Importance of pollinators in changing landscapes for world crops

The extent of our reliance on animal pollination for world crop production for human food has not previously been evaluated and the previous estimates for countries or continents have seldom used primary data. In this review, we expand the previous estimates using novel primary data from 200 countries and found that fruit, vegetable or seed production from 87 of the leading global food crops is dependent upon animal pollination, while 28 crops do not rely upon animal pollination. However, global production volumes give a contrasting perspective, since 60% of global production comes from crops that do not depend on animal pollination, 35% from crops that depend on pollinators, and 5% are unevaluated. Using all crops traded on the world market and setting aside crops that are solely passively self-pollinated, wind-pollinated or parthenocarpic, we then evaluated the level of dependence on animal-mediated pollination for crops that are directly consumed by humans. We found that pollinators are essential for 13 crops, production is highly pollinator dependent for 30, moderately for 27, slightly for 21, unimportant for 7, and is of unknown significance for the remaining 9. We further evaluated whether local and landscape-wide management for natural pollination services could help to sustain crop diversity and production. Case studies for nine crops on four continents revealed that agricultural intensification jeopardizes wild bee communities and their stabilizing effect on pollination services at the landscape scale.     

传粉动物多样性的保护与农业景观传粉服务的提升

传粉动物为许多植物尤其是作物提供了重要的传粉服务, 在保障全球粮食安全和人类福祉、缓冲气候变化对作物产量的影响等方面都发挥着重要的作用。然而来自全球土地利用变化、化学农药使用、外来物种入侵及气候变化等的威胁, 导致传粉动物的多样性下降并造成了依赖动物传粉的作物产量和品质的下降。针对这一情况, 作者提出了农业景观传粉动物多样性保护和利用的3种主要途径: (1)改善生产管理, 例如减少化学农药的使用、适当地采取有机种植; (2)促进景观多样性, 包括创建适宜野生传粉者的半自然生境、保护高价值的自然生境、作物多样化、合理配置资源和生境的空间分布; (3)加强对本土传粉动物的保护和开发利用。文章最后提出, 为进一步提升传粉服务, 还需加强对传粉者的生物学特征、传粉服务的需求与供给现状、影响传粉动物多样性和传粉服务的农作措施和景观因素等方面的研究。     

A heterogeneous landscape does not guarantee high crop pollination

The expansion of pollinator-dependent crops, especially in the developing world, together with reports of worldwide pollinator declines, raises concern of possible yield gaps. Farmers directly reliant on pollination services for food supply often live in regions where our knowledge of pollination services is poor. In a manipulative experiment replicated at 23 sites across an Ethiopian agricultural landscape, we found poor pollination services and severe pollen limitation in a common oil crop. With supplementary pollination, the yield increased on average by 91%. Despite the heterogeneous agricultural matrix, we found a low bee abundance, which may explain poor pollination services. The variation in pollen limitation was unrelated to surrounding forest cover, local bee richness and bee abundance. While practices that commonly increase pollinators (restricted pesticide use, flower strips) are an integral part of the landscape, these elements are apparently insufficient. Management to increase pollination services is therefore in need of urgent investigation.     

Bumble bee abundance and richness improves honey bee pollination behaviour in sweet cherry

Pollination service in agricultural crops increases significantly with pollinator diversity and wild pollinator abundance. Differences in the foraging behaviour of pollinating insects are one of the reasons why pollinator diversity and abundance enhances crop pollination. Here, we focused on the foraging behaviour of honey bees and bumble bees in sweet cherry orchards. In addition, we studied the influence of bee diversity and abundance on the foraging behaviour of honey bees and bumble bees. Honey bees were found to visit fewer flowers than bumble bees. Bumble bees also showed a higher probability of changing trees between rows than honey bees. Both visitation rate and probability of row changes of honey bees increased with bumble bee diversity and with bumble bee abundance. We also found that the probability of row changes of honey bees increased with increasing bumble bee abundance. These effects of bumble bee richness and abundance on the pollination behaviour of honey bees can improve the pollination performance of honey bees in crops that depend on cross pollination. Our results highlight the higher pollination performance of bumble bees and the facilitative effect of wild pollinators to crop pollination.     

Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops

If climate change affects pollinator‐dependent crop production, this will have important implications for global food security because insect pollinators contribute to production for 75% of the leading global food crops. We investigate whether climate warming could result in indirect impacts upon crop pollination services via an overlooked mechanism, namely temperature‐induced shifts in the diurnal activity patterns of pollinators. Using a large data set on bee pollination of watermelon crops, we predict how pollination services might change under various climate change scenarios. Our results show that under the most extreme IPCC scenario (A1F1), pollination services by managed honey bees are expected to decline by 14.5%, whereas pollination services provided by most native, wild taxa are predicted to increase, resulting in an estimated aggregate change in pollination services of +4.5% by 2099. We demonstrate the importance of native biodiversity in buffering the impacts of climate change, because crop pollination services would decline more steeply without the native, wild pollinators. More generally, our study provides an important example of how biodiversity can stabilize ecosystem services against environmental change.     

How much does agriculture depend on pollinators? Lessons from long-term trends in crop production

Background and Aims

Productivity of many crops benefits from the presence of pollinating insects, so a decline in pollinator abundance should compromise global agricultural production. Motivated by the lack of accurate estimates of the size of this threat, we quantified the effect of total loss of pollinators on global agricultural production and crop production diversity. The change in pollinator dependency over 46 years was also evaluated, considering the developed and developing world separately.

Methods

Using the extensive FAO dataset, yearly data were compiled for 1961–2006 on production and cultivated area of 87 important crops, which we classified into five categories of pollinator dependency. Based on measures of the aggregate effect of differential pollinator dependence, the consequences of a complete loss of pollinators in terms of reductions in total agricultural production and diversity were calculated. An estimate was also made of the increase in total cultivated area that would be required to compensate for the decrease in production of every single crop in the absence of pollinators.

Key Results

The expected direct reduction in total agricultural production in the absence of animal pollination ranged from 3 to 8 %, with smaller impacts on agricultural production diversity. The percentage increase in cultivated area needed to compensate for these deficits was several times higher, particularly in the developing world, which comprises two-thirds of the land devoted to crop cultivation globally. Crops with lower yield growth tended to have undergone greater expansion in cultivated area. Agriculture has become more pollinator-dependent over time, and this trend is more pronounced in the developing than developed world.

Conclusions

We propose that pollination shortage will intensify demand for agricultural land, a trend that will be more pronounced in the developing world. This increasing pressure on supply of agricultural land could significantly contribute to global environmental change.Key words: Agricultural production, biotic pollination, crop diversity, cultivated area, developed world, developing world, FAO, randomization     

中国农业生态系统昆虫授粉功能量与服务价值评估

所有开花植物中大约有80%的物种需要动物作为授粉媒介。系统介绍了中国重要栽培作物花的结构和类型,授粉过程、媒介和方式,作物对昆虫授粉的依赖程度,昆虫授粉功能与服务的概念,以及昆虫授粉功能量与服务价值量的评估方法;同时评估了我国各省农业生态系统中昆虫对重要作物的授粉功能量与服务价值量。结果表明:粮食作物、水果作物、蔬菜作物和经济作物不同程度的依赖昆虫授粉。根据2015年主要农作物产量、作物产品价格、昆虫授粉依赖程度等数据,计算得出昆虫对我国22类主要农作物的授粉功能量为1.8亿吨农产品产量和授粉服务价值为8860.5亿元(占当年GDP的1.3%),具有巨大的经济价值。2015年昆虫对主要栽培作物的授粉功能量和服务价值排在前五名的都是山东、河南、河北、陕西和新疆,年授粉服务价值均大于500亿元,反映出这5个省的主要农作物对昆虫授粉依赖程度较高。昆虫对作物的授粉功能量评价有助于了解昆虫对作物生物量或产量的生物学和生态学效应以及作物对昆虫授粉的需求。昆虫对作物的授粉服务价值评估有助于掌握昆虫授粉为人类所带来的经济效应或经济价值,并帮助决策维持或增强授粉昆虫多样性和种群数量的人力、物力和财力投入。     

Seasonal complementary in pollinators of soft-fruit crops

Understanding the relative contributions of wild and managed pollinators, and the functional contributions made by a diverse pollinator community, is essential to the maintenance of yields in the 75% of our crops that benefit from insect pollination. We describe a field study and pollinator exclusion experiments conducted on two soft-fruit crops in a system with both wild and managed pollinators. We test whether fruit quality and quantity is limited by pollination, and whether different pollinating insects respond differently to varying weather conditions. Both strawberries and raspberries produced fewer marketable fruits when insects were excluded, demonstrating dependence on insect pollinators. Raspberries had a short flowering season which coincided with peak abundance of bees, and attracted many bees per flower. In contrast, strawberries had a much longer flowering season and appeared to be much less attractive to pollinators, so that ensuring adequate pollination is likely to be more challenging. The proportion of high-quality strawberries was positively related to pollinator abundance, suggesting that yield was limited by inadequate pollination on some farms. The relative abundance of different pollinator taxa visiting strawberries changed markedly through the season, demonstrating seasonal complementarity. Insect visitors responded differently to changing weather conditions suggesting that diversity can reduce the risk of pollination service shortfalls. For example, flies visited the crop flowers in poor weather and at the end of the flowering season when other pollinators were scarce, and so may provide a unique functional contribution. Understanding how differences between pollinator groups can enhance pollination services to crops strengthens the case for multiple species management. We provide evidence for the link between increased diversity and function in real crop systems, highlighting the risks of replacing all pollinators with managed alternatives.     

Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency

There is evidence that pollinators are declining as a result of local and global environmental degradation [1-4]. Because a sizable proportion of the human diet depends directly or indirectly on animal pollination [5], the issue of how decreases in pollinator stocks could affect global crop production is of paramount importance [6-8]. Using the extensive FAO data set [9], we compared 45 year series (1961-2006) in yield, and total production and cultivated area of pollinator-dependent and nondependent crops [5]. We investigated temporal trends separately for the developed and developing world because differences in agricultural intensification, and socioeconomic and environmental conditions might affect yield and pollinators [10-13]. Since 1961, crop yield (Mt/ha) has increased consistently at average annual growth rates of approximately 1.5%. Temporal trends were similar between pollinator-dependent and nondependent crops in both the developed and developing world, thus not supporting the view that pollinator shortages are affecting crop yield at the global scale. We further report, however, that agriculture has become more pollinator dependent because of a disproportionate increase in the area cultivated with pollinator-dependent crops. If the trend toward favoring cultivation of pollinator-dependent crops continues, the need for the service provided by declining pollinators will greatly increase in the near future.     

Supporting crop pollinators with floral resources: network‐based phenological matching

The production of diverse and affordable agricultural crop species depends on pollination services provided by bees. Indeed, the proportion of pollinator‐dependent crops is increasing globally. Agriculture relies heavily on the domesticated honeybee; the services provided by this single species are under threat and becoming increasingly costly. Importantly, the free pollination services provided by diverse wild bee communities have been shown to be sufficient for high agricultural yields in some systems. However, stable, functional wild bee communities require floral resources, such as pollen and nectar, throughout their active season, not just when crop species are in flower. To target floral provisioning efforts to conserve and support native and managed bee species, we apply network theoretical methods incorporating plant and pollinator phenologies. Using a two‐year dataset comprising interactions between bees (superfamily Apoidea, Anthophila) and 25 native perennial plant species in floral provisioning habitat, we identify plant and bee species that provide a key and central role to the stability of the structure of this community. We also examine three specific case studies: how provisioning habitat can provide temporally continuous support for honeybees (Apis mellifera) and bumblebees (Bombus impatiens), and how resource supplementation strategies might be designed for a single genus of important orchard pollinators (Osmia). This framework could be used to provide native bee communities with additional, well‐targeted floral resources to ensure that they not only survive, but also thrive.     

Pollinator‐mediated interactions between cultivated papaya and co‐flowering plant species

Many modern crop varieties rely on animal pollination to set fruit and seeds. Intensive crop plantations usually do not provide suitable habitats for pollinators so crop yield may depend on the surrounding vegetation to maintain pollination services. However, little is known about the effect of pollinator‐mediated interactions among co‐flowering plants on crop yield or the underlying mechanisms. Plant reproductive success is complex, involving several pre‐ and post‐pollination events; however, the current literature has mainly focused on pre‐pollination events in natural plant communities. We assessed pollinator sharing and the contribution to pollinator diet in a community of wild and cultivated plants that co‐flower with a focal papaya plantation. In addition, we assessed heterospecific pollen transfer to the stigmatic loads of papaya and its effect on fruit and seed production. We found that papaya shared at least one pollinator species with the majority of the co‐flowering plants. Despite this, heterospecific pollen transfer in cultivated papaya was low in open‐pollinated flowers. Hand‐pollination experiments suggest that heterospecific pollen transfer has no negative effect on fruit production or weight, but does reduce seed production. These results suggest that co‐flowering plants offer valuable floral resources to pollinators that are shared with cultivated papaya with little or no cost in terms of heterospecific pollen transfer. Although HP reduced seed production, a reduced number of seeds per se are not negative, given that from an agronomic perspective the number of seeds does not affect the monetary value of the papaya fruit.     

Integrated crop pollination to buffer spatial and temporal variability in pollinator activity

Insect pollination improves the yield and quality of many crops, yet there is increasing evidence of insufficient insect pollinators limiting crop production. Effective Integrated Crop Pollination (ICP) involves adaptable, targeted and cost-effective management of crop pollination and encourages the use of both wild and managed pollinators where appropriate. In this study we investigate how the addition of honeybee hives affects the community of insects visiting oilseed rape, and if hive number and location affect pollinator foraging and oilseed rape pollination in order to provide evidence for effective ICP. We found that introducing hives increased overall flower visitor numbers and altered the pollinator community, which became dominated by honeybees. Furthermore a greater number of hives did not increase bee numbers significantly but did result in honeybees foraging further into fields. The timing of surveys and proximity to the field edge influenced different pollinators in different ways and represents an example of spatial and temporal complementarity. For example dipteran flower visitor numbers declined away from the field edge whereas honeybees peaked at intermediate distances into the field. Furthermore, no significant effects of survey round on wild bees overall was observed but honeybee numbers were relatively lower during peak flowering and dipteran abundance was greater in later survey rounds. Thus combining diverse wild pollinators and managed species for crop pollination buffers spatial and temporal variation in flower visitation. However we found no effect of insect pollination on seed set or yield of oilseed rape in our trial, highlighting the critical need to understand crop demand for insect pollination before investments are made in managing pollination services.     

Experimental evidence that wildflower strips increase pollinator visits to crops

Wild bees provide a free and potentially diverse ecosystem service to farmers growing pollination‐dependent crops. While many crops benefit from insect pollination, soft fruit crops, including strawberries are highly dependent on this ecosystem service to produce viable fruit. However, as a result of intensive farming practices and declining pollinator populations, farmers are increasingly turning to commercially reared bees to ensure that crops are adequately pollinated throughout the season. Wildflower strips are a commonly used measure aimed at the conservation of wild pollinators. It has been suggested that commercial crops may also benefit from the presence of noncrop flowers; however, the efficacy and economic benefits of sowing flower strips for crops remain relatively unstudied. In a study system that utilizes both wild and commercial pollinators, we test whether wildflower strips increase the number of visits to adjacent commercial strawberry crops by pollinating insects. We quantified this by experimentally sowing wildflower strips approximately 20 meters away from the crop and recording the number of pollinator visits to crops with, and without, flower strips. Between June and August 2013, we walked 292 crop transects at six farms in Scotland, recording a total of 2826 pollinators. On average, the frequency of pollinator visits was 25% higher for crops with adjacent flower strips compared to those without, with a combination of wild and commercial bumblebees (Bombus spp.) accounting for 67% of all pollinators observed. This effect was independent of other confounding effects, such as the number of flowers on the crop, date, and temperature. Synthesis and applications. This study provides evidence that soft fruit farmers can increase the number of pollinators that visit their crops by sowing inexpensive flower seed mixes nearby. By investing in this management option, farmers have the potential to increase and sustain pollinator populations over time.     

Global malnutrition overlaps with pollinator-dependent micronutrient production

Pollinators contribute around 10% of the economic value of crop production globally, but the contribution of these pollinators to human nutrition is potentially much higher. Crops vary in the degree to which they benefit from pollinators, and many of the most pollinator-dependent crops are also among the richest in micronutrients essential to human health. This study examines regional differences in the pollinator dependence of crop micronutrient content and reveals overlaps between this dependency and the severity of micronutrient deficiency in people around the world. As much as 50% of the production of plant-derived sources of vitamin A requires pollination throughout much of Southeast Asia, whereas other essential micronutrients such as iron and folate have lower dependencies, scattered throughout Africa, Asia and Central America. Micronutrient deficiencies are three times as likely to occur in areas of highest pollination dependence for vitamin A and iron, suggesting that disruptions in pollination could have serious implications for the accessibility of micronutrients for public health. These regions of high nutritional vulnerability are understudied in the pollination literature, and should be priority areas for research related to ecosystem services and human well-being.     

Mass‐flowering crops dilute pollinator abundance in agricultural landscapes across Europe

Mass‐flowering crops (MFCs) are increasingly cultivated and might influence pollinator communities in MFC fields and nearby semi‐natural habitats (SNHs). Across six European regions and 2 years, we assessed how landscape‐scale cover of MFCs affected pollinator densities in 408 MFC fields and adjacent SNHs. In MFC fields, densities of bumblebees, solitary bees, managed honeybees and hoverflies were negatively related to the cover of MFCs in the landscape. In SNHs, densities of bumblebees declined with increasing cover of MFCs but densities of honeybees increased. The densities of all pollinators were generally unrelated to the cover of SNHs in the landscape. Although MFC fields apparently attracted pollinators from SNHs, in landscapes with large areas of MFCs they became diluted. The resulting lower densities might negatively affect yields of pollinator‐dependent crops and the reproductive success of wild plants. An expansion of MFCs needs to be accompanied by pollinator‐supporting practices in agricultural landscapes.     

Ecological intensification to mitigate impacts of conventional intensive land use on pollinators and pollination

Worldwide, human appropriation of ecosystems is disrupting plant–pollinator communities and pollination function through habitat conversion and landscape homogenisation. Conversion to agriculture is destroying and degrading semi‐natural ecosystems while conventional land‐use intensification (e.g. industrial management of large‐scale monocultures with high chemical inputs) homogenises landscape structure and quality. Together, these anthropogenic processes reduce the connectivity of populations and erode floral and nesting resources to undermine pollinator abundance and diversity, and ultimately pollination services. Ecological intensification of agriculture represents a strategic alternative to ameliorate these drivers of pollinator decline while supporting sustainable food production, by promoting biodiversity beneficial to agricultural production through management practices such as intercropping, crop rotations, farm‐level diversification and reduced agrochemical use. We critically evaluate its potential to address and reverse the land use and management trends currently degrading pollinator communities and potentially causing widespread pollination deficits. We find that many of the practices that constitute ecological intensification can contribute to mitigating the drivers of pollinator decline. Our findings support ecological intensification as a solution to pollinator declines, and we discuss ways to promote it in agricultural policy and practice.     

Natural hazard threats to pollinators and pollination

Natural hazards are naturally occurring physical events that can impact human welfare both directly and indirectly, via shocks to ecosystems and the services they provide. Animal‐mediated pollination is critical for sustaining agricultural economies and biodiversity, yet stands to lose both from present exposure to natural hazards, and future climate‐driven shifts in their distribution, frequency, and intensity. In contrast to the depth of knowledge available for anthropogenic‐related threats, our understanding of how naturally occurring extreme events impact pollinators and pollination has not yet been synthesized. We performed a systematic review and meta‐analysis to examine the potential impacts of natural hazards on pollinators and pollination in natural and cultivated systems. From a total of 117 studies (74% of which were observational), we found evidence of community and population‐level impacts to plants and pollinators from seven hazard types, including climatological (extreme heat, fire, drought), hydrological (flooding), meteorological (hurricanes), and geophysical (volcanic activity, tsunamis). Plant and pollinator response depended on the type of natural hazard and level of biological organization observed; 19% of cases reported no significant impact, whereas the majority of hazards held consistent negative impacts. However, the effects of fire were mixed, but taxa specific; meta‐analysis revealed that bee abundance and species richness tended to increase in response to fire, differing significantly from the mainly negative response of Lepidoptera. Building from this synthesis, we highlight important future directions for pollination‐focused natural hazard research, including the need to: (a) advance climate change research beyond static “mean‐level” changes by better incorporating “shock” events; (b) identify impacts at higher levels of organization, including ecological networks and co‐evolutionary history; and (c) address the notable gap in crop pollination services research—particularly in developing regions of the world. We conclude by discussing implications for safeguarding pollination services in the face of global climate change.     

The pollination niche and its role in the diversification and maintenance of the southern African flora

The flora of southern Africa has exceptional species richness and endemism, making it an ideal system for studying the patterns and processes of evolutionary diversification. Using a wealth of recent case studies, I examine the evidence for pollinator-driven diversification in this flora. Pollination systems, which represent available niches for ecological diversification, are characterized in southern Africa by a high level of ecological and evolutionary specialization on the part of plants, and, in some cases, by pollinators as well. These systems are asymmetric, with entire plant guilds commonly specialized for a particular pollinator species or functional type, resulting in obvious convergent floral evolution among guild members. Identified modes of plant lineage diversification involving adaptation to pollinators in these guilds include (i) shifts between pollination systems, (ii) divergent use of the same pollinator, (iii) coevolution, (iv) trait tracking, and (v) floral mimicry of different model species. Microevolutionary studies confirm that pollinator shifts can be precipitated when a plant species encounters a novel pollinator fauna on its range margin, and macroevolutionary studies confirm frequent pollinator shifts associated with lineage diversification. As Darwin first noted, evolutionary specialization for particular pollinators, when resulting in ecological dependency, may increase the risk of plant extinction. I thus also consider the evidence that disturbance provokes pollination failure in some southern African plants with specialized pollination systems.     

The role of insect pollinators in avocado production: A global review

Insect pollination increases the yield and quality of many crops and therefore, understanding the role of insect pollinators in crop production is necessary to sustainably increase yields. Avocado Persea americana benefits from insect pollination, however, a better understanding of the role of pollinators and their contribution to the production of this globally important crop is needed. In this study, we carried out a systematic literature review and meta-analysis of studies investigating the pollination ecology of avocado to answer the following questions: (a) Are there any research gaps in terms of geographic location or scientific focus? (b) What is the effect of insect pollinators on avocado pollination and production? (c) Which pollinators are the most abundant and effective and how does this vary across location? (d) How can insect pollination be improved for higher yields? (e) What are the current evidence gaps and what should be the focus of future research? Research from many regions of the globe has been published, however, results showed that there is limited information from key avocado producing countries such as Mexico and the Dominican Republic. In most studies, insects were shown to contribute greatly to pollination, fruit set and yield. Honeybees Apis mellifera were important pollinators in many regions due to their efficiency and high abundance, however, many wild pollinators also visited avocado flowers and were the most frequent visitors in over 50% of studies. This study also highlighted the effectiveness of stingless bees (Meliponini) and blow flies (Calliphoridae) as avocado pollinators although, for the majority of flower visitors, there is a lack of data on pollinator efficiency. For optimal yields, growers should ensure a sufficient abundance of pollinators in their orchards either through increasing honeybee hive density or, for a more sustainable approach, by managing wild pollinators through practices that protect or promote natural habitat.     

Climate‐driven spatial mismatches between British orchards and their pollinators: increased risks of pollination deficits

Understanding how climate change can affect crop‐pollinator systems helps predict potential geographical mismatches between a crop and its pollinators, and therefore identify areas vulnerable to loss of pollination services. We examined the distribution of orchard species (apples, pears, plums and other top fruits) and their pollinators in Great Britain, for present and future climatic conditions projected for 2050 under the SRES A1B Emissions Scenario. We used a relative index of pollinator availability as a proxy for pollination service. At present, there is a large spatial overlap between orchards and their pollinators, but predictions for 2050 revealed that the most suitable areas for orchards corresponded to low pollinator availability. However, we found that pollinator availability may persist in areas currently used for fruit production, which are predicted to provide suboptimal environmental suitability for orchard species in the future. Our results may be used to identify mitigation options to safeguard orchard production against the risk of pollination failure in Great Britain over the next 50 years; for instance, choosing fruit tree varieties that are adapted to future climatic conditions, or boosting wild pollinators through improving landscape resources. Our approach can be readily applied to other regions and crop systems, and expanded to include different climatic scenarios.