The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks

Striking changes in food web structure occur with alterations in resource supply. Like predator–prey interactions, many mutualisms are also consumer–resource interactions. However, no studies have explored how the structure of plant–pollinator networks may be affected by nutrient enrichment. For three years, we enriched plots of subalpine plant communities with nitrogen and observed subsequent effects on plant–pollinator network structure. Although nitrogen enrichment affects floral abundance and rates of pollinator visitation, we found no effects of nitrogen enrichment on the core group of generalist plants and pollinators or on plant–pollinator network structure parameters, such as network topology (the identity and frequency of interactions) and the degree of nestedness. However, individual plant and pollinator taxa were packed into the nested networks differently among nitrogen treatments. In particular, pollinators visited different numbers and types of plants in the nested networks, suggesting weak, widespread effects of nitrogen addition on individual taxa. Independent of nitrogen enrichment, there were large interannual differences in network structure and interactions, due to species turnover among years and flexibility in interacting with new partners. These data suggest that the community structure of small‐scale mutualistic networks may be relatively robust to short‐term bottom–up changes in the resource supply, but sensitive to variation in the opportunistic behavior and turnover of plant and pollinator species among years.     

Trait matching and phenological overlap increase the spatio‐temporal stability and functionality of plant–pollinator interactions

Morphology and phenology influence plant–pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio‐temporal stability (measured as variability) of plant–pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6‐year plant–pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well‐matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non‐random extinction of species with well‐matched traits could decrease the stability of interactions within communities and reduce their functioning.     

Between‐year changes in community composition shape species’ roles in an Arctic plant–pollinator network

Inter‐annual turnover in community composition can affect the richness and functioning of ecological communities. If incoming and outgoing species do not interact with the same partners, ecological functions such as pollination may be disrupted. Here, we explore the extent to which turnover affects species’ roles – as defined based on their participation in different motifs positions – in a series of temporally replicated plant–pollinator networks from high‐Arctic Zackenberg, Greenland. We observed substantial turnover in the plant and pollinator assemblages, combined with significant variation in species’ roles between networks. Variation in the roles of plants and pollinators tended to increase with the amount of community turnover, although a negative interaction between turnover in the plant and pollinator assemblages complicated this trend for the roles of pollinators. This suggests that increasing turnover in the future will result in changes to the roles of plants and likely those of pollinators. These changing roles may in turn affect the functioning or stability of this pollination network.     

传粉网络的研究进展:网络的结构和动态

植物与传粉者之间相互作用,构成了复杂的传粉网络。近年来,社会网络分析技术的发展使得复杂生态网络的研究成为可能。从群落水平上研究植物与传粉者之间的互惠关系,为理解群落的结构和动态以及花部特征的演化提供了全新的视角。传粉网络的嵌套结构说明自然界的传粉服务存在冗余,而且是相对泛化的物种主导了传粉。在多年或者多季度的传粉网络中,虽然有很高的物种替换率,但是其网络结构仍然保持相对稳定,说明传粉网络对干扰有很强的抗性。尽管有关网络结构和动态的研究逐渐增多,但传粉网络维持的机制仍不清楚。网络结构可以部分由花部特征与传粉者的匹配来解释,也受到系统发生的制约,影响因素还包括群落构建的时间和物种多样性,以及物种在群落中的位置。开展大尺度群落动态的研究,为探索不同时间尺度、不同物种多样性水平上的传粉网络的生态学意义提供了条件。但已有的研究仍存在不足,比如基于访问观察的网络无法准确衡量传粉者的访问效率和植物间的花粉流动,以及结果受到调查精度区域研究不平衡的制约等。目前的研究只深入到传粉者携带花粉构成成分的水平,传粉者访问植物的网络不能代表植物的整个传粉过程。因此,研究应当更多地深入到物种之间关系对有性生殖的切实影响上。     

Effects of different types of low‐intensity management on plant‐pollinator interactions in Estonian grasslands

In the face of global pollinator decline, extensively managed grasslands play an important role in supporting stable pollinator communities. However, different types of extensive management may promote particular plant species and thus particular functional traits. As the functional traits of flowering plant species (e.g., flower size and shape) in a habitat help determine the identity and frequency of pollinator visitors, they can also influence the structures of plant−pollinator interaction networks (i.e., pollination networks). The aim of this study was to examine how the type of low‐intensity traditional management influences plant and pollinator composition, the structure of plant−pollinator interactions, and their mediation by floral and insect functional traits. Specifically, we compared mown wooded meadows to grazed alvar pastures in western Estonia. We found that both management types fostered equal diversity of plants and pollinators, and overlapping, though still distinct, plant and pollinator compositions. Wooded meadow pollination networks had significantly higher connectance and specialization, while alvar pasture networks achieved higher interaction diversity at a standardized sampling of interactions. Pollinators with small body sizes and short proboscis lengths were more specialized in their preference for particular plant species and the specialization of individual pollinators was higher in alvar pastures than in wooded meadows. All in all, the two management types promoted diverse plant and pollinator communities, which enabled the development of equally even and nested pollination networks. The same generalist plant and pollinator species were important for the pollination networks of both wooded meadows and alvar pastures; however, they were complemented by management‐specific species, which accounted for differences in network structure. Therefore, the implementation of both management types in the same landscape helps to maintain high species and interaction diversity.     

Drivers of plant individual-based pollinator visitation network topology in an arid ecosystem

Interactions with pollinators underlie the structure and function of plant communities. Network analysis is a valuable tool for studying plant-pollinator interactions, but these networks are most frequently built by aggregating interactions at the species level. Interactions are between individuals and an advantage of individual-based networks is the ability to integrate inter-individual variation in traits and environmental context within complex ecological networks. We studied the influence of inter-individual variation on pollinator sharing among foundation shrubs and cactus in a desert ecosystem using plant individual-based pollinator visitation networks. We hypothesized that the traits that alter attractiveness of plants to pollinators will also influence an individual plant's role within the visitation network. Foundation plants growing with higher densities of nearby blooming shrubs had higher pollinator visitation rates and had greater access to the conspecific mating pool, suggesting widespread and diffuse pollination facilitation within this community. Further, shrub density influenced the role of betweenness centrality and the effective number of partners (e^H). Floral display size also influenced the effective number of interaction partners but did not directly influence the centrality measures for individual plants or other measures of network structure despite increasing visitation rates. The individual-based visitation networks were significantly modular and module membership was predicted by species identity and pollinator visitation rates. Ecological and individual context mediate the outcome of pollinator-mediated interactions and are fundamental drivers of whole community structure. This study shows that the density of immediate neighbours can influence the overall structure of plant-pollinator interaction networks. Exploring the contribution of intraspecific variation to community interaction networks will improve our understanding of drivers of community-level ecological dynamics.     

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.     

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

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

Top‐down network analysis characterizes hidden termite–termite interactions

The analysis of ecological networks is generally bottom‐up, where networks are established by observing interactions between individuals. Emergent network properties have been indicated to reflect the dominant mode of interactions in communities that might be mutualistic (e.g., pollination) or antagonistic (e.g., host–parasitoid communities). Many ecological communities, however, comprise species interactions that are difficult to observe directly. Here, we propose that a comparison of the emergent properties from detail‐rich reference communities with known modes of interaction can inform our understanding of detail‐sparse focal communities. With this top‐down approach, we consider patterns of coexistence between termite species that live as guests in mounds built by other host termite species as a case in point. Termite societies are extremely sensitive to perturbations, which precludes determining the nature of their interactions through direct observations. We perform a literature review to construct two networks representing termite mound cohabitation in a Brazilian savanna and in the tropical forest of Cameroon. We contrast the properties of these cohabitation networks with a total of 197 geographically diverse mutualistic plant–pollinator and antagonistic host–parasitoid networks. We analyze network properties for the networks, perform a principal components analysis (PCA), and compute the Mahalanobis distance of the termite networks to the cloud of mutualistic and antagonistic networks to assess the extent to which the termite networks overlap with the properties of the reference networks. Both termite networks overlap more closely with the mutualistic plant–pollinator communities than the antagonistic host–parasitoid communities, although the Brazilian community overlap with mutualistic communities is stronger. The analysis raises the hypothesis that termite–termite cohabitation networks may be overall mutualistic. More broadly, this work provides support for the argument that cryptic communities may be analyzed via comparison to well‐characterized communities.     

Relative stability of core groups in pollination networks in a biodiversity hotspot over four years

Plants and their pollinators form pollination networks integral to the evolution and persistence of species in communities. Previous studies suggest that pollination network structure remains nested while network composition is highly dynamic. However, little is known about temporal variation in the structure and function of plant-pollinator networks, especially in species-rich communities where the strength of pollinator competition is predicted to be high. Here we quantify temporal variation of pollination networks over four consecutive years in an alpine meadow in the Hengduan Mountains biodiversity hotspot in China. We found that ranked positions and idiosyncratic temperatures of both plants and pollinators were more conservative between consecutive years than in non-consecutive years. Although network compositions exhibited high turnover, generalized core groups--decomposed by a k-core algorithm--were much more stable than peripheral groups. Given the high rate of turnover observed, we suggest that identical plants and pollinators that persist for at least two successive years sustain pollination services at the community level. Our data do not support theoretical predictions of a high proportion of specialized links within species-rich communities. Plants were relatively specialized, exhibiting less variability in pollinator composition at pollinator functional group level than at the species level. Both specialized and generalized plants experienced narrow variation in functional pollinator groups. The dynamic nature of pollination networks in the alpine meadow demonstrates the potential for networks to mitigate the effects of fluctuations in species composition in a high biodiversity area.     

The temporal dimension in individual‐based plant pollination networks

The pollination success of animal‐pollinated plants depends on the temporal coupling between flowering schedules and pollinator availability. Within a population, individual plants exhibiting disparate flowering schedules will be exposed to different pollinators when the latter exhibit temporal turnover. The temporal overlap between individual plants and pollinators will result in a turnover of interactions, which can be analyzed through a network approach. We have explored the temporal dynamics of individual‐based plant networks resulting from pairwise similarities in pollinator composition. During two flowering seasons, we surveyed the phenology and pollinator fauna of the individual plants from a population of Erysimum mediohispanicum (Brassicaceae). We analyzed the topology of these networks by means of their modularity, clustering, and core–periphery structure. These metrics are related to network functional properties such as cohesion, transitivity and centralization respectively. Afterwards, we analyzed the influence of each pollinator functional group on network topology. We found that network topology varied widely over time as a consequence of the differences in plant phenology and the idiosyncratic and contextual effect of pollinators. When integrating all temporary networks, the network became cohesive (non modular), transitive (locally clusterized), and centralized (core–periphery topology). These topologies could entail important consequences for plant reproduction. Our results highlight the importance of considering the entire flowering season and the necessity of making comprehensive temporal sampling when trying to build reliable interaction networks.     

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.     

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.     

Construction,validation, and application of nocturnal pollen transport networks in an agro‐ecosystem: a comparison using light microscopy and DNA metabarcoding

1. Moths are globally relevant as pollinators but nocturnal pollination remains poorly understood. Plant–pollinator interaction networks are traditionally constructed using either flower‐visitor observations or pollen‐transport detection using microscopy. Recent studies have shown the potential of DNA metabarcoding for detecting and identifying pollen‐transport interactions. However, no study has directly compared the realised observations of pollen‐transport networks between DNA metabarcoding and conventional light microscopy. 2. Using matched samples of nocturnal moths, we constructed pollen‐transport networks using two methods: light microscopy and DNA metabarcoding. Focussing on the feeding mouthparts of moths, we developed and provide reproducible methods for merging DNA metabarcoding and ecological network analysis to better understand species interactions. 3. DNA metabarcoding detected pollen on more individual moths, and detected multiple pollen types on more individuals than microscopy, although the average number of pollen types per individual was unchanged. However, after aggregating individuals of each species, metabarcoding detected more interactions per moth species. Pollen‐transport network metrics differed between methods because of variation in the ability of each to detect multiple pollen types per moth and to separate morphologically similar or related pollen. We detected unexpected but plausible moth–plant interactions with metabarcoding, revealing new detail about nocturnal pollination systems. 4. The nocturnal pollination networks observed using metabarcoding and microscopy were similar yet distinct, with implications for network ecologists. Comparisons between networks constructed using metabarcoding and traditional methods should therefore be treated with caution. Nevertheless, the potential applications of metabarcoding for studying plant–pollinator interaction networks are encouraging, especially when investigating understudied pollinators such as moths.     

Predicting the effect of competition on secondary plant extinctions in plant–pollinator networks

What are the limitations of models that predict the behavior of an ecological community based on a single type of species interaction? Using plant–pollinator network models as an example, we contrast the predicted vulnerability of a community to secondary extinctions under the assumption of purely mutualistic interactions versus mutualistic and competitive interactions. We find that competition among plant species increases the risk of secondary extinctions and extinction cascades. Simulations over a number of different network structures indicate that this effect is stronger in larger networks, more strongly connected networks and networks with higher plant:pollinator ratios. We conclude that efforts to model plant–pollinator communities will systematically over‐estimate community robustness to species loss if plant competition is ignored. However, because the effect of plant competition depends on network architecture, and because characterization of plant competition is work intensive, we suggest that efforts to account for plant competition in plant–pollinator network models should be focused on large, strongly connected networks with high plant:pollinator ratios.     

Reshaping our understanding of species’ roles in landscape‐scale networks

In network ecology, landscape‐scale processes are often overlooked, yet there is increasing evidence that species and interactions spill over between habitats, calling for further study of interhabitat dependencies. Here, we investigate how species connect a mosaic of habitats based on the spatial variation of their mutualistic and antagonistic interactions using two multilayer networks, combining pollination, herbivory and parasitism in the UK and New Zealand. Developing novel methods of network analysis for landscape‐scale ecological networks, we discovered that few plant and pollinator species acted as connectors or hubs, both within and among habitats, whereas herbivores and parasitoids typically have more peripheral network roles. Insect species’ roles depend on factors other than just the abundance of taxa in the lower trophic level, exemplified by larger Hymenoptera connecting networks of different habitats and insects relying on different resources across different habitats. Our findings provide a broader perspective for landscape‐scale management and ecological community conservation.     

Sampling method influences the structure of plant–pollinator networks

The search for general properties in the structure of ecological networks is currently a very active area of research. Meta‐analyses of published networks are a widely used technique. To have the best chance of discovering common properties though, networks should be constructed using a standardized approach. However, this is rarely the case, and pollination networks are constructed using two main methods: transects and timed observations. To investigate the potential for variation in network structure arising from different construction techniques we constructed plant–pollinator networks using two different methods at a single site, repeating our protocol over three field seasons. Transects and timed observation methods differ in the evenness of observation effort allocated among plant species in the observed community. We show that the uneven allocation of observation effort significantly affects the number of unique interactions in the network, and we reveal a strong trend in effects on web asymmetry and evenness of marginal abundance distributions. However, these effects do not appear to extend to the higher‐order properties of connectance and nestedness.     

Plant–pollinator networks in semi‐natural grasslands are resistant to the loss of pollinators during blooming of mass‐flowering crops

Mass‐flowering crops lead to spatial redistributions of pollinators and to transient shortages within nearby semi‐natural grasslands, but the impacts on plant–pollinator interactions remain largely unexplored. Here, we characterised which pollinator species are attracted by oilseed rape and how this affected the structure of plant–pollinator networks in nearby grasslands. We surveyed 177 networks from three countries (Germany, Sweden and United Kingdom) in 24 landscapes with high crop cover, and compared them to 24 landscapes with low or no oilseed rape during and after crop blooming. On average 55% of grassland pollinator species were found on the crop, which attracted 8–35% of individuals away from grasslands. However, networks in the grasslands were resistant to these reductions, since mainly abundant and highly mobile species were attracted. Nonetheless, simulations indicated that network structural changes could be triggered if > 50% of individuals were attracted to the crop (a value well‐above that found in our study system), which could affect community stability and resilience to further disturbance.     

Plant–floral visitor network structure in a smallholder <Emphasis Type="Italic">Cucurbitaceae</Emphasis> agricultural system in the tropics: implications for the extinction of main floral visitors

Animal pollination is responsible for the majority of the human food supply. Understanding pollination dynamics in agricultural systems is thus essential to help maintain this ecosystem service in the face of human disturbances. Surprisingly, our understanding of plant–pollinator interactions in widely distributed smallholder agricultural systems is still limited. Knowledge of pollination dynamics in these agricultural systems is necessary to fully assess how human disturbances may affect pollination services worldwide. In this study, we describe the structure of a plant–floral visitor network in a smallholder Cucurbitaceae agricultural system. We further identify the main floral visitors of these crops and tested their importance by simulating how their extinction affected network structure and robustness. The observed network was highly connected and generalized but it was neither nested nor compartmentalized. Our results suggest that the structure of agricultural plant–pollinator networks could be inherently different from those in natural communities. These differences in network structure may reflect differences in spatial distribution of floral resources between agricultural and natural systems. We identified Augochlora nigrocyanea and Peponapis limitaris as the two most frequent floral visitors. However, removal of these species did not affect network structure or its robustness, suggesting high levels of interaction rewiring. To our knowledge, this is one of the first studies to describe the structure of a plant–floral visitor network in diverse agricultural systems in the tropics. We emphasize the need for more studies that evaluate network structure in agricultural systems if we want to fully elucidate the impact of human disturbances on this key ecosystem service.