Species traits and abundances predict metrics of plant–pollinator network structure,but not pairwise interactions

Plant–pollinator mutualistic networks represent the ecological context of foraging (for pollinators) and reproduction (for plants and some pollinators). Plant–pollinator visitation networks exhibit highly conserved structural properties across diverse habitats and species assemblages. The most successful hypotheses to explain these network properties are the neutrality and biological constraints hypotheses, which posit that species interaction frequencies can be explained by species relative abundances, and trait mismatches between potential mutualists respectively. However, previous network analyses emphasize the prediction of metrics of qualitative network structure, which may not represent stringent tests of these hypotheses. Using a newly documented temporally explicit alpine plant–pollinator visitation network, we show that metrics of both qualitative and quantitative network structure are easy to predict, even by models that predict the identity or frequency of species interactions poorly. A variety of phenological and morphological constraints as well as neutral interactions successfully predicted all network metrics tested, without accurately predicting species observed interactions. Species phenology alone was the best predictor of observed interaction frequencies. However, all models were poor predictors of species pairwise interaction frequencies, suggesting that other aspects of species biology not generally considered in network studies, such as reproduction for dipterans, play an important role in shaping plant–pollinator visitation network structure at this site. Future progress in explaining the structure and dynamics of mutualistic networks will require new approaches that emphasize accurate prediction of species pairwise interactions rather than network metrics, and better reflect the biology underlying species interactions.     

Pollinators visit related plant species across 29 plant–pollinator networks

Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant–pollinator networks of varying sizes, with “clade specialization” increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization.     

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.     

Are flowers red in teeth and claw? Exploitation barriers and the antagonist nature of mutualisms

The romantic perception of plant–animal mutualisms as a cooperative endeavour has been shattered in the last decades. While the classic theory of plant–pollinator coevolution assumed that partner coevolution is largely mutualistic, an increasing appreciation of the inherent conflict of interests between such partners has led to the realization that genes that confer a reproductive advantage to plants may have negative effects on their pollinators (and vice versa), giving rise to an apparent paradox: that antagonistic processes may drive coevolution among mutualistic partners. Under this new paradigm, mutualistic partners are bound by mutual interest but shaped by “selfish” antagonistic processes. Exploitation barriers mediated by resource competition among pollinators are a key element of this paradigm. Exploitation barriers involve traits such as tubular corollas, red flowers, toxic or deterrent rewards, and attractants of floral predators. Exploitation barriers result in resource partitioning, increasing floral fidelity of favoured pollinators and therefore plant fitness; but they often entail a physiological, behavioural or developmental cost for such favoured pollinators. Resource partitioning mediated by exploitation barriers is a very powerful driver of floral diversification, robust to variation in pollinator assemblages; hence, it may contribute to elucidating the occurrence of co-evolutionary changes in multi-species contexts. Exploitation barriers provide also a mechanistic basis for trait-based modelling of interaction networks, and represent a reason for caution in assuming fixed interaction identity or strength when modelling such networks (e.g. in rarefaction procedures used to estimate secondary extinctions). We propose to replace the misleading metaphor that depicts flowers and pollinators as cooperative partners by a metaphor in which plants and pollinator are traders, seeking to obtain different services from each other in complete disregard for the benefit of their mutualistic partner.     

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.     

Intrinsic and extrinsic factors acting on the reproductive process in alpine‐snowbed plants: roles of phenology,biological interaction,and breeding system

Pollinator activity and competition for pollinators lead to quantitative and qualitative pollen limitations on seed production and affect the reproductive success of plant species, depending on their breeding system (e.g., self‐compatibility and heterospecific compatibility) and genetic load (e.g., inbreeding depression and hybrid inviability). In alpine ecosystems, snowmelt regimes determine the distribution and phenology of plant communities. Plant species growing widely along a snowmelt gradient often grow with different species among local populations. Their pollinators also vary in their abundance, activity, and behavior during the season. These variations may modify plant–pollinator and plant–plant interactions. We integrated a series of our studies on the alpine dwarf shrub, Phyllodoce aleutica (Ericaceae), to elucidate the full set of intrinsic (species‐specific breeding system) and extrinsic factors (snow condition, pollinator activity, and interspecific competition) acting on their reproductive process. Seasonality of pollinator activity led to quantitative pollen limitation in the early‐blooming populations, whereas in the late‐blooming populations, high pollinator activity ensured pollination service, but interspecific competition for pollinators led to qualitative and quantitative pollen limitation in less competitive species. However, negative effects of illegitimate pollen receipt on seed‐set success might be reduced when cryptic incompatibility systems (i.e., outcross pollen grains took priority over self‐ and heterospecific pollen grains) could effectively prevent ovule and seed discounting. Our studies highlight the importance of species‐specific responses of plant reproduction to changing pollinator availability along environmental gradients to understand the general features of pollination networks in alpine ecosystems.     

Comparing the conservatism of ecological interactions in plant–pollinator and plant–herbivore networks

Conservatism in species interaction, meaning that related species tend to interact with similar partners, is an important feature of ecological interactions. Studies at community scale highlight variations in conservatism strength depending on the characteristics of the ecological interaction studied. However, the heterogeneity of datasets and methods used prevent to compare results between mutualistic and antagonistic networks. Here we perform such a comparison by taking plant–insect communities as a study case, with data on plant–herbivore and plant–pollinator networks. Our analysis reveals that plants acting as resources for herbivores exhibit the strongest conservatism in species interaction among the four interacting groups. Conservatism levels are similar for insect pollinators, insect herbivores and plants as interacting partners of pollinators, although insect pollinators tend to have a slightly higher conservatism than the two others. Our results thus clearly support the current view that within antagonistic networks, conservatism is stronger for species as resources than for species as consumer. Although the pattern tends to be opposite for plant–pollinator networks, our results suggest that asymmetry in conservatism is much less pronounced between the pollinators and the plant they interact with. We discuss these differences in conservatism strength in relation with the processes structuring plant–insect communities.     

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.     

Adaptive foraging behaviour of individual pollinators and the coexistence of co-flowering plants

Although pollinators can play a central role in determining the structure and stability of plant communities, little is known about how their adaptive foraging behaviours at the individual level, e.g. flower constancy, structure these interactions. Here, we construct a mathematical model that integrates individual adaptive foraging behaviour and population dynamics of a community consisting of two plant species and a pollinator species. We find that adaptive foraging at the individual level, as a complementary mechanism to adaptive foraging at the species level, can further enhance the coexistence of plant species through niche partitioning between conspecific pollinators. The stabilizing effect is stronger than that of unbiased generalists when there is also strong competition between plant species over other resources, but less so than that of multiple specialist species. This suggests that adaptive foraging in mutualistic interactions can have a very different impact on the plant community structure from that in predator–prey interactions. In addition, the adaptive behaviour of individual pollinators may cause a sharp regime shift for invading plant species. These results indicate the importance of integrating individual adaptive behaviour and population dynamics for the conservation of native plant communities.     

Adaptive foraging allows the maintenance of biodiversity of pollination networks

Pollination systems are recognized as critical for the maintenance of biodiversity in terrestrial ecosystems. Therefore, the understanding of mechanisms that promote the integrity of those mutualistic assemblages is an important issue for the conservation of biodiversity and ecosystem function. In this study we present a new population dynamics model for plant–pollinator interactions that is based on the consumer–resource approach and incorporates a few essential features of pollination ecology. The model was used to project the temporal dynamics of three empirical pollination network, in order to analyze how adaptive foraging of pollinators (AF) shapes the outcome of community dynamics in terms of biodiversity and network robustness to species loss. We found that the incorporation of AF into the dynamics of the pollination networks increased the persistence and diversity of its constituent species, and reduced secondary extinctions of both plants and animals. These findings were best explained by the following underlying processes: 1) AF increased the amount of floral resources extracted by specialist pollinators, and 2) AF raised the visitation rates received by specialist plants. We propose that the main mechanism by which AF enhanced those processes is (trophic) niche partitioning among animals, which in turn generates (pollen vector) niche partitioning among plants. Our results suggest that pollination networks can maintain their stability and diversity by the adaptive foraging of generalist pollinators.     

Temporal variations in the linkages between plants and flower visitors and the pollination success of Primula modesta along the snowmelt gradient

Although pollination networks between plants and flower visitors are diverse and flexible, seed production of many plant species is restricted by pollen limitation. Obligate outcrossers often suffer from low pollinator activity or severe interspecific competition for pollinator acquisition among co-flowering species. This study focused on seasonal changes in plant–flower visitor linkages in an alpine ecosystem and examined whether and how this seasonality affected the seed-set of Primula modesta, a self-incompatible distylous herb having long-tubed flowers. First, we recorded the linkages between plants and flower visitors along the snowmelt gradient. Then, pollination experiment was conducted to estimate the degree of pollen limitation over the course of flowering season of P. modesta. Flower visitors were classified by their tongue length based on the morphological matching with P. modesta flowers. As the season progressed, plant–visitor linkages became more diverse and generalized, and the visitation frequency to P. modesta flowers increased. In the later part of the season, however, the seed set of P. modesta was significantly reduced due to severe pollen limitation, presumably because of increased competition for long-tongued pollinators among co-flowering species. The present study revealed that pollinator availability for specialist species may be restricted even when plant–visitor linkages are diverse and generalized as a whole. In the case of P. modesta, morphological matching and competition for pollinators might be the main factors explaining this discrepancy.     

Predicting abundances of plants and pollinators using a simple compartmental mutualistic model

Key gaps to be filled in population and community ecology are predicting the strength of species interactions and linking pattern with process to understand species coexistence and their relative abundances. In the case of mutualistic webs, like plant–pollinator networks, advances in understanding species abundances are currently limited, mainly owing to the lack of methodological tools to deal with the intrinsic complexity of mutualisms. Here, we propose an aggregation method leading to a simple compartmental mutualistic population model that captures both qualitatively and quantitatively the size-segregated populations observed in a Mediterranean community of nectar-producing plant species and nectar-searching animal species. We analyse the issue of optimal aggregation level and its connection with the trade-off between realism and overparametrization. We show that aggregation of both plants and pollinators into five size classes or compartments leads to a robust model with only two tunable parameters. Moreover, if, in each compartment, (i) the interaction coefficients fulfil the condition of weak mutualism and (ii) the mutualism is facultative for at least one party of the compartment, then the interactions between different compartments are sufficient to guarantee global stability of the equilibrium population.     

What plant–pollinator network structure tells us about the mechanisms underlying the bidirectional biodiversity productivity relationship?

The Biodiversity – Ecosystem Functioning (B–EF) relationship remains a topic of ongoing debate with most studies focusing on primary productivity, and documenting that this relationship takes many forms. It remains unclear if biodiversity drives productivity or productivity shapes biodiversity or the relationship is bidirectional. B-EF studies explore almost exclusively the relationship between species richness and ecosystem functioning, while the role of biotic interactions, a key component of ecosystem functioning, has been neglected. Here, using data of 80 local plant–pollinator networks on 20 Aegean islands, and of gross primary productivity (GPP) from the MODIS satellite, we explored the bidirectional relationship between interaction network structure (nestedness and specialization), species richness (plants and pollinators) and mean and inter-annual variability of GPP. We found that nestedness and specialisation of plant–pollinator networks is driven by mean GPP. However, specialisation alone was a significant predictor of mean GPP, implying that networks tend to be more specialised in low-productivity areas. Pollinator species richness exerted a strong effect on mean GPP with the remaining factors playing a minor role, while the effect of mean GPP on pollinator species richness was weaker. Furthermore, the nestedness of plant–pollinator networks drives inter-annual variability of GPP with more nested networks displaying less variability, which is in accordance with the predictions of the insurance hypothesis. Plant and pollinator species richness were also associated with inter-annual variability of GPP.     

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.     

Network robustness and structure depend on the phenological characteristics of plants and pollinators

Many structural patterns have been found to be important for the stability and robustness of mutualistic plant–pollinator networks. These structural patterns are impacted by a suite of variables, including species traits, species abundances, their spatial configuration, and their phylogenetic history. Here, we consider a specific trait: phenology, or the timing of life history events. We expect that timing and duration of activity of pollinators, or of flowering in plants, could greatly affect the species'' roles within networks in which they are embedded. Using plant–pollinator networks from 33 sites in southern British Columbia, Canada, we asked (a) how phenological species traits, specifically timing of first appearance in the network and duration of activity in a network, were related to species'' roles within a network, and (b) how those traits affected network robustness to phenologically biased species loss. We found that long duration of activity increased connection within modules for both pollinators and plants and among modules for plants. We also found that date of first appearance was positively related to interaction strength asymmetry in plants but negatively related to pollinators. Networks were generally more robust to the loss of pollinators than plants, and robustness increased if the models allow new interactions to form when old ones are lost, constrained by overlapping phenology of plants and pollinators. Robustness declined with the loss of late‐flowering plants, which tended to have higher interaction strength asymmetry. In addition, robustness declined with loss of early‐flying or long‐duration pollinators. These pollinators tended to be among‐module connectors. Our results point to networks being limited by early‐flying pollinators. If plants flower earlier due to climate change, plant fitness may decline as they will depend on early emerging pollinators, unless pollinators also emerge earlier.     

Invasive plant integration into native plant–pollinator networks across Europe

The structure of plant–pollinator networks has been claimed to be resilient to changes in species composition due to the weak degree of dependence among mutualistic partners. However, detailed empirical investigations of the consequences of introducing an alien plant species into mutualistic networks are lacking. We present the first cross-European analysis by using a standardized protocol to assess the degree to which a particular alien plant species (i.e. Carpobrotus affine acinaciformis, Impatiens glandulifera, Opuntia stricta, Rhododendron ponticum and Solanum elaeagnifolium) becomes integrated into existing native plant–pollinator networks, and how this translates to changes in network structure.Alien species were visited by almost half of the pollinator species present, accounting on average for 42 per cent of the visits and 24 per cent of the network interactions. Furthermore, in general, pollinators depended upon alien plants more than on native plants. However, despite the fact that invaded communities received more visits than uninvaded communities, the dominant role of alien species over natives did not translate into overall changes in network connectance, plant linkage level and nestedness. Our results imply that although supergeneralist alien plants can play a central role in the networks, the structure of the networks appears to be very permeable and robust to the introduction of invasive alien species into the network.     

Invasibility of Nectarless Flowers in Plant–Pollinator Systems

This paper considers plant–pollinator systems in which plants are divided into two categories: The plants that secret a substantial volume of nectar in their flowers are called secretors, while those without secreting nectar are called nonsecretors (cheaters). The interaction between pollinators and secretors is mutualistic, while the interaction between pollinators and nonsecretors is parasitic. Both interactions can be described by Beddington–DeAngelis functional responses. Using dynamical systems theory, we show global dynamics of a pollinator–secretor–cheater model and demonstrate mechanisms by which nectarless flowers/nonsecretors can invade the pollinator–secretor system and by which the three species could coexist. We define a threshold in the nonsecretors’ efficiency in translating pollinator–cheater interaction into fitness, which is determined by parameters (factors) in the systems. When their efficiency is above the threshold, non-secretors can invade the pollinator–secretor system. While the nonsecretors’ invasion often leads to their persistence in pollinator–secretor systems, the model demonstrates situations in which the non-secretors’ invasion can drive secretors into extinction, which consequently leads to extinction of the nonsecretors themselves.     

Plant–pollinator network assembly along the chronosequence of a glacier foreland

Forelands of retreating glaciers offer an ideal model system to study community assembly processes during primary succession. As plants colonize the area that is freed from ice they should be accompanied by their pollinators to successfully reproduce and spread. However, little is known about the assembly of plant–pollinator networks. We therefore used quantitative network analysis to study the structure of plant–pollinator interactions at seven sites representing a chronosequence from 8 to 130 years since deglaciation on the foreland of the Morteratsch glacier (southeastern Switzerland). At these sites, individual visits of plant flowers by insects were recorded throughout the flowering season. Species richness of insect‐pollinated plants and plant‐pollinating insects, together with measures of interaction diversity and evenness, increased along the chronosequence at least for the first 80 years after deglaciation. Bees were the most frequent flower visitors at the two youngest sites, whereas flies dominated in mature communities. Pollinator generalization (the number of visited plant species weighted by interaction strength), but not plant generalization, strongly increased during the primary succession. This was reflected in a pronounced decline in network level specialization (measured as Blüthgen's H₂’) and interaction strength asymmetry during the first 60 years along the chronosequence, while nestedness increased along the chronosequence. Thus, our findings contradict niche‐theoretical predictions of increasing specialization of pollination systems during succession, but are in agreement with expectations from optimal foraging theory, predicting an increase in pollinator generalization with higher plant diversity but similar flower abundance, and an increase in diet breadth at higher pollinator densities during primary succession.     

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.