Pollinator diversity, pollination services, and conservation in agroecosystems: A mini‐review on the successes and challenges in China

Pollinators provide important pollination services for crops around the world. In China, numerous studies have been conducted on pollinators within agroecosystems, yet a comprehensive review of such research remains to be completed. This study discusses the existing knowledge of pollinator diversity in Chinese agroecosystems, examines the provision of pollination services, and identifies key achievements and limitations. We propose a series of conservation and management actions to promote pollinator health and ecosystem services in these agroecosystems: (1) long‐term monitoring of pollinator populations, (2) designing agricultural landscapes that are conducive to pollinators, and (3) implementing microscale habitat modifications to improve conditions for pollinators.


Plain language summary
Pollinators, such as bees and moths, are crucial for the pollination of crops globally.In China, significant research has been done on pollinators in agricultural settings but a comprehensive review of these studies is missing.This study examines the current research on pollinator diversity within Chinese agroecosystems and the vital pollination services these species provide for agricultural production.It also proposes a series of conservation and management strategies aimed at preserving pollinator diversity in China's agricultural landscapes.These include long-term monitoring of insect pollinators, designing agricultural landscapes that support pollinators, and making small-scale habitat changes to enhance their living conditions.

| INTRODUCTION
Pollinators, critical for crop pollination globally (Aizen et al., 2009;Olhnuud et al., 2022), have significantly contributed to agricultural growth in China in the past 60 years.The expansion of cultivated areas and total agricultural yields has been notably higher in pollinator-dependent crops compared to those not requiring pollinators, indicating the vital role of pollination services in the country (Mashilingi et al., 2021).Despite their importance, pollinator research in China has been surprisingly limited (Teichroew et al., 2017;Warrit et al., 2023).While the general pollination ecology in China has been reviewed (Ren et al., 2018), there remains a need for focused synthesis on pollinator diversity and pollination services within agroecosystems.
With one of the world's largest human populations and limited arable land due to the highly complex and heterogeneous environment, food security is a central issue in China.The majority of Chinese farmlands are owned by smallholders with less than two hectares (Lowder et al., 2016).These small-scale farmers are particularly vulnerable to the decline of pollination services, as their livelihoods and food security rely heavily on crop production.Despite the significance of these issues, Chinese agricultural systems are often overlooked in global pollination research (Allen-Perkins et al., 2022;Garibaldi et al., 2016).
To address this knowledge gap, we conducted a synthetic mini-review focusing on the progress and challenges of studies on pollinator diversity, pollination services, and conservation in agroecosystems in China.This review does not aim to provide an exhaustive summary, such as detailing pollinator diversity in each type of Chinese agroecosystem, but rather to synthesize key aspects.We discuss three important areas in pollinator research within Chinese agroecosystems.Initially, we explore the current status of pollinator diversity studies on pollinator diversity.Following this, we analyze the contributions of pollinators to crop yields and how better management of pollinators can enhance these yields.Finally, we propose strategies to improve the conservation of pollinators within these agroecosystems.
As examples of the high diversity seen in crops, Wu et al. (2019) (Ollerton, 2017;Orr et al., 2021).In contrast, subtropical and tropical regions exhibit a greater abundance of social bee species and other pollinating groups, including vertebrates such as generalist passerine birds for loquat (Fang et al., 2012) and bats for tropical fruit orchards (Sritongchuay et al., 2019).
In agroecosystems, landscape dynamics shape pollinator communities (Tscharntke et al., 2005).Seminatural habitats within agricultural landscapes are beneficial for pollinators, providing nesting sites and materials, floral resources, and a buffer against the negative effects of herbicides or pesticides (Garibaldi et al., 2021;Park et al., 2015).In China, research has demonstrated that seminatural habitats can increase wild pollinator diversity (Wu, Dai, et al., 2021;Zou, Bianchi, et al., 2017) and mitigate the negative impacts of agricultural intensification (Shi et al., 2021).However, the type of seminatural habitat plays a role, with certain types, like shrubs, being more beneficial to wild pollinator communities than others (Wu et al., 2019).Most agricultural regions in China, such as the Huang-Huai-Hai region, have limited seminatural habitats due to the large population and scarce arable land.In such areas, alternative conservation approaches, like establishing wildflower strips, are crucial for sustaining diverse wild pollinator populations of different species, although preserving nesting habitats also remains essential.
In agricultural landscapes, Xie et al. (2019) and Lu et al. (2019) have investigated the foraging patterns of pollinators, noting their movements from seminatural habitats to croplands.Threats to pollinators, such as introduced species, natural enemies, and the application of herbicides and pesticides-particularly during flowering periods-have been documented (Mu et al., 2022;Song et al., 2021;Yan et al., 2022).Research has also extended to broader scales, like the long-distance windborne migration of hoverflies, which are potential crop pollinators across China (Jia et al., 2022).Such studies are essential to gain a better understanding of pollinator diversity and its influence at various scales within China.While some studies have focused on the effects of pesticide residues on managed honeybees (Li, 2022;Tong et al., 2018), more comprehensive investigations are needed.The use of chemicals in agriculture can significantly affect pollinators and their services (Ma et al., 2024), underscoring the need for extensive research in this area.
The functional traits of pollinators, such as body size, can affect their pollination performance (Campbell et al., 2022;Fontaine et al., 2005), with larger bees often being more effective than smaller ones (Jauker et al., 2016), except for pollinating smallflowered species inaccessible to larger bees.Despite this, studies on the functional diversity of pollinators within the Chinese landscape are limited.Agricultural landscape management can affect pollinator groups based on their traits, such as nesting biology.For example, removing wood might reduce available space for cavity-nesting species, and a lack of bare ground can limit ground-nesting species (Williams et al., 2010).A contributing factor to the scarcity of functional diversity studies might be the lack of functional trait data, like diet breadth, which is often challenging to determine.To address this gap, it is necessary to investigate and record comprehensive functional trait data for wild pollinators, particularly in representative sites across China and for species with well-understood traits.This will facilitate more detailed studies on pollinator dynamics and their responses to agricultural landscapes.Therefore, recognizing the high diversity of pollinators in China's agroecosystems, further research should aim to assess the impact of agricultural landscapes on pollinator diversity, with a focus on functional diversity, to gain a more comprehensive understanding.

| POLLINATION SERVICES IN CHINA'S AGROECOSYSTEMS
Pollination services significantly contribute to agricultural yield, attracting considerable attention from researchers and stakeholders (Breeze et al., 2011).In China, extensive research has been conducted on the pollination services provided by both wild and managed pollinators, like honeybees, for various crops (Li, Orr, et al., 2022;Wu, Tscharntke, et al., 2021;Zhang et al., 2015).Efforts to rear and manage bumblebees are also underway, with a recent shift toward using native species rather than the introduced Bombus terrestris (Orr et al., 2022).Wild pollinators have been shown to significantly enhance yields; for instance, Zou, Xiao, et al., 2017 reported wild pollinators could contribute a 12% yield increase for oilseed rape.
The interaction between pollinators and farming practices-like irrigation, tillage, and agrochemical use-needs further exploration to guide farmland management in China, although some studies have begun to address this (Wu, Tscharntke, et al., 2021).He et al. (2020) reported 78.7% and 31.9%yield increases for oil peony crops pollinated by honeybees and ground bumblebees, respectively.However, assessments on pollination services of stingless bees are lacking, despite the fact that multiple stingless bee species are potential managed pollinators for tropical crops and fruits in southern China, including mango (Qu, Wang, et al., 2022;Qu, Wen, et al., 2022).
There is a global consensus that increasing pollinator diversity can promote pollination services (Garibaldi et al., 2014;Woodcock et al., 2019).Yet, in China, there is a need for more studies to establish the specific relationship between pollinator diversity and pollination services.In some specific cases, conserving pollinator diversity may not lead to increases in pollination services because not all species contribute equally to pollination effectiveness.Research has shown that flower visitor communities in agroecosystems are often dominated by a small number of common insect species, while threatened species are rarely observed on crops (Kleijn et al., 2015).Moreover, not all pollinators present in agroecosystems visit crop flowers, which can disconnect their presence from actual yield impacts.Hence, in terms of tackling pollen deficits and improving yields, the focus should shift toward studying the species that specialize in pollinating dependent crops, such as Osmia excavata for apple and Colletes gigas for oil tea, to better understand and harness their potential in pollination services (Huang et al., 2021).
To ensure stable crop yields, the role of managed pollinators becomes key.Beyond the commonly managed honeybees (A.mellifera and A. cerana), alternative pollinators like bumblebees and other wild bee species, including the aforementioned O. excavata, have been explored for their effectiveness in agricultural settings (Ding et al., 2019;Huang & An, 2018;Huang et al., 2021;Lyu et al., 2023;Naeem et al., 2020;Orr et al., 2022;Wei et al., 2002;Zhang, Han, et al., 2022).There is now a positive shift toward the use of native species for managed pollination, moving away from introduced species such as the bumblebee B. terrestris.Within an agroecosystem, it is possible that these managed pollinators can provide synergistic pollination benefits by working alongside local wild pollinators to further increase yields, but studies exploring the interactions between managed pollinators and native pollinator communities in China are lacking.Furthermore, there are concerns that introduced pollinators may compete with native pollinators for food and nesting locations, potentially disrupting local ecosystems (Russo, 2016).Future studies in China are required to assess these potential negative impacts.Identifying and managing the most effective pollinators for specific crops involves assessing the best application timings and regions, conducting cost-benefit analyses, and considering the potential risks of introducing pollinators into agroecosystems.Through comprehensive evaluations, it should be possible to discern which crops most necessitate managed pollination and select the most suitable pollinators for these tasks.

| PROPOSED STRATEGIES FOR POLLINATOR CONSERVATION IN AGROECOSYSTEMS IN CHINA
Pollinator conservation approaches have been welldeveloped in Europe and North America, including wildflower strips (Campbell et al., 2017), wild bee hotels (e.g., bee nests for cavity-nesting bees, see MacIvor & Packer, 2015), and general biodiversity conservation methods that can benefit pollinators such as intercropping (Järvinen et al., 2022) and organic farming (Gabriel & Tscharntke, 2007).However, these strategies from other countries may not be directly applicable to China due to its vast and varied agricultural landscapes undergoing dramatic land use changes.Therefore, there is a need for cost-effective conservation approaches, such as wildflower strips, tailored to Chinese agroecosystems to ensure efficient use of limited management and conservation funds.
Herein, we propose three practices for improving pollinator conservation in Chinese agroecosystems: establishing long-term pollinator monitoring, designing pollinator-friendly agricultural landscapes, and developing effective pollinator conservation schemes, such as wildflower strips and bee hotels (Figure 1).
First, the establishment of long-term monitoring plans and networks in China is fundamental for tracking pollinator population trends and diversity, and for evaluating the impact of environmental changes on pollination services, particularly for major crops and fruits in their primary production areas.These efforts would also contribute to developing vital biodiversity baselines in regions where they do not yet exist.Investigating pollen deficits in key crops is another critical aspect.Additionally, given the adverse effects of pollutants such as heavy metals and pesticides on pollinators (Ma et al., 2024;Shi et al., 2023), monitoring these substances both in wild bees' bodies and their food sources (pollen and nectar) is crucial for protecting their health.The findings from such studies should be published and shared with conservation biologists, farmers, and other stakeholders to facilitate decision-making in agricultural practices and enhance participation in pollinator conservation schemes.
Second, creating pollinator-friendly agricultural landscapes is essential, especially in areas dominated by pollinator-dependent crops.Landscape design should incorporate a certain proportion of semi-natural habitats like forests, shrubs, vegetated field margins, and grasslands within agricultural landscapes, ideally within a 1000 m radius (Garibaldi et al., 2021).Additionally, increasing flowering crop diversity through methods such as intercropping is beneficial (Järvinen et al., 2022;Layek et al., 2021).However, these approaches must be tailored to regional conditions, as what works in one area may not be suitable in another.For instance, pollinator conservation efforts in smallholder farmlands in montane southern China should differ from those in state-owned farmland in northern China due to variations in field size, farmland management, climate, regional vegetation, and crop types (Figure 2) (Zou et al., 2024).Therefore, location-specific pollinator-friendly landscape designs are necessary as some of the successful strategies developed in Europe may not be applicable in China.In areas like southern China, with high landscape heterogeneity, merely increasing semi-natural habitat coverage may not suffice for effective pollinator conservation.Alternative strategies adapted to the local context and crop needs should be prioritized.We suggest that, in these regions, our third approach (see below) may be more effective for conserving pollinators in agroecosystems.
Third, microscale habitat modifications can be made to improve environments normally unsuitable for pollinators.This involves planning food and nesting resources, such as wildflower strips for feeding and bee hotels or bare ground for nesting.For example, in China, native flowering plants should be selected for wildflower strips to provide alternative food sources for native pollinators, especially outside the main blooming seasons of mass flowering crops (Hellwig et al., 2022).However, selecting appropriate plants can be complex due to regional differences in flora and fauna (Zhang, Han, et al., 2022), a process that is further complicated as life history information is lacking for many species (Warrit et al., 2023).Suitable nesting sites should be provided for wild pollinators, such as bee hotels for flower-visiting bees and wasps (Udayakumar & Shivalingaswamy, 2022), or bare ground for ground-nesting species, a technique that can be highly effective if a variety of bare ground is made accessible (e.g., soil and sand).Although researchers in China have begun to explore the ecological dynamics of trap nests (Guo et al., 2021), little has been done to explore their potential in Chinese agroecosystems, particularly outside of direct pollinator management (e.g., for Osmia).For places where pollinators are insufficient, alongside these efforts, initial fixes are possible by using native honeybees (A.cerana) not only for pollination but also for honey production (Bi et al., 2022(Bi et al., , 2024;;Guo et al., 2020).These approaches can also be coupled with broader initiatives, such as the adoption of noregret solutions aimed at stemming insect decline and others to reduce pollution.Implementation should include both top-down approaches with government departments, especially agricultural agencies such as the Ministry of Agriculture and Rural Affairs and the Ministry of Ecology and Environment, establishing pollinator conservation plans and regulations with cascading effects throughout Chinese agroecosystems and bottom-up approaches, with nongovernmental organizations (NGOs) collaborating with farmers at local scales to implement these measures effectively and sustainably.
In addition to the conservation approaches given above, collaboration among experts from different disciplines, such as entomologists, botanists, and agricultural scientists, is critical.Expert taxonomists can assist researchers in a variety of fields like agroecology or biodiversity conservation by identifying sampled pollinators, describing new species, and finding out important biological traits crucial for mass rearing or conservation efforts.Given the constant shortage of morphology-based taxonomists (Hong et al., 2022;Zhu et al., 2022), new techniques and pipelines have been developed for pollinator identification, including the construction of reference species libraries and DNA databases that cover multiple loci (Chesters et al., 2022;Liu et al., 2017).These advanced techniques can be incorporated into routine pollinator surveys to accelerate pollinator diversity research, offering deeper evolutionary insights for ecological analysis and conservation planning.Lastly, farmers, as stakeholders and landowners in agroecosystems, play important roles in pollinator conservation programs (Bloom et al., 2021); yet, their involvement has been minimal.Strengthening their engagement is crucial for a successful and cohesive pollinator protection strategy, requiring both governmental and NGO support, although a comprehensive strategy for this purpose is still lacking in China.

F
I G U R E 1 This schematic diagram describes the three proposed conservation interventions: a long-term pollinator monitoring plan, suitable agricultural landscapes, and wildflower strips and bee hotels.

F
I G U R E 2 The smallholder agricultural landscape in Jiangxi Province, Southern China, characterized by high seminatural habitat coverage.
Xiaoyu Shi, Dunyuan Huang, Huanli Xu, Zongxin Ren, Yanhui Lu, Jiandong An, Yi Zou, Yunhui Liu, Fang Ouyang, Douglas Chesters, Junpeng Mu, Chunling He, A'rong Luo, Rui Cheng, Qingsong Zhou, Zeqing Niu, Xin Zhou, Lei Zhao, Massimo Martini, Changsheng Ma, Wenda Cheng, Michael Orr, Wenjun Peng, Chaodong Zhu: Conceptualization; writing-original draft.Xia Chen: Conceptualization.ACKNOWLEDGMENTS We thank all the people who have contributed to the pollinator research in agroecosystem in China.Xiaoyu Shi was funded as a postdoc researcher by a program to investigate pollinator insects in East China from Ministry of Science and Technology (2018FY100401) and National Science & Technology Fundamental Resources Investigation Program of China (2018FY100400).A'rong Luo was supported by the National Science Fund for Excellent Young Scholars (32122016) and the National Natural Science Foundation of China (32070465).Chaodong Zhu's lab was supported by grants from the Key Laboratory of the Zoological Systematics and Evolution of the Chinese Academy of Sciences (grant number 2008DP173354).