Insect pollinators provide vital ecosystem services through its maintenance of plant biological diversity and its role in food production. Indeed, adequate pollination services can increase the production and quality of fruit and vegetable crops. This service is currently challenged by land use intensification and expanding human population growth. Hence, this study aims: (1) to assess the pollination services in different land uses with different levels of disturbance through GIS mapping technique using insect pollinators abundance and richness as indicators, and (2) estimate the economic value of pollination by insects in agricultural crops. Our study takes place in a small oceanic island, Terceira (Azores, Portugal). Our results showed, remarkably, that not only the pristine vegetation areas, but also the orchards and agricultural areas have relatively high values of pollination services, even though both land uses have opposite disturbance levels. For the economic valuation, we analyzed 24 crops in the island and found that 18 depend on pollinators with one-third of these crops having 65% or 95% dependence on pollinators. The economic contribution of pollinators totals 36.2% of the total mean annual agricultural income of the dependent crops, highlighting the importance of insect pollinators in agricultural production and consequent economic gain productions.

Ecosystem service, GIS, pollination, insects, agriculture, economic value

Research at the interface of ecology and economics to characterize, value, and manage ecosystem services (henceforth ES) has supported a paradigm shift in how society thinks about biodiversity, ecosystems and human relationships to them (MEA 2005; TEEB 2010; Garbach et al. 2014). This awareness of the ES started with classical papers of Daily (1997) and Constanza et al. (1997); and in 2005, the Millennium Ecosystem Assessment (MEA) promoted and defined the concept of ES as “the benefits that humans recognize as obtained from ecosystems that support, directly or indirectly, their survival and quality of life”. MEA suggests to group ES into four categories: (1) provisioning services, such as food, water, timber, and fiber; (2) regulating services that affect climate, floods, disease, wastes, and water quality; (3) cultural services that provide recreational, aesthetic, and spiritual benefits; and (4) supporting services such as soil formation, photosynthesis, and nutrient cycling (MEA 2005).

The valuation and mapping of ES constitutes a continuous and very complex work for several national governments and organizations, and this process is only currently available for few countries (e.g. Portugal, Pereira et al. 2009; UK, Maresca et al. 2011; France, Watson et al. 2011). ES assessment aims usually to estimate of the marginal values of these services to inform decisions and to evaluate how trade-offs in ES provision will affect human well-being. Therefore, researchers are interested in developing methods for quantifying the provision and value of ES so this information can be incorporated into mapping, planning and decision-making at different scales and in different public and private sectors (see e.g., Losey and Vaughan 2006; Allsopp et al. 2008; Gallai et al. 2009; Nelson et al. 2009; Tallis and Pollaski 2009; Villa et al. 2009; Maes et al. 2012; Nemec and Raudsepp-Hearne 2013; Nahuelhual et al. 2013; 2015).

Pollination together with seed dispersal is considered as one of the key ES, classified by the Common International Classification of Ecosystem Services (CICES) coding system (Haines-Young and Potschin 2013) as a “Regulation & Maintenance ES” with the code 2.3.1.1. Among other studies, Klein et al. (2007), Aizen et al. (2009), Gallai et al. (2009), Calderone (2012) and Giannini et al. (2015) show that pollination services contribute significantly to the agricultural production and subsequently assures 75% of food production worldwide (Klein et al. 2007) (as well as to other flowering plants) by ensuring plant reproduction, fruit set development and dispersion (e.g. Ollerton et al. 2011; Altieri et al., 2015). Notably, the pollination of some vegetable crops (e.g. cabbage and other brassicas, carrots, turnips, lettuce, chicory and onions) increases the quality of the seed production (Gallai and Vassière 2009). In addition, insect pollinators enhance fruit and seed quality (Garibaldi et al 2013; Bartomeus et al 2014; Garratt et al. 2014; Marini et al. 2015; Saeed et al. 2016) and reinforces pest management (Cross et al. 2015) which constitutes an indirect and difficult benefit to measure, but extremely important for the agricultural market. Also, a recent study on pollination by wild insect pollinators has showed their capacity to increase the seed production in 41 agricultural systems globally, regardless of the abundance of honey bees (Garibaldi et al. 2013). Additionally, it was also documented that wild insect pollinators can buffer the impact of climate change on crop production (Rader et al. 2013), most likely due to their high biological diversity that can in turn stabilize ES against habitat disturbances (Cardinale et al. 2012).

Besides these findings, there is also a general consensus that native pollinators abundance and richness are declining throughout the world (Ghazoul 2005; Biesmeijer et al. 2006; Winfree et al. 2009). This global decline has sparked the formation of a global policy framework for pollinators, primarily through the International Pollinator Initiative within the Convention of Biological Diversity (CBD) and several other programs (e.g. Food and Agricultural Organization (FAO) Global Action on Pollination Services for Sustainable Agriculture; Bee Life European Beekeeping Coordination). All of these initiatives emphasize the need to assess and monitor the pollinators in different regions in order to better plan their conservation, restoration and to preserve the ES they supply for humans.

The Intergovernmental Platform on Biodiversity and Ecosystem Services (IPBES) from United Nations Environment Programme (UNEP; Zisenis 2015; Schmeller and Bridgewater 2016) was recently created as a Knowledge-Policy interface (Díaz et al. 2015; Schmeller and Bridgewater 2016). In the fourth plenary of IPBES (IPBES-4) the agenda’s item 5 (work programme of the Platform) included the development of works towards the approval of the thematic assessment on pollinators, pollination and food production (“Deliverable 3a” - see http://www.ipbes.net/workprogramme/pollination). This “Deliverable 3a” highlighted substantial knowledge gaps in different regions on the status and trend of pollinators and pollination, making the global assessment of insect pollinators (henceforth IP) not possible due to lack of data, although regional and national assessments indicated that more than 40 % of insect pollinators are threatened locally (Schmeller and Bridgewater 2016).

These knowledge gaps unveil how the interactions between plants and insects are numerous and complex. So, the understanding of how plant-insect species’ interactions affect ecological functions and are affected by land management (Kremen et al. 2007) is central to maintain and enhance associated ES. As a vital and increasingly threatened ES, pollination (Klein et al. 2007; Potts et al. 2010) has become an often-cited example of how the ES are economically valuable (Hanley et al., 2015). Two additional recent examples of studies about ES pollination in Europe (EU) that complement each other are from Leonhardt et al. (2013) and Schulp et al. (2014), both showing results that provide an overview of ES importance, variation and influence throughout European regions.

In this work, we assess the ES provision and values provided by insect pollinators in the Azores archipelagic region (Portugal) where few studies on ES assessment (e.g. Cruz et al. 2011; Mendonça et al. 2013; Vergílio et al 2016) or related to pollination and seed dispersal services have been undertaken (e.g. Pereira 2008; Heleno et al. 2009; Olesen et al. 2002, 2012). We use a database on the spatial distribution of insect pollination in Terceira Island (Azores) recently collected (Picanço et al. 2017) to provide the first insight of the bees and other IP contribution to the pollination services and for assessing pollination-related ES in a small oceanic island. With this purpose, we applied two types of methodological approaches: (1) mapping pollination services with geographic information systems (GIS; e.g. Nemec and Raudsepp 2013) using bees and other IP abundance and richness numerical values as indicators; and (2) economic valuation - through the production function approach - by using crops production estimates and crops dependence ratio (Klein et al. 2007; Gallai and Vassière 2009; Hanley et al. 2015). Our goals were to determine: (I) the spatial variations of the pollination services; (II) whether the variations of the pollination services were influenced by the different land-uses and/or level of disturbance; (III) the number of crops for which production has a certain level of dependence on IP (or vulnerability ratio); and (IV) estimation of the island’s IP economic value.

Under the same thematic as “Deliverable 3a” from IPBES (Schmeller and Bridgewater 2016) – i.e., assessment of the contribution of insect pollinators to the pollination and food production - our findings highlight the great importance of insect pollinators on a small oceanic island economy. Our results are relevant since they are based both in field and economic data with the aim of providing quantitative information as in Leonhardt et al. (2013) and Schulp et al. (2014), but by using a completely different approach to evaluate insect pollinators distribution in comparison to Londorsf et al. (2009) and Polce et al. (2013), which have used other biological indicators and modeling techniques. Concerning the field‐based mapping of pollination-related ES, similar spatial patterns were revealed for both bees and overall insect pollinators (IP): (i) high values of abundance (N) and/or species richness (S) are directly associated to the pristine native forest areas with lower disturbance (D), on one side with low percentage of island area covered (Tables 2–5); and (ii) on the other side these same high values of pollination services are also observed in orchards and agricultural areas with high level of disturbance (D) covering large island areas (Tables 2–5). These results show that Azorean native pollinators (e.g. Pierisbrassicaeazorensis, Anaspisproteus, Lasioglossum spp., Eupeodescorollae, Stomorhinalunata - see Suppl. material 1: Table S1) are providing key pollination services not only in native habitats for which they are originally adapted, but also in low altitude agro-ecosystems in which they expended their range. This finding call for the need of a whole island integrated management strategy for pollinators in Terceira in order to decrease the 32.6% VR of crops production. However, intensive managed pastures, the most dominant land use in the island with highest disturbance index D (see classes 8 and 12 in Tables 2–5), showed low abundance (N) and/or richness (S) classes for both bees and IP (Fig. 3), evidencing therefore a low performance of pollination services, as observed in previous studies (e.g. Batary et al. 2010; Sjödin 2007). Indeed, this land-use, subject to frequent and intense grazing events does not foster the occurrence of abundant pollinator populations.

Based on the results obtained for low altitude agricultural areas, the disturbance index D variable, in contrast to other studies (e.g. Boieiro et al. 2013; Cardoso et al. 2013, 2014; Florencio et al., 2013), do not fully and adequately explain the spatial abundance of native pollinators in this island. Unmeasured variables associated to current and past land uses that reflect specific agro-ecosystems management regimes in Terceira Island may have driven the current spatial heterogeneity of the pollinators’ abundance and diversity. The numerous resources available for pollinators at low altitude (e.g. private gardens, abandoned orchards) together to a low input of pesticides in abandoned orchards are possibly fostering an ideal situation for the spread of native pollinators across the landscape (see also Picanço et al. 2017).

This study also highlights the fact that about one-third of Terceira Island crops have an essential or great dependence on pollinators, therefore complementing the above information on high values of insect pollinator abundance and richness in low altitude agro-ecosystems. The economic contribution of pollinators totalizes 36.2% (€170K) of the mean total annual agricultural income of the dependent crops (€469K). This EVIP percentage represents also the VR of agricultural production. Moreover, the consumer surplus loss was estimated between €156K and €231K based upon average price elasticities of −1.2 to −0.8 respectively. This interval of prices on the consumer surplus loss represents the difference between what island consumer are willing or able to pay for the ES relatively to its market price, in case of pollination services loss. These values referred to Frutercoop production only represents 54% of the island’s total crop productions (Tables 6 and 7). However, the presented estimates are underestimated values, since not all agricultural production is officially declared (family production, production in backyards, urban gardens, etc.).

Our study also indicates the high socioeconomic relevance of pollination-related ES in a small oceanic islands’ context. Nevertheless, bio-economics based valuation studies have been inherently and generally unable to provide thorough and consistent results, due to frequent changes in currency values, labor costs and food prices. This type of approach has also failed to consider and propose realistic and cost-effective mitigation efforts that might reduce the impact of a pollination crisis. In general, the costs are still being strongly dependent on the local agro-ecological setting, namely the crops phenology, the local insect populations, and the existing ecological relationships between farmland and surrounding natural or semi-natural areas.

Some crops, despite their modest or little dependence, showed very high values of mean annual production and, therefore, even in these cases, the contribution of pollinators is significant (Gallai and Vassière 2009; Tables 6 and 7). Moreover, there is no available information on pollinator dependence for some relevant crops, showing the urgent need to address this issue through basic research on reproductive biology and pollination ecology.

As a result, these pollinator-dependent crops are crucial for maintaining the agricultural food balance of the increasing population-growth of Terceira Island’s consumers. Meanwhile, at the world scale, IP are becoming increasingly more vulnerable to (i) land-use intensification (Power et al. 2012); (ii) use of pesticides (Kevan 1999; Suchail et al. 2001; Dos Santos et al. 2016; Geslin et al. 2016); (iii) use of insecticides (Sánchez-Bayo et al. 2016; Straub et al. 2016); (iv) use of fertilizers (McLaughlin and Mineau 1995; Andersson et al. 2014); (v) cultivation of some genetically modified crops (Warwick et al. 2009); (vi) occurrence of biological invasions (Campbell et al. 2015); (vii) climate change (Gill et al. 2016; Ferreira et al 2016); and (viii) the interactions of these ecological stressors (Potts et al. 2010; Vanbergen 2013). Nevertheless, it seems that intensive pastures aside, IP populations in Terceira Island are abundant and diverse in several agro-ecosystems (Fig. 3), and performing adequate pollination services to crops.

With the expected need for an increased production of vegetables and fruit in Terceira Island in the coming years, integrated mitigation measures (e.g. biological pest control, wild flowering plants production areas, promotion of organic farming), as well as (cost-) effective, innovative and attractive (for farmers) agri-environmental schemes are required in order to adequately promote pollination services and to compensate for some eventual crops’ failing production (e.g. Wilson and Hart 2001; Power et al 2012; Andersson et al. 2014). It appears to be increasingly consensual that organic farming regimes benefit biodiversity, zoophilous wildflowers and IP abundance on a local scale (Gabriel and Tscharntke 2007). As such, if strategically and effectively promoted and applied, this management practice may have the potential to benefit crop pollination and to increase IP abundance across the whole island. This needs to be taken into account for the sustainable long-term management and conservation of pollinator communities and insect-pollinated plants in Terceira Island (e.g. Power et al. 2012).

Agri-environmental schemes aiming to foster and to pay/compensate farmers for a more sustainable management of low-intensity pasture systems and to implement integrated farm management and organic agriculture practices should be especially encouraged in the north-western, eastern and south-eastern agro-ecosystem areas of Terceira Island.

Finally, this broad, straightforward and cost-effective methodological approach may be able to be applied in further small oceanic islands with the aim of improving the capacity of effectively assessing and monitoring pollination-related ecosystem services, in order to improve the existing decision support systems for land use planning/management policies, especially those related to agriculture and nature conservation.

We would like to thank the reviewers Nicolai Gallai and Natacha Chacoff for their useful comments on the manuscript. AP was supported by a Ph.D. grant from Direção Regional da Ciência e Tecnologia dos Açores (M3.1.2/F/031/2011). FR was supported by the Post-Doc Grant FCT – PTDC/BIA-BIC/119255/2010 and AG was supported by the Post-Doc Grant FCT – SFRH/BPD/100017/2014, funded by the National Budget of the Ministry of Education and Science of Portugal and by the European Social Fund. PB and AG were partly financed by the Project CSA-SEP-210140185-ESMERALDA. We would like also to acknowledge FRUTER/Frutercoop and Serviço de Desenvolvimento Agrário da Ilha Terceira for giving information related to crop production.