Phenologically explicit models for studying plant–pollinator interactions under climate change

Climate change is significantly influencing phenology. One potential effect is that historically interacting partners will respond to climate change at different rates, creating the potential for a phenological mismatch among previously synchronized interacting species, or even sexes of the same species. Focusing on plant demographics in a plant–pollinator interaction, we develop a hybrid dynamical model that uses a “non-autonomous” differential equation system (Zonneveld model) for within-season dynamics and discrete equations for season-to-season dynamics. Our model outlines how and when changes in the relative phenologies of an interacting species pair will alter the demographic outcome of the interaction. For our plant–pollinator system, we find that plant population growth rates are particularly sensitive to phenology mismatch when flowers are short-lived, when pollinators are short-lived, or when flowers and pollinators exhibit high levels of within-population synchrony in emergence or arrival dates. More generally, our aim is to introduce the use of hybrid dynamical models as a framework through which researchers can directly explore the demographic consequences of climatically driven phenological change.     

RATES OF FLORAL EVOLUTION: ADAPTATION TO BUMBLEBEE POLLINATION IN AN ALPINE WILDFLOWER,POLEMONIUM VISCOSUM

Animal pollinators are thought to shape floral evolution, yet the tempo of this process has seldom been measured. I used the prediction equation of quantitative genetics, R = h²S , to predict the rate at which a change in pollinator abundance may have caused divergence in floral morphology of the alpine skypilot, Polemonium viscosum. A selection experiment determined the rate at which such divergence can actually proceed. Corolla flare in this species increases by 12% from populations pollinated by a wide assemblage of insect visitors to those pollinated only by bumblebees. To simulate the evolutionary process giving rise to this change, I used a pollinator selection experiment. Plants with broad flowers set significantly more seeds than plants with narrow flowers under bumblebee pollination but had equivalent fecundity when visited by other insects or hand-pollinated. Bumblebee-mediated selection for broad corolla flare intensified from 0.07 at seed set to 0.17 at progeny establishment. Maternal parent-offspring regression yielded a confidence interval of 0.22–1.00 for trait heritability. Given these parameter estimates, the prediction equation shows that broadly flared flowers of bumblebee-pollinated P. viscosum could have evolved from narrower ones in a single generation. This prediction is matched by an observed 9% increase in offspring corolla flare after a single bout of bumblebee-mediated selection, relative to offspring of unselected controls. Findings show that plant populations can adapt rapidly to abrupt changes in pollinator assemblages.     

Effects of floral traits and plant genetic composition on pollinator behavior

Pollinator-mediated selection plays a major role in floral evolution and speciation. Floral traits that influence animal pollinator behavior are the target of pollinator-mediated selection, but can only evolve if floral phenotypes have underlying genetic variation. Thus, understanding the genetic basis of a floral trait is a crucial step in studying pollinator-mediated selection. In this study I tested the effect of quantitative trait loci (QTL) underlying floral traits on pollinator behavior in recombinant inbred lines (RILs) in the common sunflower, Helianthus annuus L. and its crop relative. The indirect effects of QTL on pollinator behavior, mediated by floral phenotypes, were analyzed for six insect visitor types using structural equation modeling (SEM) and path analysis. For three of the six visitor types (large and small bees and non-bee insects) valid models were revealed when all three levels (QTL, floral traits, and pollinator behavior) were incorporated. Nested model without genetics were validated for five of the six visitor types. The results suggest that insect behavior as a reaction to floral phenotypes is affected by the genetic architecture of floral traits. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: Heikki Hokkanen     

Colour evolution within orchids depends on whether the pollinator is a bee or a fly

• Orchids are a classic angiosperm model for understanding biotic pollination. We studied orchid species within two species‐rich herbaceous communities that are known to have either hymenopteran or dipteran insects as the dominant pollinators, in order to understand how flower colour relates to pollinator visual systems.
• We analysed features of the floral reflectance spectra that are significant to pollinator visual systems and used models of dipteran and hymenopteran colour vision to characterise the chromatic signals used by fly‐pollinated and bee‐pollinated orchid species.
• In contrast to bee‐pollinated flowers, fly‐pollinated flowers had distinctive points of rapid reflectance change at long wavelengths and a complete absence of such spectral features at short wavelengths. Fly‐pollinated flowers also had significantly more restricted loci than bee‐pollinated flowers in colour space models of fly and bee vision alike.
• Globally, bee‐pollinated flowers are known to have distinctive, consistent colour signals. Our findings of different signals for fly pollination is consistent with pollinator‐mediated selection on orchid species that results from the distinctive features of fly visual systems.

     

Variable flowering phenology and pollinator use in a community suggest future phenological mismatch

Recent anthropogenic climate change is strongly associated with average shifts toward earlier seasonal timing of activity (phenology) in temperate-zone species. Shifts in phenology have the potential to alter ecological interactions, to the detriment of one or more interacting species. Recent models predict that detrimental phenological mismatch may increasingly occur between plants and their pollinators. One way to test this prediction is to examine data from ecological communities that experience large annual weather fluctuations. Taking this approach, we analyzed interactions over a four-year period among 132 plant species and 665 pollinating insect species within a Mediterranean community. For each plant species we recorded onset and duration of flowering and number of pollinator species. Flowering onset varied among years, and a year of earlier flowering of a species tended to be a year of fewer species pollinating its flowers. This relationship was attributable principally to early-flowering species, suggesting that shifts toward earlier phenology driven by climate change may reduce pollination services due to phenological mismatch. Earlier flowering onset of a species also was associated with prolonged flowering duration, but it is not certain that this will counterbalance any negative effects of lower pollinator species richness on plant reproductive success. Among plants with different life histories, annuals were more severely affected by flowering–pollinator mismatches than perennials. Specialized plant species (those attracting a smaller number of pollinator species) did not experience disproportionate interannual fluctuations in phenology. Thus they do not appear to be faced with disproportionate fluctuations in pollinator species richness, contrary to the expectation that specialists are at greatest risk of losing mutualistic interactions because of climate change.     

Do we realize the full impact of pollinator loss on other ecosystem services and the challenges for any restoration in terrestrial areas?

Pollinators are key agents for ecosystems and humankind concerning biodiversity, agriculture, climate change adaptation, and all other ecosystem services. Particularly in industrialized countries pollinator diversity is in decline. The bulk of research is on entomological or plant‐pollinator network related topics, but the broad range of impacts of pollinator loss on coupled human and natural systems is not yet studied. As 87% of all flowering plants depend on pollinators, they are basic for all ecosystem services to some extent. Therefore, pollinator loss might cause simultaneous degradation of ecosystem services inducing counterproductive human responses and interlinked poverty spirals. The interaction of climate change, a main risk factor for pollinators, and unadvised human responses to pollinator decline are rarely studied. Tipping points of pollinator loss are not yet identified. Can counterproductive human responses to pollinator deficiency upscale pollinator decline toward a pollinator‐loss syndrome in the course of climate change? The article argues for research on the impacts of pollinator loss on other ecosystem services, useful and counterproductive human strategies on pollinator‐loss induced degradation, and the integration of pollinator protection into all terrestrial restoration efforts.     

Climate mediates roles of pollinator species in plant–pollinator networks

Aim

Understanding how climate conditions influence plant–pollinator interactions at the global scale is crucial to understand how pollinator communities and ecosystem function respond to environmental change. Here, we investigate whether climate drives differences in network roles of the main insect pollinator orders: Diptera, Coleoptera, Lepidoptera and Hymenoptera.

Location

Global.

Time period

1968–2020.

Major taxa studied

Diptera, Coleoptera, Lepidoptera and Hymenoptera.

Methods

We collated plant–pollinator networks from 26 countries and territories across the five main Köppen–Geiger climate zones. In total, we compiled data from 101 networks that included >1500 plant species from 167 families and >2800 pollinator species from 163 families. We assessed differences in the composition of plant–pollinator interactions among climate zones using a permutational ANOVA. We calculated standard network metrics for pollinator taxonomic groups and used Bayesian generalized mixed models to test whether climate zone influenced the proportion of pollinator network links and the level of pollinator generalism.

Results

We found that climate is a strong driver of compositional dissimilarities between plant–pollinator interactions. Relative to other taxa, bees and flies made up the greatest proportion of network links across climate zones. When network size was accounted for, bees were the most generalist pollinator group in the tropics, whereas non-bee Hymenoptera were the most generalist in arid zones, and syrphid flies were the most generalist in polar networks.

Main conclusions

We provide empirical evidence at the global scale that climate strongly influences the roles of different pollinator taxa within networks. Importantly, non-bee taxa, particularly flies, play central network roles across most climate zones, despite often being overlooked in pollination research and conservation. Our results identify the need for greater understanding of how global environmental change affects plant–pollinator interactions.     

Plant–pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations?

Climate change can affect plant–pollinator interactions in a variety of ways, but much of the research attention has focused on whether independent shifts in phenology will alter temporal overlap between plants and pollinators. Here I review the research on plant–pollinator mismatch, assessing the potential for observational and experimental approaches to address particular aspects of the problem. Recent, primarily observational studies suggest that phenologies of co‐occurring plants and pollinators tend to respond similarly to environmental cues, but that nevertheless, certain pairs of interacting species are showing independent shifts in phenology. Only in a few cases, however, have these independent shifts been shown to affect population vital rates (specifically, seed production by plants) but this largely reflects a lack of research. Compared to the few long‐term studies of pollination in natural plant populations, experimental manipulations of phenology have yielded relatively optimistic conclusions about effects of phenological shifts on plant reproduction, and I discuss how issues of scale and frequency‐dependence in pollinator behaviour affect the interpretation of these ‘temporal transplant’ experiments. Comparable research on the impacts of mismatch on pollinator populations is so far lacking, but both observational studies and focused experiments have the potential to improve our forecasts of pollinator responses to changing phenologies. Finally, while there is now evidence that plant–pollinator mismatch can affect seed production by plants, it is still unclear whether this phenological impact will be the primary way in which climate change affects plant–pollinator interactions. It would be useful to test the direct effects of changing climate on pollinator population persistence, and to compare the importance of phenological mismatch with other threats to pollination.     

The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae)

Differences in floral traits among plant species have often been attributed to adaptation to pollinators. We explored the importance of pollinator shifts in explaining floral divergence among 15 species of Iochroma. We examined four continuously varying floral traits: corolla length, nectar reward, display size, and flower color. Pollinator associations were characterized with a continuously varying measure of pollinator importance (the product of visitation and pollen deposition) for four groups of pollinators: hummingbirds, Hymenoptera, Lepidoptera, and Diptera. A phylogenetic generalized least squares approach was used to estimate correlations between pollinator groups and floral traits across a sample of Bayesian trees using different models of trait evolution. Multivariate analyses were also employed to identify suites of traits associated with each pollinator group. We found that nonphylogenetic models typically fit the data better than phylogenetic models (Brownian motion, Ornstein-Uhlenbeck), and thus results varied little across trees. Our results indicated that species with high nectar reward and large displays are significantly more likely to be pollinated by hummingbirds and less likely to be pollinated by all groups of insects. Corolla length and flower color did not show any consistently significant associations with pollinator groups. For these two traits, we discuss alternative evolutionary forces, including phylogenetic inertia and community-level factors.     

Ecology and evolution of plant�Cpollinator interactions

Background

Some of the most exciting advances in pollination biology have resulted from interdisciplinary research combining ecological and evolutionary perspectives. For example, these two approaches have been essential for understanding the functional ecology of floral traits, the dynamics of pollen transport, competition for pollinator services, and patterns of specialization and generalization in plant–pollinator interactions. However, as research in these and other areas has progressed, many pollination biologists have become more specialized in their research interests, focusing their attention on either evolutionary or ecological questions. We believe that the continuing vigour of a synthetic and interdisciplinary field like pollination biology depends on renewed connections between ecological and evolutionary approaches.

Scope

In this Viewpoint paper we highlight the application of ecological and evolutionary approaches to two themes in pollination biology: (1) links between pollinator behaviour and plant mating systems, and (2) generalization and specialization in pollination systems. We also describe how mathematical models and synthetic analyses have broadened our understanding of pollination biology, especially in human-modified landscapes. We conclude with several suggestions that we hope will stimulate future research. This Viewpoint also serves as the introduction to this Special Issue on the Ecology and Evolution of Plant–Pollinator Interactions. These papers provide inspiring examples of the synergy between evolutionary and ecological approaches, and offer glimpses of great accomplishments yet to come.Key words: Floral traits, generalization and specialization, global change, male fitness, mating systems, multiple paternity, plant–pollinator networks, pollen and gene dispersal, pollinator behaviour, pollination syndromes, pollination webs, self-fertilization     

Insect preference for symmetrical artificial flowers

An insect preference for floral symmetry may be maintained because plants with symmetrical flowers, which are able to control developmental processes under given environmental conditions, also are able to provide more pollinator rewards than plants with asymmetrical flowers. Alternatively, insects may have an inherent preference for symmetrical structures and thereby impose selection for the maintenance of symmetry in flowers even in the absence of any pollinator rewards. We tested for an insect preference for radially symmetrical flowers by using horizontally placed units of four circular coloured flower models varying in size and symmetry. The shape and colour of the model flowers did not resemble any naturally occurring flowers in the environment. Insects and Hymenoptera, respectively (five species of Diptera and one species of Coleoptera) that visited the flower models clearly preferred symmetrical models over asymmetrical ones, and the ranking of visits to the models reflected a preference for large, symmetrical flowers. These results provide evidence for a preference for symmetrical flower models, even in the absence of pollinator rewards. Received: 11 September 1997 / Accepted: 2 November 1997     

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.     

The sudden collapse of pollinator communities

Declines in pollinator populations may harm biodiversity and agricultural productivity. Little attention has, however, been paid to the systemic response of mutualistic communities to global environmental change. Using a modelling approach and merging network theory with theory on critical transitions, we show that the scale and nature of critical transitions is likely to be influenced by the architecture of mutualistic networks. Specifically, we show that pollinator populations may collapse suddenly once drivers of pollinator decline reach a critical point. A high connectance and/or nestedness of the mutualistic network increases the capacity of pollinator populations to persist under harsh conditions. However, once a tipping point is reached, pollinator populations collapse simultaneously. Recovering from this single community‐wide collapse requires a relatively large improvement of conditions. These findings may have large implications for our view on the sustainability of pollinator communities and the services they provide.     

Additive effects of exotic plant abundance and land-use intensity on plant–pollinator interactions

The continuing spread of exotic plants and increasing human land-use are two major drivers of global change threatening ecosystems, species and their interactions. Separate effects of these two drivers on plant–pollinator interactions have been thoroughly studied, but we still lack an understanding of combined and potential interactive effects. In a subtropical South African landscape, we studied 17 plant–pollinator networks along two gradients of relative abundance of exotics and land-use intensity. In general, pollinator visitation rates were lower on exotic plants than on native ones. Surprisingly, while visitation rates on native plants increased with relative abundance of exotics and land-use intensity, pollinator visitation on exotic plants decreased along the same gradients. There was a decrease in the specialization of plants on pollinators and vice versa with both drivers, regardless of plant origin. Decreases in pollinator specialization thereby seemed to be mediated by a species turnover towards habitat generalists. However, contrary to expectations, we detected no interactive effects between the two drivers. Our results suggest that exotic plants and land-use promote generalist plants and pollinators, while negatively affecting specialized plant–pollinator interactions. Weak integration and high specialization of exotic plants may have prevented interactive effects between exotic plants and land-use. Still, the additive effects of exotic plants and land-use on specialized plant–pollinator interactions would have been overlooked in a single-factor study. We therefore highlight the need to consider multiple drivers of global change in ecological research and conservation management.     

Buzziness as usual? Questioning the global pollination crisis

Concerns have been raised that invertebrate pollinators of crops and wild plants are in decline as a result of modern agricultural practices, habitat degradation, and introduced pests and diseases. This has led to demands for a response by land managers, conservationists and political decision makers to the impending 'global pollinator crisis'. In questioning this crisis, it becomes apparent that perceptions of a pollinator crisis are driven mainly by reported declines of crop-pollinating honeybees in North America, and bumblebees and butterflies in Europe, whereas native pollinator communities elsewhere show mixed responses to environmental change. Additionally, few staple food crops depend on pollinator services, and most crops that do are grown at small scales in diversified agro-ecosystems that are likely to support healthy pollinator communities, or in highly managed systems that are largely independent of wild pollinators. Consequently, justifying conservation action on the basis of deteriorating pollinator services might be misplaced. Nevertheless, existing initiatives to monitor pollinators are well founded, given the uncertainty about the dynamics of pollinator populations.     

The Importance of Pollinator Generalization and Abundance for the Reproductive Success of a Generalist Plant

Previous studies have examined separately how pollinator generalization and abundance influence plant reproductive success, but none so far has evaluated simultaneously the relative importance of these pollinator attributes. Here we evaluated the extent to which pollinator generalization and abundance influence plant reproductive success per visit and at the population level on a generalist plant, Opuntia sulphurea (Cactaceae). We used field experiments and path analysis to evaluate whether the per-visit effect is determined by the pollinator’s degree of generalization, and whether the population level effect (pollinator impact) is determined by the pollinator’s degree of generalization and abundance. Based on the models we tested, we concluded that the per-visit effect of a pollinator on plant reproduction was not determined by the pollinators’ degree of generalization, while the population-level impact of a pollinator on plant reproduction was mainly determined by the pollinators’ degree of generalization. Thus, generalist pollinators have the greatest species impact on pollination and reproductive success of O. sulphurea. According to our analysis this greatest impact of generalist pollinators may be partly explained by pollinator abundance. However, as abundance does not suffice as an explanation of pollinator impact, we suggest that vagility, need for resource consumption, and energetic efficiency of generalist pollinators may also contribute to determine a pollinator’s impact on plant reproduction.     

Drought and leaf herbivory influence floral volatiles and pollinator attraction

The effects of climate change on species interactions are poorly understood. Investigating the mechanisms by which species interactions may shift under altered environmental conditions will help form a more predictive understanding of such shifts. In particular, components of climate change have the potential to strongly influence floral volatile organic compounds (VOCs) and, in turn, plant–pollinator interactions. In this study, we experimentally manipulated drought and herbivory for four forb species to determine effects of these treatments and their interactions on (1) visual plant traits traditionally associated with pollinator attraction, (2) floral VOCs, and (3) the visitation rates and community composition of pollinators. For all forbs tested, experimental drought universally reduced flower size and floral display, but there were species‐specific effects of drought on volatile emissions per flower, the composition of compounds produced, and subsequent pollinator visitation rates. Moreover, the community of pollinating visitors was influenced by drought across forb species (i.e. some pollinator species were deterred by drought while others were attracted). Together, these results indicate that VOCs may provide more nuanced information to potential floral visitors and may be relatively more important than visual traits for pollinator attraction, particularly under shifting environmental conditions.     

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.     

Sky islands as foci for divergence of fig trees and their pollinators in southwest China

The dynamics of populations and their divergence over time have shaped current levels of biodiversity and in the case of the “sky islands” of mountainous southwest (SW) China have resulted in an area of exceptional botanical diversity. Ficus tikoua is a prostrate fig tree subendemic to the area that displays unique intraspecific diversity, producing figs typical of different pollination modes in different parts of its range. By combining climate models, genetic variation in populations of the tree's obligate fig wasp pollinators and distributions of the different plant phenotypes, we examined how this unusual situation may have developed. We identified three genetically distinct groups of a single Ceratosolen pollinator species that have largely parapatric distributions. The complex topography of the region contributed to genetic divergence among the pollinators by facilitating geographical isolation and providing refugia. Migration along elevations in response to climate oscillations further enhanced genetic differentiation of the three pollinator groups. Their distributions loosely correspond to the distributions of the functionally significant morphological differences in the male figs of their host plants, but postglacial expansion of one group has not been matched by spread of its associated plant phenotype, possibly due to a major river barrier. The results highlight how interplay between the complex topography of the “sky island” complex and climate change has shaped intraspecies differentiation and relationships between the plant and its pollinator. Similar processes may explain the exceptional botanical diversity of SW China.     

探讨监测传粉者的方法

种子植物的有性生殖依赖于花粉传递, 传粉者是花粉传递的媒介。传粉者为野生植物和农作物提供的传粉服务, 是我们绿色星球最重要的生态过程之一, 在维持生物多样性和农作物生产方面具有重要作用。农业集约化、生境破碎、全球气候变暖等因素加剧了传粉者衰减和灭绝的风险, 对生态系统的功能和农业生产造成了不利影响。为了维系植物与传粉者生态互作关系的稳定性, 人们建立了一系列从局部地区到国际、由普通民众到科研人员参与的传粉者监测项目, 以期掌握传粉生态系统的状况和发展趋势, 为自然和农业生态系统的健康提供预警和反馈。本文强调了监测传粉者的首要前提条件, 即正确区分传粉者和访花者; 总结了监测传粉者的直接和间接方法, 包括群落水平的直接观察监测, 以及利用关联数据进行间接推断与调查; 介绍了具有潜力的由大众参与的公众监测项目。针对7种常见传粉者类群, 讨论了可行的适用于各类群的监测方法, 为监测拓展到更多的传粉者类群提供了可能。期望能为生物多样性的保护、传粉者动态的精准监测提供建议与参考。