Pollinators: a brief overview

From an evolutionary perspective, pollinators are a driving force behind most pollination processes on our planet. Angiosperms evolved the incredible variety of flower morphologies we appreciate, also thanks to the inputs of pollinators (Van der Niet and Johnson, Reference Van der Niet and Johnson2012). Pollinators may be as diverse as a bee from a bat: however, they all play the fundamental role of providing the pollination service, i.e., transferring pollen from one flower to another and allowing the production of fruits and seeds. Co-evolution is the process that depicted the present networks of plant–pollinator interactions: given flowers visited by a given guild of pollinators. Both, the plants and the pollinators, also evolved functional traits especially developed to strengthen the relationship (Faegri and Van der Pijl, Reference Faegri and Van der Pijl1971). For example, papilionaceous flowers (as those of black locust and peas) developed a mechanism that the insect visitor needs to trig to reach the nectar at the base of the corolla, and mechanisms can be as complex as the lever one found in the sages, Lamiaceae (Claßen-Bockhoff et al., Reference Claßen-Bockhoff, Speck, Tweraser, Wester, Thimm and Reith2004). Not all pollinators have the necessary strength or morphology to pay a visit to these flowers; however, adaptative behaviors may help individuals in overcoming physical barriers posed by the plants (Aronne et al., Reference Aronne, Giovanetti and De Micco2012; Giovanetti, Reference Giovanetti2019). While some pollinators may adapt to visit and get resources even from plants and flowers they did not co-evolve with (Giuliani et al., Reference Giuliani, Giovanetti, Foggi and Mariotti Lippi2016), others are seriously limited by the evolution of an extreme specialization: i.e., some pollinators are linked to few flowering species and may become rare when these are unavailable. Bosch et al. (Reference Bosch, Martín González, Rodrigo and Navarro2009) underlined the essential contribution of depicting the floral specialization of rare species to better understand the structure underneath pollination networks and to design proper conservation measures to contrast biodiversity loss.

We are facing mounting evidence of the decline of pollinators, widely reported in the scientific literature (reviewed in Cane and Tepedino Reference Cane and Tepedino2001; Kluser and Peduzzi, Reference Kluser and Peduzzi2007). This decline is alarming at the global level and does not refer only to the potential loss of biodiversity. The decline of pollinators brings within wide economic losses that will hurt the market of important products, especially fruits, vegetables and stimulants. Gallai et al. (Reference Gallai, Salles, Settele and Vaissière2009) investigated crops used for human food based on FAO categories and found that, out of 89 direct crops and 11 commodities, almost half of them (n = 46) were dependent on pollinators. For six of them, insect pollinators were essential, while pollinator contribution varied for the others: it was great for 13 crops, modest for 13 and little for 14, with the most pollinator-dependent crop categories being vegetables, fruits and edible oil crops. Interestingly, these categories are also the ones with the highest value per ton produced. Therefore, we need to address the issue of pollinator decline and provide measures of conservation to prevent heavy negative consequences (a) on biodiversity and the natural world, and (b) on the economy and health of mankind.

Where to start? Somehow obviously, by identifying the causes behind the decline. It has been a long debate deeply addressed back in 2001 in a special issue of the journal ‘Ecology and Society’ (https://www.ecologyandsociety.org/issues/view.php?sf=7). Various causes have been pointed out in the last decades: habitat fragmentation, agricultural practices and use of pesticides, lack of floral diversity, competition from non-native species, diseases and pathogens spread and recently even climate change. Most of them lead back to agroecosystems, and the intensive cultivation approach often preferred: securing food safety and global competition are often the main reasons called to justify this agricultural model. Actually, some literature sustains the need of conventional agriculture to ensure food availability and farmers’ income. For example, in its review Alvarez (Reference Alvarez2022) report a generalized reduction in yields obtained through organic management (an average gap of 25%), even if the reduction changes accordingly to the type of crop considered. The author also indicated the importance of considering productivity, often generating a gap greater than that of the yield. However, despite a higher yield per hectare, sales price of the product may be lower, at least for some food products where quality can be directly perceived by the consumer. Crowder and Reganold (Reference Crowder and Reganold2015) investigated the performance of conventional and organic farming, reviewing studies covering 55 crops grown on five continents: they highlighted that organic agriculture was significantly more profitable than conventional one. Similar conclusions were reached by the meta-analysis of Sánchez et al. (Reference Sánchez, Kamau, Grazioli and Jones2022): according to them, diversified farming systems are at least as profitable as simplified ones and may contribute to employment opportunities, sustainable food production, biodiversity conservation and climate mitigation. Moreover, we also know about the global problem of food waste: FAO (2011) reported approximately a third of all food produced for human consumption as lost or wasted. Possibly we are on the way to be able to modify the current conventional agricultural model maintaining satisfactory food production and farm competition. For such a change, different stakeholders need to interact: farmers and consumers in the first place. Farmers’ perception of major environmental problems and problems with animal welfare was found to be contrasting between organic farmers and consumers vs conventional farmers in Norway (Storstad and Bjørkhaug, Reference Storstad and Bjørkhaug2003). Farming decisions can also be strongly impacted by country-level decisions on investments (Azam and Shaheen, Reference Azam and Shaheen2019). Consumers may have a greater willingness to pay for organic products, with respect to conventional ones: greater market appreciation can counteract a lower yield by increasing sale price, as was the case of lemon production in the South of Italy analyzed by Sgroi et al. (Reference Sgroi, Candela, Di Trapani, Foderà, Squatrito, Testa and Tudisca2015). In a near future, consumer attitudes may also be sustained by younger generations, more sensitive to dietary quality (Pelletier et al., Reference Pelletier, Laska, Neumark-Sztainer and Story2013) and sustainable production.

Agroecosystems deeply influence the environment and its content, in terms of the variety and distribution of floral resources. Not only the resources, actually: the structure of the environment itself has been modified, reducing the presence of suitable nesting sites and widening the areas that a pollinator should travel in search of food. Pollinators may have a hard time reproducing in such hostile surroundings. Moreover, the environment is becoming poisonous due to the spread of chemicals. Phytosanitary products have been introduced to reduce the pests on crops or increase soil fertility and productivity; however, their design often resulted highly toxic for organisms other than the target ones. Among all, neonicotinoids have certainly been the most dangerous in recent decades (Singla et al., Reference Singla, Barmota, Sahoo and Kang2021): these molecules can act in synergy with each other or with other stress factors in determining the decline of pollinators (Goulson et al., Reference Goulson, Nicholls, Botías and Rotheray2015; Azpiazu et al., Reference Azpiazu, Bosch, Bortolotti, Medrzycki, Teper, Molowny-Horas and Sgolastra2021). Consumers express concerns about potential residues of pesticides in their food, even if some recognition is paid to beneficial contributions to food security and the national economy, and this situation did not change in the last 30 years (Dunlap and Beus, Reference Dunlap and Beus1992; Simoglou and Roditakis, Reference Simoglou and Roditakis2022). Ad hoc and holistic crop protection strategies that keep parasitic disease damage under control, do not harm pollinators, respect the environment and are socio-economically sustainable should be implemented.

Europe: the pollinator perspective

In Europe, pollinators have been supported by different types of actions, such as project funding, legislation and protection measures, developed under subsequent Framework Programmes (Fig. 1a). The scientific community was supported through research funds to better understand biodiversity loss, as in the project ALARM (Assessing Large-Scale Environmental Risks For Biodiversity), under the 6th Framework Programme. In the following 7th Framework Programme, researchers’ efforts concentrated directly on pollinator decline in the project STEP (Status and Trends of European Pollinators). This project contributed to the publication of the first ‘European Red List’ (Nieto et al., Reference Nieto, Roberts, Kemp, Rasmont, Kuhlmann, García Criado, Biesmeijer, Bogusch, Dathe, De la Rúa, De Meulemeester, Dehon, Dewulf, Ortiz-Sánchez, Lhomme, Pauly, Potts, Praz, Quaranta, Radchenko, Scheuchl, Smit, Straka, Terzo, Tomozii, Window and Michez2014), which recaps results for 1965 of Europe's native species of bees and points out the extinction risk of 9.2% of them. Research results helped in highlighting that threatened species suffer from agriculture intensification often linked to practices that include the use of pesticides and fertilizers, land and soil use related to urban development, the increased frequency of fires and climate change. Out of funds for research projects, the EU also contributed, even if indirectly, through protection measures for biodiversity (Directive 79/409/EEC for Bird protection and Directive 92/43/EEC for Habitat protection). These play a major role in targeting species and sites at risk and in need of direct actions of protection: pollinators are not a direct subject of these measures but may benefit from their application. So far protection measures were therefore mostly indirect; some measures that focused on protection/creation of beneficial habitats (by providing food resources or controlling invasive alien species) were considered a valid, almost direct contribution to pollinator protection. Alternatively, the few direct measures only referred to a single pollinator species, the managed honeybee. An example of such direct measures is the legislation on the employment of pesticides: acknowledgements related to their effects on the honeybees were included in Directive 91/414/EEC and the following Regulation (EC) No 1107/2009, and finally build up the Bee Guidance published by the European Food Safety Authority (EFSA Reference EFSA2013). The latter is currently under implementation, with ongoing meetings, technical reports and public consultations, including on bees other than the honeybee (e.g., bumblebees and wild bees Auteri et al., Reference Auteri, Arce, Ingels, Marchesi, Neri, Rundlöf and Wassenberg2022).

Figure 1. European temporal paths of documents and expression of interest from different stakeholders on the topic of pollinators or other topics possibly related to them (i.e., biodiversity). Documents cited were selected based on relevance. (a) Baseline made of legislation, project funding and conservation actions before 2018; (b) 2018 results of public consultation (on the left) as an impulse to move forward: the European Pollinator Initiative; (c) 2019: new documents (EU Green Deal, Farm to Fork) that deals (also) with the environmental protection and biodiversity with possible fallouts on pollinators, plus spontaneous citizens’ interest in pollinators and farming practice evolution; (d) 2020: the EU Biodiversity Strategy and EU Pollinator Monitoring in member states; awaiting the new CAP-post 2020 implementations.

In recent years, we faced numerous initiatives toward pollinators (and biodiversity). Citizens are often involved to express their opinion, also when the initiative comes from a governmental level. First, we need to acknowledge the public perception of pollinators’ importance and threats (Fig. 1b). The year 2018 is the recent milestone in acknowledging pollinators, with the public consultation associated with the EU Pollinators Initiative (COM/2018/395). Out of this consultation, nine out of ten respondents marked the reported decline of pollinators as alarming. The EU Pollinators Initiative, a framework with ten actions and 31 sub-actions, was intended to tackle the decline of pollinators. It was deeply discussed and recently prompted a revision, that started by going back to asking citizens’ opinions through a new running questionnaire (https://ec.europa.eu/info/law/better-regulation/have-your-say/initiatives/13142-EU-pollinators-initiative-revision/public-consultation_en). Again, even in this second public consultation, 91% of respondents indicated as very urgent to protect pollinators in the EU and added a negative perception of how the loss of pollinator habitats in agricultural areas is tackled. Even worst the perception of MS policies: 91% of respondents are convinced that their country does not at all address the decline of pollinators, or at least not well. Initiatives may move in different directions (objectives, documents, campaigns) and from different baselines (citizens, MSs, The European Parliament; Fig. 1c). An example of an initiative that was started by citizens is ‘Save bees and farmers! Towards a bee-friendly agriculture for a healthy environment’. It is promoting a campaign intending to protect bees and people's health, by discharging synthetic pesticides by 2035, restoring biodiversity and supporting farmers. This initiative is challenging considering that the first two objectives will need to be attained along a transition period, with farmers as the active component.

Governmental initiatives can be taken at the European or national level. The EU is widening its targets with important strategic documents: the EU Green Deal (COM/2019/640) to reduce greenhouse gas emissions by at least 55% by 2030, with the horizontal topic of the Farm To Fork strategy for an environment-friendly food system. Both the above-mentioned documents involve a goal to reverse the loss of biodiversity, but this has been implemented by the document EU Biodiversity strategy (COM/2011/0244), a long-term plan to protect nature and reverse the degradation of ecosystems (Fig. 1d). Directly related to pollinators, the EU is sustaining the proposal for a European Pollinator Monitoring Scheme (EUPoMS), inspired by the national UK PoMS. In May 2021, the SPRING project (Strengthening Pollinator Recovery Through Indicators and Monitoring) started to build recommendations for the future EUPoMS. Generally, the EU MSs behave as participatory units that may act independently or associated. For SPRING, Europe has been divided into seven biogeographical zones. However, monitoring can be carried out also at the national level, through national monitoring plans: in Italy, that is the case of the Italian BeeNet (Giovanetti and Bortolotti, Reference Giovanetti and Bortolotti2021), fostered by the Ministry of Agriculture, Food Sovereignty and Forestry through the National Rural Network. Monitoring projects, at any landscape level, are exploding worldwide (Giovanetti et al., Reference Giovanetti, Albertazzi, Flaminio, Ranalli, Bortolotti and Quaranta2021), dedicated to given pollinators (butterflies, bees, syrphid flies, honeybees) or all of them as a group, to given environments (agroecosystems, parks and urban contexts included), or individual plant species (cultivated and spontaneous). While it is certainly very important to raise awareness among citizens (i.e., through the citizens’ science approach applied to pollinators monitoring), still, above all actions that the EU and MSs will foster, those of major and sudden impact on pollinators’ conservation are related to changes in agricultural practices.

Actions on agroecosystems: the future to be expected

Agroecosystems should be evaluated for the resilience that the applied management brings within, possibly by introducing indicators of performance (Cabell and Oelofse, Reference Cabell and Oelofse2012). The indicators should span from an ecologically oriented perspective (e.g., spatial and temporal heterogeneity; local natural capitals) to a social- (e.g., learning; legacy) and economic-one (e.g., reasonably profitable). It is expected that an approach combining ecological–social–economic orientations may need to be sustained by a different set of laws and measures. Even if being intrinsically based on totally different characteristics, an ecological–social–economic orientation will ensure wider participation in changes to be applied. A very ambitious objective that in the European Community was supposedly addressed by the CAP.

The CAP has been introduced long ago; notwithstanding it undertook numerous reforms, its main effort finally translates into an agricultural funding policy (Pe'er et al., Reference Pe'er, Bonn, Bruelheide, Dieker, Eisenhauer, Feindt, Hagedorn, Hansjürgens, Herzon, Lomba, Marquard, Moreira, Nitsch, Oppermann, Perino, Röder, Schleyer, Schindler, Wolf, Zinngrebe, Lakner and Gaston2020). Unfortunately, agricultural intensification and industrialization are key drivers of biodiversity decline and ecosystem services loss (IPBES 2019): on the one hand, conventional agriculture improved cropping efficiency, herbicide use and fertilizer use; on the other hand, we faced an abandonment of traditional agricultural land uses, including grazing and mowing. The last CAP (2014–2020) had already renewed the approach toward a more sustainable agriculture, by incorporating obligatory measures to support environment-friendly practices. These were compiled along two main pillars and included the cross-compliance, obligatory for farmers to comply with high EU standards for public, plant and animal health and welfare; the greening payment scheme, still obligatory, contributing to about 30% of direct payments, and including ploughing, permanent pasture, crop diversification and ecological focus areas; finally, the optional agri–environment–climate measures. These schemes were not directly involving pollinators, but as mentioned above they could have counterbalanced pollinators’ decline by acting at the local environmental level. However, ‘greening’, possibly the most interesting to sustain pollinators, resulted mainly ineffective even if obligatory (Pe'er et al., Reference Pe'er, Zinngrebe, Moreira, Sirami, Schindler, Müller, Bontzorlos, Clough, Bezák, Bonn, Hansjürgens, Lomba, Möckel, Passoni, Schleyer, Schmidt and Lakner2019). The European Court of Auditors (ECA) (2020) examined the progress in the protection of wild pollinators after the Commission Initiatives, finding so far that actions delivered on biodiversity conservation, agriculture and the use of pesticides (the only measurable units) did not halt the decline. Cole et al. (Reference Cole, Kleijn, Dicks, Stout, Potts, Albrecht and Scheper2020) and Mottershead and Underwood (Reference Mottershead and Underwood2020) resumed similar findings: when considering especially pollinators, CAP 2014–2020 measures did not result effectively. An important reason behind this is the absence of direct actions or measures to protect pollinators and the absence of high-level strategic importance given to wild pollinators. Mottershead and Underwood (Reference Mottershead and Underwood2020) reported no overt or limited mention of wild pollinators, or strongly geared toward biodiversity, in RDPs funding options, this way missing a crucial strategic overview in five out of six case-studies. Not always the faults at the institutional level are replicated downscale: in some of the same case-studies, authors found evidence of advice available to farmers, even focusing on pollinators in general or bees. Unfortunately, these favorable conditions were not replicated in the entire MS, when dealing at the regional scale. Other reasons that may have partly contributed to the failure in pollinators’ enhancement and protection along the CAP may be an unbalanced distribution of incentives, a missing effort in pressing farmers’ engagement, and poor monitoring and evaluation procedures. Since farmers can choose low-demanding options, greening does not trigger any substantial change in farming practices. A shortcoming of active promotion of the importance of change in agricultural practices is especially evident in studies that highlight success when applying communication tools more adequate to the farmers’ audience: cooperation and social learning, social networks and agriculture-related organizations, technical advice or extension services, farming press news (Defrancesco et al., Reference Defrancesco, Gatto, Runge and Trestini2008; Niens and Marggraf, Reference Niens and Marggraf2010, Pascucci et al., Reference Pascucci, Capitanio, Adinolfi and De Magistris2011, Dedeurwaerdere et al., Reference Dedeurwaerdere, Polard and Melindi-Ghidi2015).

A new CAP is on its way: CAP post-2020. The European Commission proposed the document in June 2018 (EC, 2018), acknowledging the urgency to address environmental and sustainability challenges. The absence of a substantial variation in agricultural practices induced to modification of the structure of the previous CAP. In the new one, cross-compliance is expected to be enlarged and reinforced: to obtain direct payments, farmers need to apply more stringent rules. Greening measures have been integrated into the eco-schemes, together with agri–environment–climate measures, and payments for them can be added up. Ideally, the combination may push the adoption of more schemes by individual farmers, fostering a real change at the local landscape context. The document also suggests the introduction of a new Green Architecture by proposing a model that offers MSs higher flexibility inside their boundaries. MSs are invited to present their list of priorities in the form of eco-schemes; therefore, the EC encourages a view that includes local peculiarities following local stakeholders’ groups. This is a great opportunity to foster pollinator protection. In Italy, this opportunity is acknowledged by the eco-schemes proposed to the European Commission and included an eco-scheme on pollinators (national refs: Articolo 21; DM 23 dicembre 2022, n. 660087). Four out of five eco-schemes do include changes in agricultural practice that may sustain pollinators and predicted to be coupled with the eco-scheme on pollinators. For the eco-scheme specific for pollinators, farmers will commit to the cultivation of non-productive crops reach in nectar and/or pollen resources in arable land or in the inter-row of permanent crops, including a commitment not to use herbicides and other phytosanitary products in the field and the borders in the year of engagement. Another eco-scheme refers to the grassing of tree crops: in this case, the contribution toward pollinator protection will be achieved by selecting a proper floral mixture or legumes as grassing method. Rotation of legumes and fodder crops is expected also in another eco-scheme: therefore, again food for bees. Finally, a very special eco-scheme is that related to olive grows, in which the list of commitments already includes the ones related to the eco-scheme on pollinators.