Pollination Ecosystem Services Research Articles

Insect pollinators boost the market price of culturally important crops: holly, mistletoe and the spirit of Christmas

Animal pollination is a vital ecological process in both natural and agricultural ecosystems. Economic valuation studies have demonstrated that pollination services may underpin a significant proportion of global crop market outputs. However these assessments are probably under-estimates because they have rarely included non-food crops, for which very few data are currently available. In particular, culturally symbolic plants have received no attention. Here we show that pollinators have considerable economic benefits to sales of European holly and mistletoe, two seasonal cultural crops that are almost wholly dependent upon insect pollinators for the production of ornamental berries. Analyses of a time series of auction records spanning 11 years indicates that wholesale prices paid for holly with berries are twice those paid for the crop without berries, whilst mistletoe with berries sells for almost three times the price of the crop lacking fruit. The benefits of this insect pollination ecosystem service to this market are therefore considerable. These findings demonstrate that pollinators can play a significant role in adding value to crops that provide resources other than food. In the future such crops should be included in assessments of regional and global value of animal pollination to increase the accuracy of assessments of the value of pollination as an ecosystem service. Our results also support arguments for continued efforts to conserve pollinator diversity and abundance in agro-ecological systems, not least for their contribution as providers of ecosystem services.

Insect pollinators boost the market price of culturally important crops: holly, mistletoe and the spirit of Christmas

Animal pollination is a vital ecological process in both natural and agricultural ecosystems. Economic valuation studies have demonstrated that pollination services may underpin a significant proportion of global crop market outputs. However these assessments are probably under-estimates because they have rarely included non-food crops, for which very few data are currently available. In particular, culturally symbolic plants have received no attention. Here we show that pollinators have considerable economic benefits to sales of European holly and mistletoe, two seasonal cultural crops that are almost wholly dependent upon insect pollinators for the production of ornamental berries. Analyses of a time series of auction records spanning 11 years indicates that wholesale prices paid for holly with berries are twice those paid for the crop without berries, whilst mistletoe with berries sells for almost three times the price of the crop lacking fruit. The benefits of this insect pollination ecosystem service to this market are therefore considerable. These findings demonstrate that pollinators can play a significant role in adding value to crops that provide resources other than food. In the future such crops should be included in assessments of regional and global value of animal pollination to increase the accuracy of assessments of the value of pollination as an ecosystem service. Our results also support arguments for continued efforts to conserve pollinator diversity and abundance in agro-ecological systems, not least for their contribution as providers of ecosystem services.

Bumblebees in the city: abundance, species richness and diversity in two urban habitats

Bumblebees are well known for their contribution to the ecosystem service of pollination. In urban areas, green space management beneficial to pollinators can be an important step in sustaining large urban bee populations. The abundance, number of species and diversity of bumblebees (Bombus spp), as well as the abundance of honeybees (Apis mellifera), were studied in 13 urban gardens (including allotments) and 13 ornamental flowerbeds (in parks and green spaces) in the city centre of Gothenburg, Sweden. In total, 12 species of bumblebees were observed. Species richness was significantly higher in gardens than in flowerbeds, but diversity (Berger–Parker and Simpson indices) was higher in flowerbeds than in urban gardens. The abundance in gardens was significantly higher and approximately twice that found in flowerbeds. The number of honeybee individuals was positively correlated with the abundance of bumblebees. Neither species richness nor abundance of bumblebees was affected by site size. However, a high flowering frequency positively affected the total number of bumblebee and honeybee individuals at the sites. We conclude that urban gardens contribute to sustaining a high abundance of bumblebees in the city centre, and indirectly facilitates small scale urban food production. A pollinator-friendly management of urban green space with plentiful flowering may promote a community of bumblebees with high abundance and diversity.

Where is the value in valuing pollination ecosystem services to agriculture?

Current national and global scale monetary valuation of pollination services do not accurately estimate the contribution of wild pollinators to agricultural production. First, ecosystem (wild) pollination services remain largely bundled with those of managed pollinators. This problem is compounded by the fact that the dependency of crops on pollination, a key parameter used in current valuations, does not reflect variation in pollinator density, crop cultivars and growing conditions that exist in practice. Over half of the €153 billion of estimated global pollination service value in 2005 is based on estimates of pollinator dependency from crops with fewer than three field studies that measure actual levels of pollinator activity and corresponding fruit set. The resulting uncertainty may be most distorting when applied to widely-planted intensive oilseed crops. Furthermore, current valuations are underpinned by simplistic assumptions regarding the likelihood of pollinator decline and the impact on agricultural prices. Although efforts to motivate wild pollinator protection through their ecosystem service value remain highly circumscribed by conceptual and empirical limitations, we identify the need to go beyond technical solutions and develop a critical framework that could account for why pollinator conservation has come to be predominantly justified in these terms to begin with.

Pollination ecosystem services in South African agricultural systems

Insect pollinators, both managed and wild, have become a focus of global scientific, political and media attention because of their apparent decline and the perceived impact of this decline on crop production. Crop pollination by insects is an essential ecosystem service that increases the yield and quality of approximately 35% of crops worldwide. Pollinator declines are a consequence of multiple environmental pressures, e.g. habitat transformation and fragmentation, loss of floral resources, pesticides, pests and diseases, and climate change. Similar environmental pressures are faced in South Africa where there is a high demand for pollination services. In this paper, we synthesise data on the importance of different pollinators as a basis for services to South African crops and on the status of managed honeybees. We also focus on insect pollination services for the Western Cape deciduous fruit industry, which is worth ZAR9800 million per year and is heavily reliant on pollination services from managed honeybees. We discuss landscape and regional level floral resources needed to maintain sufficient numbers of managed honeybee colonies. In summary, the available literature shows a lack of data on diversity and abundance of crop pollinators, and a lack of long-term data to assess declines. We highlight key areas that require research in South Africa and emphasise the critical role of floral resource availability at the landscape and regional scale to sustain pollinators. We conclude that understanding the dynamics of how floral resources are used will help inform how landscapes could be better managed in order to provide long-term sustainable pollination services.

National patterns of functional diversity and redundancy in predatory ground beetles and bees associated with key UK arable crops

Summary Invertebrates supporting natural pest control and pollination ecosystem services are crucial to world‐wide crop production. Understanding national patterns in the spatial structure of natural pest control and pollination can be used to promote effective crop management and contribute to long‐term food security. We mapped the species richness and functional diversity of ground beetles and bees to provide surrogate measures of natural pest control and pollination for Great Britain. Functional diversity represents the value and range of morphological and behavioural traits that support ecosystem services. We modelled the rate at which functional diversity collapsed in response to species extinctions to provide an index of functional redundancy. Deficits in functional diversity for both pest control and pollination were found in areas of high arable crop production. Ground beetle functional redundancy was positively correlated with the landscape cover of semi‐natural habitats where extinctions were ordered by body size and dispersal ability. For bees, functional redundancy showed a weak positive correlation with semi‐natural habitat cover where species extinctions were ordered by feeding specialization. Synthesis and applications. Increasingly, evidence suggests that functionally diverse assemblages of ground beetles and bees may be a key element to strategies that aim to support pollination and natural pest control in crops. If deficits in both functional diversity and redundancy in areas of high crop production are to be reversed, then targeted implementation of agri‐environment schemes that establish semi‐natural habitat may provide a policy mechanism for supporting these ecosystem services.

Hedgerows surrounding organic apple orchards in north‐west Spain: potential to conserve beneficial insects

Abstract Flowering plant species in hedgerows may be food sources for beneficial insects and therefore play a role in biodiversity conservation and agroecosystem functioning. Research was conducted in eight organic cider‐apple orchards in Asturias (north‐west Spain) aiming to (i) identify the native flowering plants in the surrounding hedgerows and (ii) assess the attractiveness of those flowers for beneficial insects, such as pollinators and natural enemies of pests. A total of 7745 flowers belonging to 63 plant species were recorded in the hedgerows from May to September 2012. Flower abundance and species richness decreased as the season progressed. Orchard differences were observed for plant species richness but not for the total number of flowers in the hedgerows, likely as a result of similar management among orchards. Hymenoptera pollinators (honey bees, bumblebees and wild bees) accounted for 37.8% of the total insects recorded visiting flowers, whereas predatory hoverflies (14.9%) were the dominant natural enemies. The attractiveness for insects was assessed for 21 of the flowering plant species identified in the hedgerows. Flowering plants differed in the number of taxa that they attracted and in their attractiveness for particular insect groups and for insects as a whole. The present study described the floral composition of the hedgerows that surround apple orchards and identified the local floral resources that could provide benefits for farmers by improving ecosystem services of pollination and biological control of pests.

Microbial symbionts of honeybees: a promising tool to improve honeybee health

Among pollinators, honeybees are the most important ones and exert the essential key ecosystem service of pollination for many crops, fruit and wild plants. Indeed, several crops are strictly dependent on honeybee pollination. Since few decades, honeybees are facing large-scale losses worldwide, the causes of which are found in the interaction of several biotic and abiotic factors, such as the use of pesticides, the habitat loss, the spread of pathogens and parasites and the occurrence of climate changes. Insect symbionts are emerging as a potential tool to protect beneficial insects, ameliorating the innate immune homeostasis and contributing to the general insect wellbeing. A review about the microbial symbionts associated to honeybees is here presented. The importance of the honeybee microbial commensals for the maintenance and improvement of honeybee health is discussed. Several stressors like infestations of Varroa mites and the use of pesticides can contribute to the occurrence of dysbiosis phenomena, resulting in a perturbation of the microbiocenosis established in the honeybee body.

Organic Farming Improves Pollination Success in Strawberries

Pollination of insect pollinated crops has been found to be correlated to pollinator abundance and diversity. Since organic farming has the potential to mitigate negative effects of agricultural intensification on biodiversity, it may also benefit crop pollination, but direct evidence of this is scant. We evaluated the effect of organic farming on pollination of strawberry plants focusing on (1) if pollination success was higher on organic farms compared to conventional farms, and (2) if there was a time lag from conversion to organic farming until an effect was manifested. We found that pollination success and the proportion of fully pollinated berries were higher on organic compared to conventional farms and this difference was already evident 2–4 years after conversion to organic farming. Our results suggest that conversion to organic farming may rapidly increase pollination success and hence benefit the ecosystem service of crop pollination regarding both yield quantity and quality.

Effects of organic farming on biodiversity and ecosystem services: taking landscape complexity into account

The recent intensification of the arable landscape by modern agriculture has had negative effects on biodiversity. Organic farming has been introduced to mitigate negative effects, but is organic farming beneficial to biodiversity? In this review, we summarize recent research on the effects of organic farming on arable biodiversity of plants, arthropods, soil biota, birds, and mammals. The ecosystem services of pollination, biological control, seed predation, and decomposition are also included in this review. So far, organic farming seems to enhance the species richness and abundance of many common taxa, but its effects are often species specific and trait or context dependant. The landscape surrounding the focal field or farm also seems to be important. Landscape either enhances or reduces the positive effects of organic farming or acts via interactions where the surrounding landscape affects biodiversity or ecosystem services differently on organic and conventional farms. Finally, we discuss some of the potential mechanisms behind these results and how organic farming may develop in the future to increase its potential for sustaining biodiversity and associated ecosystem services.

Testing Pollen of Single and Stacked Insect-Resistant Bt-Maize on In vitro Reared Honey Bee Larvae

The ecologically and economic important honey bee (Apis mellifera) is a key non-target arthropod species in environmental risk assessment (ERA) of genetically modified (GM) crops. Honey bee larvae are directly exposed to transgenic products by the consumption of GM pollen. But most ERA studies only consider responses of adult bees, although Bt-proteins primarily affect the larval phases of target organisms. We adopted an in vitro larvae rearing system, to assess lethal and sublethal effects of Bt-pollen consumption in a standardized eco-toxicological bioassay. The effects of pollen from two Bt-maize cultivars, one expressing a single and the other a total of three Bt-proteins, on the survival and prepupae weight of honey bee larvae were analyzed. The control treatments included pollen from three non-transgenic maize varieties and of Heliconia rostrata. Three days old larvae were fed the realistic exposure dose of 2 mg pollen within the semi-artificial diet. The larvae were monitored over 120 h, until the prepupal stage, where larvae terminate feeding and growing. Neither single nor stacked Bt-maize pollen showed an adverse effect on larval survival and the prepupal weight. In contrast, feeding of H. rostrata pollen caused significant toxic effects. The results of this study indicate that pollen of the tested Bt-varieties does not harm the development of in vitro reared A. mellifera larvae. To sustain the ecosystem service of pollination, Bt-impact on A. mellifera should always be a crucial part of regulatory biosafety assessments. We suggest that our approach of feeding GM pollen on in vitro reared honey bee larvae is well suited of becoming a standard bioassay in regulatory risk assessments schemes of GM crops.

Changing Bee and Hoverfly Pollinator Assemblages along an Urban-Rural Gradient

BackgroundThe potential for reduced pollination ecosystem service due to global declines of bees and other pollinators is cause for considerable concern. Habitat degradation, destruction and fragmentation due to agricultural intensification have historically been the main causes of this pollinator decline. However, despite increasing and accelerating levels of global urbanization, very little research has investigated the effects of urbanization on pollinator assemblages. We assessed changes in the diversity, abundance and species composition of bee and hoverfly pollinator assemblages in urban, suburban, and rural sites across a UK city.Methodology/Principal FindingsBees and hoverflies were trapped and netted at 24 sites of similar habitat character (churchyards and cemeteries) that varied in position along a gradient of urbanization. Local habitat quality (altitude, shelter from wind, diversity and abundance of flowers), and the broader-scale degree of urbanization (e.g. percentage of built landscape and gardens within 100 m, 250 m, 500 m, 1 km, and 2.5 km of the site) were assessed for each study site. The diversity and abundance of pollinators were both significantly negatively associated with higher levels of urbanization. Assemblage composition changed along the urbanization gradient with some species positively associated with urban and suburban land-use, but more species negatively so. Pollinator assemblages were positively affected by good site habitat quality, in particular the availability of flowering plants.Conclusions/SignificanceOur results show that urban areas can support diverse pollinator assemblages, but that this capacity is strongly affected by local habitat quality. Nonetheless, in both urban and suburban areas of the city the assemblages had fewer individuals and lower diversity than similar rural habitats. The unique development histories of different urban areas, and the difficulty of assessing mobile pollinator assemblages in just part of their range, mean that complementary studies in different cities and urban habitats are required to discover if these findings are more widely applicable.

Honey bee risk assessment: new approaches for in vitro larvae rearing and data analyses

Summary1. To sustain the vital ecosystem service of pollination, new methodical developments are needed for research on the underlying factors of globally observed bee losses. In particular, robust laboratory methods for assessing adverse effects on honey bee brood are required. In addition, from a statistical point of view, the shared origin of test individuals must be considered when analysing ecotoxicological data.2. To improve honey bee in vitro rearing, we adopted a nongrafting method to collect honey bee larvae without direct manipulation. Linear mixed effects model to evaluate LD50, larvae survival and prepupae weights integrated the colony background of larvae as a random factor into the statistical analyses. The novel rearing approach and appropriate statistical tools for data analyses are illustrated in an in vitro case study on acute oral dimethoate toxicity.3. We recommend our honey bee larvae collection approach for in vitro larvae‐rearing applications, because of (i) a mere 3% background mortality upon the prepupae stage, (ii) a high quantitative capacity and (iii) because of robustness of performance which are great benefits for standardization.4. The analyses indicate clear adverse effects of dimethoate by a significant survival reduction and prepupae weight reduction. For second instars, the acute 48‐h LD50 was 1·67 μg dimethoate per larva.5. We conclude that both our larvae collection method and the applied statistical approaches will help to improve the quality of environmental risk assessment studies on honey bees, to secure honey bee pollination and to sustain biodiversity.

Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus)

The conservation genetics of bees is of particular interest because many bee species are in decline, so jeopardizing the essential ecosystem service of plant pollination that they provide. In addition, as social haplodiploids, inbred bees may be vulnerable to the extra genetic load represented by the production of sterile diploid males. Using microsatellite markers, we investigated the genetic structure of populations of the Great Yellow Bumblebee (Bombus distinguendus Morawitz) in the UK, where this species has undergone a precipitous decline. By means of a mixture of analytical methods and simulation, we also extended--and then applied--genetic methods for estimating foraging distance and nest density in wild bees. B. distinguendus populations were characterized by low expected heterozygosity and allelic richness, inbreeding coefficients not significantly different from zero, absence of detected diploid males, absence of substantial demographic bottlenecking, and population substructuring at large (c. 100+ km) but not small (10s of km) spatial scales. The minimum average effective population size at our sampling sites was low (c. 25). In coastal grassland (machair), the estimated modal foraging distance of workers was 391 m, with 95% of foraging activity occurring within 955 m of the nest, and estimated nest density was 19.3 nests km(-2). These findings show that B. distinguendus exhibits some genetic features of scarce, declining or fragmented populations. Moreover, B. distinguendus workers appear to forage over above-average distances and nests remain thinly distributed even in current strongholds. These considerations should inform future conservation actions for this and similar species.

Detecting changes in habitat-scale bee foraging in a tropical fragmented landscape using stable isotopes

As the body of research on the ecosystem service of pollination grows, our ability to tackle a range of agricultural, conservation, and land management issues is limited by our understanding of pollinator foraging patterns and requirements. In particular, better knowledge of which habitats bees utilize for foraging over their lifetime would inform a range of applied and theoretical questions. Traditional methods of studying foraging are either impractical for insects (e.g. radio tracking) or else are limited spatially or temporally (e.g. observations by researchers). Here we describe a method for using stable isotopes of carbon and nitrogen from bee tissues to gain an integrated signal of which habitats a bee has foraged in over its lifetime, using three species of social stingless bee (Apidae: Meliponini) in a fragmented tropical forest landscape in southern Costa Rica as a test case. There were strongly significant differences in the carbon and nitrogen isotope signals of bees collected in the landscape extremes: the largest forests and largest open pastures in the region. We could not estimate proportions of dietary carbon and nitrogen derived from different habitats, however, due to the high sample variance. Still, isotope ratios reflect a signature of the habitat that a bee has foraged in, and we found significant relationships between foraging patterns and season, landscape context (proportion of forest surrounding sample sites) and local biotic context (bee and plant diversity and abundance). Landscape context was the most consistent factor among the analyses, in line with the idea that meliponines do not preferentially forage in deforested habitats. Bee and plant diversity and abundance showed various significant relationships with the isotopic values of the different species, but the patterns were inconsistent. These results are potentially consistent with habitat switching from pasture to forest in areas of greater competition, but the extreme spatiotemporal variability in resource density likely blurs these patterns.

Landscape structure, habitat fragmentation, and the ecology of insects

Landscape structure, habitat fragmentation, and the ecology of insects