivory, parasitism and seed dispersal. The structure of these networks is usually characterised by calculating one or more indices that capture different aspects of network architecture. While these indices capture useful properties of networks, they are relatively insensitive to changes in network structure. Consequently, variation in ecologically‐important interactions can be missed. Network motifs are a way to characterise network structure that is substantially more sensitive to changes in pairwise interactions and is gaining in popularity. However, there is no software available in R, the most popular programming language among ecologists, for conducting motif analyses in bipartite networks. Similarly, no mathematical formalisation of bipartite motifs has been developed. Here we introduce bmotif: a package for motif analyses of bipartite networks. Our code is primarily an r package, but we also provide matlab and Python code of the core functionality. The software is based on a mathematical framework where, for the first time, we derive formal expressions for motif frequencies and the frequencies with which species occur in different positions within motifs. This framework means that analyses with bmotif are fast, making motif methods compatible with the permutational approaches often used in network studies, such as null model analyses. We describe the package and demonstrate how it can be used to conduct ecological analyses, using two examples of plant–pollinator networks. We first use motifs to examine the assembly and disassembly of an Arctic plant–pollinator community and then use them to compare the roles of native and introduced plant species in an unrestored site in Mauritius. bmotif will enable motif analyses of a wide range of bipartite ecological networks, allowing future research to characterise these complex networks without discarding important meso‐scale structural detail.

A systems approach reveals urban pollinator hotspots and conservation opportunities.

Urban areas are often perceived to have lower biodiversity than the wider countryside, but a few small-scale studies suggest that some urban land uses can support substantial pollinator populations. We present a large-scale, well-replicated study of floral resources and pollinators in 360 sites incorporating all major land uses in four British cities. Using a systems approach, we developed Bayesian network models integrating pollinator dispersal and resource switching to estimate city-scale effects of management interventions on plant-pollinator community robustness to species loss. We show that residential gardens and allotments (community gardens) are pollinator ‘hotspots’: gardens due to their extensive area, and allotments due to their high pollinator diversity and leverage on city-scale plant-pollinator community robustness. Household income was positively associated with pollinator abundance in gardens, highlighting the influence of socio-economic factors. Our results underpin urban planning recommendations to enhance pollinator conservation, using increasing city-scale community robustness as our measure of success.

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

A long‐standing question in ecology is how species interactions are structured within communities. Although evolutionary theory predicts close size matching between floral nectar tube depth and pollinator proboscis length of interacting species, such size matching has seldom been shown and explained in multispecies assemblages. Here, we investigated the degree of size matching among Asteraceae and their pollinators and its relationship with foraging efficiency. The majority of pollinators, especially Hymenoptera, choose plant species on which they had high foraging efficiencies. When proboscides were shorter than nectar tubes, foraging efficiency rapidly decreased because of increased handling time. When proboscides were longer than nectar tubes, a decreased nectar reward rather than an increased handling time made shallow flowers more inefficient to visit. Altogether, this led to close size matching. Overall, our results show the importance of nectar reward and handling time as drivers of plant–pollinator network structure.

Lifelong foraging and individual specialisation are influenced by temporal changes of resource availability

Resource availability largely determines the distribution and behaviour of organisms. In plant–pollinator communities, availability of floral resources may change so rapidly that pollinator individuals can benefit from switching between multiple resources, i.e. different flowering plant species. Insect pollinator individuals of a given generation often occur in different time windows during the reproductive season. This temporal variation in individual occurrences, together with the rapidly changing resource availability, may lead individuals of the same population to encounter and use different resources, resulting in an apparent individual specialisation. We hypothesized, that 1) individual pollinators change their resource use (flower visitation) during their lifetime according to the changing availability of floral resources, and that 2) temporal variation in individual occurrences of pollinators and in resource availability will partly explain individual specialisation. To test these hypotheses, we observed flower visitations of individually marked clouded Apollo butterflies Parnassius mnemosyne during one reproductive season. We found temporal changes in lifetime individual resource use that followed the changes in resource availability, indicating that butterflies can adjust foraging to varying resource availability. Individuals differed considerably in their resource use. This variation was partly explained by temporal variation in both floral resource availability and temporal occurrence of individual butterflies. We suggest the butterfly as a sequential specialist, i.e. short‐term specialist and long‐term generalist. This foraging plasticity can be essential for short‐living insect pollinators in rapidly changing environments. Although flowering dynamics do not fully explain the variability in foraging, our results highlight the importance of temporal dimension in resource use studies. Ultimately, the relative pace of environmental change compared to individual lifespan may be a key factor in resource use plasticity.

Motifs in bipartite ecological networks: uncovering indirect interactions

Indirect interactions play an essential role in governing population, community and coevolutionary dynamics across a diverse range of ecological communities. Such communities are widely represented as bipartite networks: graphs depicting interactions between two groups of species, such as plants and pollinators or hosts and parasites. For over thirty years, studies have used indices, such as connectance and species degree, to characterise the structure of these networks and the roles of their constituent species. However, compressing a complex network into a single metric necessarily discards large amounts of information about indirect interactions. Given the large literature demonstrating the importance and ubiquity of indirect effects, many studies of network structure are likely missing a substantial piece of the ecological puzzle. Here we use the emerging concept of bipartite motifs to outline a new framework for bipartite networks that incorporates indirect interactions. While this framework is a significant departure from the current way of thinking about bipartite ecological networks, we show that this shift is supported by analyses of simulated and empirical data. We use simulations to show how consideration of indirect interactions can highlight differences missed by the current index paradigm that may be ecologically important. We extend this finding to empirical plant–pollinator communities, showing how two bee species, with similar direct interactions, differ in how specialised their competitors are. These examples underscore the need to not rely solely on network‐ and species‐level indices for characterising the structure of bipartite ecological networks.

The vulnerability of plant-pollinator communities to honeybee decline: A comparative network analysis in different habitat types

The populations of most pollinators, including honeybees, are declining that heavily affects both crop and wild plant pollination. Wild bee diversity and habitat type may modulate these effects. We addressed the question how the structure of plant-pollinator networks in different habitat types may influence the vulnerability of pollinator communities to the hypothetical loss of honeybees. We performed network analysis based on plant-visitation data in a traditional agricultural landscape and quantified the structural vulnerability (i.e. the effect of the loss of honeybee) of the plant-pollinator networks by a topological index (distance-based fragmentation). We found that very different plant-pollinator communities inhabited the studied different agricultural habitat types. The early summer arable fields had the most, pastures in mid-summer had the less vulnerable structure and, in general, an intermediate plant/pollinator ratio was associated with high vulnerability in the absence of honeybees. We suggest that increased plant species richness can ensure higher wild bee diversity and more stable plant-pollinator networks without honeybee, where flower-visitation can rely more on wild bees. Decreased management intensity in agricultural landscapes can therefore contribute to the maintenance of diverse plant-pollinator communities in agricultural landscapes and to sustainable farming.

Past and potential future effects of habitat fragmentation on structure and stability of plant-pollinator and host-parasitoid networks.

Habitat fragmentation is a primary threat to biodiversity, but how it affects the structure and stability of ecological networks is poorly understood. Here, we studied plant-pollinator and host-parasitoid networks on 32 calcareous grassland fragments covering a size gradient of several orders of magnitude and with amounts of additional habitat availability in the surrounding landscape that varied independent of fragment size. We find that additive and interactive effects of habitat fragmentation at local (fragment size) and landscape scales (1,750 m radius) directly shape species communities by altering the number of interacting species and, indirectly, their body size composition. These, in turn, affect plant-pollinator, but not host-parasitoid, network structure: the nestedness and modularity of plant-pollinator networks increase with pollinator body size. Moreover, pollinator richness increases modularity. In contrast, the modularity of host-parasitoid networks decreases with host richness, whereas neither parasitoid richness nor body size affects network structure. Simulating species coextinctions also reveals that the structure-stability relationship depends on species' sensitivity to coextinctions and their capacity for adaptive partner switches, which differ between mutualistic and antagonistic interaction partners. While plant-pollinator communities may cope with future habitat fragmentation by responding to species loss with opportunistic partner switches, past effects of fragmentation on the current structure of host-parasitoid networks may strongly affect their robustness to coextinctions under future habitat fragmentation.

Structural stability as a consistent predictor of phenological events.

The timing of the first and last seasonal appearance of a species in a community typically follows a pattern that is governed by temporal factors. While it has been shown that changes in the environment are linked to phenological changes, the direction of this link appears elusive and context-dependent. Thus, finding consistent predictors of phenological events is of central importance for a better assessment of expected changes in the temporal dynamics of ecological communities. Here we introduce a measure of structural stability derived from species interaction networks as an estimator of the expected range of environmental conditions compatible with the existence of a community. We test this measure as a predictor of changes in species richness recorded on a daily basis in a high-arctic plant-pollinator community during two spring seasons. We find that our measure of structural stability is the only consistent predictor of changes in species richness among different ecological and environmental variables. Our findings suggest that measures based on the notion of structural stability can synthesize the expected variation of environmental conditions tolerated by a community, and explain more consistently the phenological changes observed in ecological communities.