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.     

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。     

生长季放牧对高寒草甸传粉网络的影响

植物-传粉者相互作用面临人类活动的威胁。在青藏高原地区,放牧是一项主要的人类活动干扰,过度放牧导致高寒草甸植被严重退化。然而在该区域放牧如何影响植物-传粉者相互作用网络还不得而知。在青藏高原东部的高寒草甸选取了两个研究样点,每个样点包括一块禁牧样地（生长季禁牧）和放牧样地（全年放牧）。在2016年至2018年每年的生长季（7月和8月）进行了连续3年观测,共构建16个传粉网络。结果发现,在研究区域的高寒草甸生态系统中,传粉者群落的物种组成以双翅目昆虫为主。放牧后双翅目、鳞翅目以及鞘翅目传粉者的种类数减少,但膜翅目传粉者的种类数未受到放牧的影响。放牧干扰显著降低了群落中植物、传粉者以及它们之间相互作用的多样性,但对传粉网络的嵌套性和特化程度（H₂''）没有显著影响,说明网络的稳定性和恢复力没有受到放牧的影响。探讨了放牧对传粉网络的影响,发现区域放牧强度过大,降低了传粉昆虫和传粉网络的多样性。未来需要进一步深入研究高寒草甸生态系统中放牧强度对传粉网络的影响模式,以期为合理的放牧制度模式提供理论依据。     

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.     

Year‐to‐year variation in the topology of a plant–pollinator interaction network

Vigorous discussion of the degree of specialization in pollination interactions, combined with advances in the analysis of complex networks, has revitalized the study of entire plant–pollinator communities. Noticeably rare, however, are attempts to quantify temporal variation in the structure of plant–pollinator networks, and to determine whether the status of species as specialists or generalists is stable. Here we show that network structure varied through time in a montane meadow community from southern California, USA, in that pollinator species did not form the same links with plant species across years. Furthermore, composition of the generalized core group of species in the network varied among summers, as did the identity of those species involved in relationships that appeared to be reciprocally specialized within any one summer. These differences appear to be related to severe drought conditions experienced in the second summer of the 3 year study. In contrast to this variation, the pollinator community remained similarly highly nested in all three summers, even though species were packed into the nested matrix differently from year to year. These results suggest that plant–pollinator networks vary in detail through time, while retaining some basic topological properties. This dynamic aspect of community‐scale interactions has implications for both ecological and evolutionary inferences about pollination mutualisms.     

Temporal stability of pollinator preference in an alpine plant community and its implications for the evolution of floral traits

A traditional view of diverse floral traits is that they reflect differences in foraging preferences of pollinators. The role of pollinators in the evolution of floral traits has been questioned recently by broad community surveys, especially studies concerning variation in pollinator assemblages and visitation frequency, which suggest a diminished role of pollinators in floral evolution. Here, we investigate the relationships between six categories of floral traits of 29 species and 10 pollinator functional groups in an alpine meadow in the Hengduan Mountains of China, over three consecutive years. Simpson’s diversity index was used to estimate the level of pollinator generalization of each plant species by considering both pollinator groups and their relative visitation frequencies. Multivariate analyses indicated that eight of the ten pollinator groups showed constant preferences for at least two floral traits, leading to a relatively stable level of ecological generalization for most floral traits (two out of three categories), despite the fact that the level of generalization of the entire community varied across years. Shape preferences of butterflies, honeybees and beeflies varied such that open flowers exhibited a lower level of ecological generalization in 2007 than closed flowers, in contrast with the other 2 years. These results suggest that temporally stabilized preferences of diverse pollinators may contribute to the evolution of specialized versus generalized floral traits; however, their role may be moderated by variation in community structure, including both the composition and abundance of plants and pollinators.     

Pollination networks and functional specialization: a test using Lesser Antillean plant–hummingbird assemblages

Network analysis has in recent years improved our understanding of pollination systems. However, there is very little information about how functionally specialized plants and pollinators interact directly and indirectly in pollination networks. We have developed a parameter, Functional specialization index, to quantify functional specialization in pollination networks. Using this parameter, we examined whether different sized hummingbirds visit a distinct set of flowers in five hummingbird-pollinated plant assemblages from the Lesser Antilles, obtaining a simple relationship between hummingbird body size, network parameter and ecological function. In the Lesser Antilles, functionally specialized hummingbird pollination is distinct for plant species pollinated by the largest hummingbird species, whereas the pollination niche gradually integrates with the insect pollinator community as hummingbird body size decreases. The network approach applied in this study can be used to validate functional specialization and community-level interdependence between plants and pollinators, and it is therefore useful for evaluating and predicting plant resilience to pollinator loss, presently a global concern.     

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.     

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.     

Bird and insect pollinators differ in specialization and potential pollination services along disturbance and resource gradients

Combined studies of the communities and interaction networks of bird and insect pollinators are rare, especially along environmental gradients. Here, we determined how disturbance by fire and variation in sugar resources shape pollinator communities and interactions between plants and their pollinating insects and birds. We recorded insect and bird visits to 21 Protea species across 21 study sites and for 2 years in Fynbos ecosystems in the Western Cape, South Africa. We recorded morphological traits of all pollinator species (41 insect and nine bird species). For each site, we obtained estimates of the time since the last fire (range: 2–25 calendar years) and the Protea nectar sugar amount per hectare (range: 74–62 000 g/ha). We tested how post-fire age and sugar amount influence the total interaction frequency, species richness and functional diversity of pollinator communities, as well as pollinator specialization (the effective number of plant partners) and potential pollination services (pollination service index) of insects and birds. We found little variation in the total interaction frequency, species richness and functional diversity of insect and bird pollinator communities, but insect species richness increased with post-fire age. Pollinator specialization and potential pollination services of insects and birds varied differently along the environmental gradients. Bird pollinators visited fewer Protea species at sites with high sugar amount, while there was no such trend for insects. Potential pollination services of insect pollinators to Protea species decreased with increasing post-fire age and resource amounts, whereas potential pollination services of birds remained constant along the environmental gradients. Despite little changes in pollinator communities, our analyses reveal that insect and bird pollinators differ in their specialization on Protea species and show distinct responses to disturbance and resource gradients. Our comparative study of bird and insect pollinators demonstrates that birds may be able to provide more stable pollination services than insects.     

Community structure of pollination webs of Mauritian heathland habitats

Pollination webs have recently deepened our understanding of complex ecosystem functions and the susceptibility of biotic networks to anthropogenic disturbances. Extensive mutualistic networks from tropical species-rich communities, however, are extremely scarce. We present fully quantitative pollination webs of two plant–pollinator communities of natural heathland sites, one of which was in the process of being restored, on the oceanic island of Mauritius. The web interaction data cover a full flowering season from September 2003 to March 2004 and include all flowering plant and their pollinator species. Pollination webs at both sites were dominated by a few super-abundant, disproportionately well-connected species, and many rare and specialised species. The webs differed greatly in size, reflecting higher plant and pollinator species richness and abundance at the restored site. About one fifth of plant species at the smaller community received <3 visits. The main pollinators were insects from diverse taxonomic groups, while the few vertebrate pollinator species were abundant and highly linked. The difference in plant community composition between sites appeared to strongly affect the associated pollinator community and interactions with native plant species. Low visitation rate to introduced plant species suggested little indirect competition for pollinators with native plant species. Overall, our results indicated that the community structure was highly complex in comparison to temperate heathland communities. We discuss the observed differences in plant linkage and pollinator diversity and abundance between the sites with respect to habitat restoration management and its influence on pollination web structure and complexity. For habitat restoration to be successful in the long term, practitioners should aim to maintain structural diversity to support a species-rich and abundant pollinator assemblage which ensures native plant reproduction.     

Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization

We analysed the dynamics of a plant-pollinator interaction network of a scrub community surveyed over four consecutive years. Species composition within the annual networks showed high temporal variation. Temporal dynamics were also evident in the topology of the network, as interactions among plants and pollinators did not remain constant through time. This change involved both the number and the identity of interacting partners. Strikingly, few species and interactions were consistently present in all four annual plant-pollinator networks (53% of the plant species, 21% of the pollinator species and 4.9% of the interactions). The high turnover in species-to-species interactions was mainly the effect of species turnover (c. 70% in pairwise comparisons among years), and less the effect of species flexibility to interact with new partners (c. 30%). We conclude that specialization in plant-pollinator interactions might be highly overestimated when measured over short periods of time. This is because many plant or pollinator species appear as specialists in 1 year, but tend to be generalists or to interact with different partner species when observed in other years. The high temporal plasticity in species composition and interaction identity coupled with the low variation in network structure properties (e.g. degree centralization, connectance, nestedness, average distance and network diameter) imply (i) that tight and specialized coevolution might not be as important as previously suggested and (ii) that plant-pollinator interaction networks might be less prone to detrimental effects of disturbance than previously thought. We suggest that this may be due to the opportunistic nature of plant and animal species regarding the available partner resources they depend upon at any particular time.     

Contrasting effects of invasive plants in plant–pollinator networks

The structural organization of mutualism networks, typified by interspecific positive interactions, is important to maintain community diversity. However, there is little information available about the effect of introduced species on the structure of such networks. We compared uninvaded and invaded ecological communities, to examine how two species of invasive plants with large and showy flowers (Carpobrotus affine acinaciformis and Opuntia stricta) affect the structure of Mediterranean plant–pollinator networks. To attribute differences in pollination to the direct presence of the invasive species, areas were surveyed that contained similar native plant species cover, diversity and floral composition, with or without the invaders. Both invasive plant species received significantly more pollinator visits than any native species and invaders interacted strongly with pollinators. Overall, the pollinator community richness was similar in invaded and uninvaded plots, and only a few generalist pollinators visited invasive species exclusively. Invasive plants acted as pollination super generalists. The two species studied were visited by 43% and 31% of the total insect taxa in the community, respectively, suggesting they play a central role in the plant–pollinator networks. Carpobrotus and Opuntia had contrasting effects on pollinator visitation rates to native plants: Carpobrotus facilitated the visit of pollinators to native species, whereas Opuntia competed for pollinators with native species, increasing the nestedness of the plant–pollinator network. These results indicate that the introduction of a new species to a community can have important consequences for the structure of the plant–pollinator network.     

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.     

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.     

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.     

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

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Plant–pollinator networks: adding the pollinator's perspective

Pollination network studies are based on pollinator surveys conducted on focal plants. This plant-centred approach provides insufficient information on flower visitation habits of rare pollinator species, which are the majority in pollinator communities. As a result, pollination networks contain very high proportions of pollinator species linked to a single plant species (extreme specialists), a pattern that contrasts with the widely accepted view that plant–pollinator interactions are mostly generalized. In this study of a Mediterranean scrubland community in NE Spain we supplement data from an intensive field survey with the analysis of pollen loads carried by pollinators. We observed 4265 contacts corresponding to 19 plant and 122 pollinator species. The addition of pollen data unveiled a very significant number of interactions, resulting in important network structural changes. Connectance increased 1.43-fold, mean plant connectivity went from 18.5 to 26.4, and mean pollinator connectivity from 2.9 to 4.1. Extreme specialist pollinator species decreased 0.6-fold, suggesting that ecological specialization is often overestimated in plant–pollinator networks. We expected a greater connectivity increase in rare species, and consequently a decrease in the level of asymmetric specialization. However, new links preferentially attached to already highly connected nodes and, as a result, both nestedness and centralization increased. The addition of pollen data revealed the existence of four clearly defined modules that were not apparent when only field survey data were used. Three of these modules had a strong phenological component. In comparison to other pollination webs, our network had a high proportion of connector links and species. That is, although significant, the four modules were far from isolated.