Interactions between pollinators and their plant hosts are central to maintaining global biodiversity and ensuring our food security. In this special issue, we compile reviews that summarize existing knowledge and point out key outstanding research areas to understand and safeguard pollinators, pollinators–host plant interactions and the pollination ecosystem services they provide. The vast diversity of the pollinator–plant interactions that exists on this planet still remains poorly explored, with many being associations involving a specialist pollinator partner, although historically most focus has been given to generalist pollinators, such as the honeybee. Two areas highlighted here are the ecology and evolution of oligolectic bee species, and the often-neglected groups of pollinators that forage solely at night. Advances in automated detection technologies could offer potential and complementary solutions to the current shortfall in knowledge on interactions occurring between less well-documented plant–pollinator associations, by increasing the collection range and capacity of flower visitation data over space and time. Pollinator–host plant interactions can be affected by external biotic factors, with herbivores and pathogens playing particularly important roles. Such interactions can be disrupted by modifying plant volatile and reward chemistry, with possible effects on pollinator attraction and pollination success. Mechanisms which underpin interactions between plants and their pollinators also face many anthropogenic disturbances. Reviews in this issue discuss threats from parasites and climate change to pollinator populations and plant–pollinator networks, and suggest new ways to mitigate these threats. While the protection of existing plant–pollinator networks will be a crucial goal for conservation biology, more research is needed to understand how lost interactions in degraded habitats may be restored with mutual benefits to plants and pollinators.
Growing importance of pollination biology
Plant–pollinator relationships are fundamental to the biodiversity of this planet, with an estimated 87.5% of all flowering plants depending to varying degrees on animal pollination , (Figure 1). These relationships are often mutually beneficial. Plants receive benefits from animals through the transfer of pollen between plants, ensuring fertilization and gene flow, while pollinators are rewarded by plants through the provision of food resources and/or a safe place to shelter, mate, oviposit and develop. Plant selection and acceptance by the pollinator, according to the quality and quantity of resources supplied by the plant partner, is crucial in securing the continuity and success of the partnership and maintaining the valued ecosystem services they provide.
The research and interest in plant–pollinator interactions has surged due to the growing realization of their central importance for global biodiversity and ecosystem services, and has become more urgent with increasing evidence for the decline of key insect, bird and mammal pollinators coming to light [2,3]. Seminal data analyses pushed pollination biology to the fore of intergovernmental conservation policy with the development of many international initiatives which set out to assess the importance of pollinators and outline research needs and strategies to mitigate the threats for pollination ecosystem services to policy makers. These initiatives include the Millenium Ecosystem Assessment , the Economics of Ecosystems and Biodiversity (TEEB) initiative [5,6], the EU biodiversity strategy  and the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) assessment report on pollinators, pollination and food production [8,9]. Economic valuation of pollination services from these initiatives, estimating the contribution of pollination services to the global economy at over $500 billion annually , have triggered additional research and policies to tackle pollinator decline by developing sustainable land-management practices. Urgent action is needed to mitigate the combined threats to pollinators from parasites, pesticides and loss of food plants .
Thus, ‘Anthecology’ (or the study of pollination biology), has evolved over 200 years of history since the foundational works of Sprengel and Darwin [11,12], now bringing together a range of disciplines not only including the classic subjects of botany, zoology and ecology, but advancing to include broader transdisciplinary studies incorporating environmental and agricultural sciences, climatology, genomics, microbiology and computer sciences to tackle the gaps in our knowledge in understanding the diversity, intensity and extent of detrimental drivers threatening species loss. Today, we find there are few higher education and agricultural extension facilities which fail to include pollination studies and applied training in green infrastructure and bee friendly environments in some way or another. Further mainstreaming in pollinator conservation through charities, citizen science projects and popular factual texts and children's fiction has improved the way we consider the importance and needs of pollinators for cultural, environmental and economic stability.
Where next and what is required?
The global decline of pollinator diversity and abundance [2,9,13] demands that we urgently look more closely at interactions between pollinators and their host plants, to determine which abiotic or biotic factors are key contributors, and develop strategies to halt or reverse species losses. Clearly many questions in pollination ecology remain unanswered and knowledge gaps remain . For example, we have only studied and elucidated a small fraction of the pollination mechanisms occurring in the estimated 300 000 animal–pollinated plants on earth. Our gap in knowledge on biotic interactions, sometimes called the Eltonian shortfall, forms a major impediment for our ability to understand and efficiently protect biodiversity . Even for many valued plant species, including plant products traditionally harvested from wild sources, we often lack sufficient understanding on wild pollen-vectoring taxa that contribute to successful pollination. This is particularly true for pollination in developing countries, but even within intensely studied areas like temperate Europe many gaps in our knowledge on the pollination ecology of common valued species still remain . Beyond this, regionally confined pollinator–plant interactions associated with endangered species of plants (IUCN Red listed) are vital to study in order to understand how to manage, conserve and restore these partnerships in their natural habitats, increasing their ability in the long-term to withstand environmental change. New tools, including genomics, metabolomics or automated detection and recognition technologies, will help to speed up our discovery and understanding of the diversity, ecology, and evolution of plant–pollinator interactions. This special issue of Emerging Topics in Life Sciences brings together a range of reviews for a transdisciplinary overview of current research in this area, each highlighting the requirements for future studies and methodologies to better understand mechanisms in pollination ecology and resolve negative drivers contributing to pollination service declines.
Bee-pollinators arguably provide the most well-known of all examples of pollinator–plant interactions, with critical importance for sustaining high yields in many agro-ecosystems. Rasmussen et al.  deviate from the common focus on generalists foraging in managed agricultural landscapes to highlight the wealth of specialized interactions that exist between bee species and host plants. They stress that a stronger focus on native, specialized bee species in agricultural and natural ecosystems may provide better pollination services in the future compared with the current overemphasis on generalist, often non-native bees like the European honeybee (Apis mellifera). They outline dietary, morphological and behavioural specializations of bees, linking factors such as foraging frequency and timing, cues for host-plant selection, adaptation for accessing and removing food rewards from flowers, and the nutritional chemistry of pollen with requirements for optimal protein quality for larval growth and development. Macgregor and Scott-Brown  present nocturnal pollination as an area of pollinator interactions rarely acknowledged in the growing body of literature on ecosystem services. While the evidence is given here on the service that nocturnal pollinator guilds contribute to a range of wild and minor commercial crop plants, the authors also draw attention to the urgent need for knowledge on the impact of drivers of global change, particularly those which impact the range of finely-tuned, sensory plant–insect signalling mechanisms which underpin beneficial mutualisms prone to switching to antagonisms. Kessler and Chautá  further the evidence for conflicts arising in plant-insect interactions, exploring trade-offs which can exist between activation of induced plant defence mechanisms against herbivorous insects and the direct and indirect effects this has on the attractiveness of flowers for pollinators, and resulting pollination success. Herbivore-induced defence strategies can occur at high cost to plant fitness, occurring through down-regulating primary metabolism and additionally through changes in floral traits (flower morphology, phenology and secondary metabolite production) potentially impacting attraction and suitability of rewards and resources on offer to pollen-vectors. Hypotheses are given for co-evolution of plants and associated insects driving selection for mechanisms that enable conflicts between repelling herbivores while attracting pollinators to be overcome, such as multifunctional chemistries for chemical cues.
In an increasingly connected world, commercially reared pollinators have been introduced to many parts of the world to produce premium commodities such as honey, and to improve pollination of agricultural crops. However, the global transfer of pollinators has come at the cost of the introduction of exotic parasites jumping species barriers to novel hosts which lack the ability to defend against these emergent parasites. In this context, Noël et al.  review recent research shedding new light on the host-parasite relationship between Varroa destructor and Apis mellifera, as the parasitic mite continues to extend its distribution range causing widespread destruction to honey bee colonies across continents together with its associated viruses. The authors discuss new insights into the behaviour, physiology and genetics of V. destructor which contribute to its current status as an economically important pest and highlight how new studies focusing on selection for host resistance are currently extending knowledge on the potential of such strategies for future methods of control. Fowler et al.  take a broader view of parasite challenges to bee pollinators beyond honeybees, and integrate current knowledge on immunity, nutritional ecology and microbial associates including potentially beneficial microbes of diverse social and solitary bee species. They present evidence that social behaviour in some bee species influences selection for defensive traits. The reduction in diet quality and exposure to pesticides can be key factors which increase the likelihood of bees becoming infected by impairing the immune system and altering the gut microbiome. Bees may also prevent or cure parasite infections through floral rewards from specific plant species [22,23]. As most research has been on eusocial bee species, they identify that there is a gap in knowledge in defense strategies in solitary and semi-social bee species. Gaining a more holistic understanding of these different factors affecting bee health will help inform future conservation management strategies.
Climate change presents another important threat to plant–pollinator interactions including predicted shifts in global temperatures and precipitation. This will lead to increased risk of fire and flooding and impact the geographic range of plants and the animals which are closely associated with them. Gérard et al.  summarize the evidence for spatial or phenological shifts that can occur in populations either side of these partnerships in response to global warming. The authors review the potential of ecological shifts occurring when a rise in ambient temperature impacts the equilibrium between the partnership. The impact on morphological traits and/or disruption to host attraction and foraging behaviours, for example through changes to floral volatile organic compound abundance, composition and emission rates, can ultimately lead to the formation of novel community assemblages. While generalist species can often fill the gap when pollinator abundance or distribution change, it is unclear if there are negative effects on plant fitness and ultimately if this impacts wider ecosystem functioning.
To effectively protect beneficial interactions between pollinators and their plant hosts from threats, and prevent plant decline or extinction from pollinator loss, we need to develop a comprehensive understanding of the diversity of plant–pollinator network interactions. Yet, the considerable time that a human observer has to expend to study the floral visitors of even just one plant species, means that we are still lacking knowledge on the extent of the diversity and functioning of many interactions that occur between flowering plants and their animal pollen-vectors [1,25]. This shortfall in natural history knowledge on the majority of plant–pollinator interactions that occur in nature limits our ability for effective conservation measures of vital mutualisms beneficial for both pollinator and plant partner, and community interactions beyond this. One potential path to overcoming this impediment may come from novel automated audio, visual and thermal detection systems, with examples and applications of new video technologies outlined by Pegoraro et al. . With advances in both hardware for digital imaging, and software for automated image or video analysis, flowers can be monitored in the field for their interactions with potential pollinators with rapidly decreasing human workload. Automated species recognition from captured images facilitated by artificial intelligence promises to speed up this process even further, and in conjunction with fieldwork studies could lead to a step change in our knowledge of pollination ecology.
Finally, a key challenge going forward will not only be to protect, but to restore lost diversity in plant–pollinator networks. Restoration of ecosystem functionality in degraded and fragmented habitats is an important, but often neglected concern for conservation programmes aiming to re-establish or increase populations of endangered plant species. A reduction in pollinator interactions within a restored community can impact the entire assembly. Cariveau et al.  review opportunities that arise to enhance pollination within ecological restoration programmes, focusing on the conservation of wild native species within plant communities. This approach provides contrast with the more widely studied, human-centric approach to restoration ecology within agricultural landscapes, where the majority of research in this area is dedicated to improving crop pollination. Attention is drawn to the deficit of knowledge on seed mixes to enable optimization to foraging preference and nutrition of native pollinators , to plant diversity and proportion to adjust for plant species dominance and to the value of non-floral rewards such as suitable nesting sites for example within restored habitats . The authors further discuss management at a local and landscape scale, defining the broad set of challenges that need to be addressed in planning, implementing and management of restored plant and pollinator communities if we are to achieve levels of pollinator functionality in these environments that are resilient to predicted global change.
Research in the area of pollination biology has reached a turning point where emerging solutions to some of the key problems are being identified, new technologies trialled and tested, and tools developed to measured, monitored and managed benefits (social, economic and environmental) in a more sustainable way. Increasingly, stakeholders and governmental agencies are implementing policies to safeguard this essential ecosystem service, and more objective, comprehensive data on plant–pollinators interactions will be needed. We hope this special issue will provide the reader with a timely overview of some of the most pertinent research avenues in pollination biology, and that it may contribute to the preservation of these ever fascinating and essential biotic interactions.
The authors declare that there are no competing interests associated with the manuscript.
A. Scott-Brown was supported by a Kew Career Development Research Fellowship (Chemical Ecology, Pollination). H. Koch was supported by the Peter Sowerby Foundation as the Ann Sowerby Fellow in Pollinator Health.
Both authors contributed equally to the literature review and writing of this manuscript.
Behind the production of this special issue has been much work from the Portland Press team, in particular, the staff from the two supporting Societies, The Royal Society of Biology and The Biochemical Society and we are very grateful for the help we have received in putting the issue together. We also thank the reviewers who contributed to improving each manuscript, including this preface, through their rigorous attention to detail and expert advice freely given.