Monographs on bee pollination in China.
Abstract
This work investigates the bee pollination of fruit trees, especially apples and pears in the field. We first introduce research carried out into bee pollination of crops in China, and then our own pollination experiments with managed bees such as Apis mellifera in the field. We monitor the efficiency of bee pollination of fruit trees by regulating hive bees and tree arrangement. In addition, we develop some methods to attract bees to visit fruit trees. Our research shows that the number of beehives and the arrangement of trees greatly influence bee pollination. The results provide a comprehensive tutorial on the best practices of bee pollination of fruit trees.
Keywords
- Bees
- pollination
- fruit tree
- apples
- pears
- pollination efficiency
1. Introduction
About 75 of all crops require pollination by bees. Some pollination is done by domesticated honeybees, but the pollination of most crops is done by wild insects, including wild bees. The decline of wild bee diversity in China has forced farmers to depend on managed bees such as
2. Pollination problem facing development of the fruit industry in China
2.1. Development of the fruit industry
China is a large country with many natural habitats and rich fruit tree resources. The cultivation of fruit trees involves more than 50 families of fruit trees, more than 300 species, and more than 10,000 varieties. Principal among these are apple, pear, peach, plum, apricot, plum, grapes, cherry, walnuts, citrus fruit, lychee, longan, loquat, olives, kiwi fruit, fig, pomegranate,
Apple trees have a wide distribution in China, can be evergreen or deciduous, and are widely grown across the YunnanGuizhou plateau. The deciduous varieties can be broken down into temperate deciduous, deciduous with dry temperature, dry cold deciduous, and hardy deciduous (figure 1)[1]. In 2011 the cultivated area devoted to apples in China reached 2.177 million hm2, accounted for about 42.0 of the world's total area devoted to the cultivation of apple, total output reached 35.985 million t, represented about 54.2 of total world yield, and had an output value of 160.52 billion yuan[2].
Pear trees are also important; they are grown across five fruit zones. They too can be deciduous or evergreen. Subtropical evergreen trees are grown in the south, whereas cold and dry deciduous fruit trees are grown in the north[1] (figure 1). By the end of 2012, according to statistical data released by the United Nations Food and Agriculture Organization[3], China's harvest pear covers an area of 1.138 million hm2, production is 1.721 million t, and area and yield are among the highest in the world.
Peach trees grow in temperate areas of China. They are mainly distributed in the YunnanGuizhou Plateau. They too can be evergreen or deciduous. They can be broken down into evergreen and deciduous mixed, temperate deciduous, drytemperature deciduous (figure 1)[1]. According to statistical data published by the United Nations Food and Agriculture Organization[3] by the end of 2010 the area devoted to peach cultivation in China was 732,000 hm2 and yield reached 10.828 million t, both of which were the highest in the world.
Fruit production has made great progress in China in recent years. This mainly applies to producing larger varieties, breeding, developing good fruit quality, and marketing of popular market varieties. The biological characteristics of tree species, their adaptability to the environment, improvement of plant varieties, and growing stock in the most appropriate biome possible, all help to optimize efficiency[4, 5] and improve fruit market competitiveness and economic benefits.
2.2. Serious shortage of fruit tree pollinators
Most of the apple, pear, plum, apricot, and chestnut varieties as well as almost all the sweet cherry varieties need be crosspollinated for the production of seed[6]. Because the pollen grains of nuts and fruits are big, heavy, sticky, and have an outer wall with a pattern of bumps, the wind cannot spread them easily. These fruits rely mainly on insect pollination, especially bees[7,8].
According to a survey of the literature, in the major appleproducing areas in Shanxi Province a total of 23 species of insects visit apple flowers. They belong to 4 orders and 14 families, mainly comprising hymenopteran (Hymenoptera) bees (Apidae), an anthophorid bee (Anthophoridae), leafcutting bees (Megachilidae), an andrenid bee (Andrenidae), and a dipteran (Diptera, Syrphidae). Among them, the Italian bee (
In recent years the number of bees and other pollinators has fallen sharply, which has drawn wide attention across the world. It is likely due to the use of pesticides resulting in a significant decline in the number of wild pollinators[13, 14]. In addition, largescale clearing of land for farming in the 15th and 16th centuries led to serious restriction of the habitat of wild insects. Climate change may cause inconsistency in plant phenophases and pollinator development periods, resulting in inadequate pollination[17]. In short, fruit tree pollination is the most pressing problem, with artificial pollination having to be adopted in some areas (figure 2); for example, about 30 of China's pear trees are artificially pollinated[18].
3. Present situation of fruit industry pollination technology in China
3.1. Chinese institutions engaged in research on fruit tree pollination technology
Chinese literature from 1980 to 2013 reveals that there are 161 institutions engaged in fruit tree pollination research, principal among which are the Chinese Academy of Agricultural Sciences Institute of Bees, the Horticulture Institute of the Shanxi Academy of Agricultural Sciences, and the Beijing Academy of Agriculture and Forestry. Between 1980 and 2011, there were 324 research papers on bees pollinating trees (figure 3), including 66 articles written between 1980 and 1992 (an average of 5 articles per year), a relatively stable number of articles between 1993 and 2001, and 204 articles from 2001 to 2011. Research content covered a wide range of factors from bee pollination methods, bee species selection to effects on cultivation and pollination evaluation. There were a few papers looking into how bee pollination increases production, bee pollination and ecology, crop breeding, and pollination colony management (figure 4).
Between 2001 and 2011, nine books were published on insect pollination technology research and application (table 1).
Monograph title | Author | Publishing date | Press | Page extent |
---|---|---|---|---|
Zeng Zhijiang | 2001.07 | Shanghai Popular Science Press | 274 | |
Shao Youquan | 2001.09 | Shanxi Science and Technology Press | 113 | |
Zhou Weiru | 2002.01 | Jindun Press | 143 | |
Wu Jie | 2004.01 | Chinese Agric ulture Press |
204 | |
Zhang Zhongyin, An Jiandong, Luo Shudong et al. | 2008.10 | Chinese Agri culture Press |
93 | |
Wang Yong | 2009.05 | Chinese Agriculture Science and Technology Press |
127 | |
Shao Youquan, Qi Haiping | 2010.05 | Jindun Press | 202 | |
Liu Xinyu, Gao Chongdong | 2011.05 | Northwest Agric ulture and Forestry University Press |
133 | |
Wu Jie, Shao Youquan | 2011.07 | Chinese agriculture press | 173 |
According to the State Intellectual Property Office patent database, from 2000 to 2013 there were 54 classes of bee pollination patents: 43 invention patents and 11 utility model patents. They covered a wide range of factors from bee pollination application technology, pollinating bee breeding technology, pollinating bee management methods, to the induction of bee pollination methods, design and transformation of pollination hives, and bee pollination control devices. Patentees came from a number of provinces and cities, with Beijing, Zhejiang, and Shandong ranking in the top three. Between 2000 and 2007 a total of 15 patents were granted, and between 2008 and 2013 the total was 39. Patents related to bee pollination are clearly on the increase.
From the National Network of Scientific and Technological Achievements we retrieved 41 classes of bee pollination, principal among which were 17 classes on bee species breeding and selection accounting for 41.5 of total results. In addition, there were classes covering bee application and technology research (14), beehive design (2), and pollinating bee species resources (3). The results show that of the pollinating beesbumblebees, osmia bees, and leafcuttersbumblebee research was the most impotant. From the point of view of achievements, institutes in Beijing, Jilin, and Shanxi were in the top three. Regarding the number of achievements the Beijing Forestry Academy of Sciences, the Chinese Academy of Agricultural Sciences Institute of Bees, and the Horticulture Institute of the Shanxi Academy of Agricultural Sciences were in the top three. The Beijing Academy of Agriculture and Forestry made great progress in providing facilities for crop pollination, bee species breeding, utilization, demonstration, and pollination hive development. The Chinese Academy of Agricultural Sciences Institute of Bees made a breakthrough in bumblebee breeding, utilization, and application. The Horticulture Institution of the Shanxi Academy of Agricultural Sciences had a lot of success as a result of providing improved facilities for vegetable production technology research and application.
3.2. Effectiveness evaluation of bee pollination for fruit trees
After the bee
After using
In addition, the effect of using a variety of bees for pear and peach pollination was clear. Liu Jinli et al. increased the fruit yield of crown pears, emerald pears, south fruit pears, and gold pears by using concavelipped osmia for pollination by 11 to 18.4 compared with that of artificial pollination[25]. Guo Yuan et al. researched different pollination methods for pear and found that the fruit yield of bee pollination was 32.9, artificial pollination 13.05, and natural pollination only 2.83[26]. Dong Jie et al. used Italian bees and
From 2008 to 2015, researchers from the Horticultural Institute of the Shanxi Academy of Agricultural Sciences carried out research into bee pollination for the Red Fuji apple; the results show that bees can significantly improve the fruitsetting rate (table 2).
Variety | Pollination pattern | Flower number | Fruit number | Fruitsetting rate () |
---|---|---|---|---|
Bee | 1004 | 240 | 23.9 | |
Nature | 1044 | 96 | 9.2 | |
Bee | 1258 | 438 | 34.8 | |
Nature | 1098 | 93 | 8.5 |
In addition, three, five, seven, and nine lots of bee pollination resulted in increased fruit yield to the tune of 11.1, 19, 21.7, and 25, respectively, as shown in figure 5. So the greater the number of visits made by bees to pollinate the higher the fruit yield.
Bee pollination stimulates the growth of young fruit. The average yield of each tree after bee pollination was 69.8 kg compared with 31.9 kg of natural pollination. The fruit shape index of bee pollination and natural pollination were similar, but the coloring index of bee pollination was significantly better than the natural pollination group; the results are shown in table 3.
Pollination pattern | Fruit shape index | Color index () | Chemical quality | ||
---|---|---|---|---|---|
Solid content () | Acidity () | TSS:acid ratio | |||
0.8282 | 67.33 | 13.531.63A | 0.340.05B | 40.98 A | |
0.8516 | 47.33 | 13.931.34A | 0.430.07A | 32.71 B |
3.3. Key technology underlying bee pollination of apples and pears
3.3.1. Configuration of pollination trees
About 70 of trees under production in orchards in Shanxi receive insufficient or no pollination. We have researched the ratio between pollination partners and the cultivation of fruit trees. In some pear gardens, pollination branch grafting guarantees bee pollination. Research shows that selfincompatibility occurs when pear trees have the same Stype genotypes, hence cultivation of at least one S genotype of different varieties as pollination partners should be undertaken. Table 4 outlines the main culture of some varieties and their appropriate pollination partners.
Main varieties | Pollination partners |
---|---|
P. |
|
Rehd. Rehd. |
|
Rehd. |
|
Max., |
|
Rehd. |
|
Rehd. |
The ratio between pollination partners and the main variety can be 1:41:8; 1:6 has been found to be optimal. To ensure full pollination and prevent flowering inconsistency the main variety should be paired with two pollination partners; namely, six main varieties and one pollination variety.
In addition, we can increase the supply of pollen by means of grafting pollination branches (figure 6).
3.3.2. Selection of pollinating bee species
Figure 7 shows that the outflying temperature of
The weight of total pollen and pear pollen collected by bees in one hour was compared and analyzed (figure 8).
The proportion of pear pollen collected by
Since pear trees bloom throughout China at different times, there is a need for pollinating bees that are not only good at pollen collection but adapt well to the environment. Pear trees flower early when the temperature is low, so bees have little choice but to pollinate pear trees in low temperatures. Of the nine species of bees selected,
3.3.3. Control of pollination bees
Insect pollination can be used to improve the fruitbearing rate and yield, but it does not follow that the higher the fruitbearing rate the better the yield. If the fruitbearing rate is too high, nutrients will be depleted resulting in smallsized fruit and poor yield. Therefore, the key technical problem is to adjust the number of bees to control the fruitsetting rate.
Table 5 shows that the greater the varieties of bees the greater the subsidence on stigma pollen, the higher the fruitsetting rate, and the greater the yield. The fruitsetting rate is low with one to four varieties of bees; however, when the varieties of bees are increased to six or eight there could be an increase to 9.6 or 17.9, respectively. In addition, using different varieties of pollination bees can also affect the quality of apples (table 6). When six varieties of pollination bees were employed the fruit not only met the appropriate requirements but tasted good too. All in all, when the ratio between pollination partners and main varieties is 1:4, each tree can meet production requirements with six bees.
Number of bee varieties used | Pollen amount on stigma | Fruitsetting rate () | Average yield/each tree (kg) |
---|---|---|---|
678.52 | 2.87 | ||
832.08 | 3.07 | ||
1,112.9 | 3.31 | ||
1,145.8 | 9.63 | ||
Number of bee varieties used | Soluble solids () | Acid () | Hardiness in the sun (N/cm2) | Hardiness in the shade (N/cm2) |
Fruit shape index | TSSacid ratio |
---|---|---|---|---|---|---|
1 | 15.0527bc | 0.302d | 9.154b | 9.24b | 86.44 | 49.79 |
2 | 14.8423c | 0.318cd | 10.809a | 10.72a | 87.81 | 46.7 |
4 | 15.9480ab | 0.3906b | 10.509a | 10.23a | 86.96 | 40.82 |
6 | 16.6893a | 0.502a | 10.46a | 10.31a | 88.49 | 33.25 |
8 | 15.6733bc | 0.375bc | 9.485b | 8.73b | 85.65 | 41.78 |
When the ratio between the main variety of “Red Fuji” apples and pollination partners of “Qinguan” is 20:1, the fruit yield, fruit shape index, seed number, and deformity fruit rate of each tree employing 6, 12, and 18 varieties of bees are, respectively, shown in figure 10, table 7, and table 8. Notes: Means within a column followed by the same letter are not significantly different.
Number of bee varieties used (each tree) | Average longitudinal diameter (mm) |
Average diameter (mm) | Fruit shape index |
---|---|---|---|
6 | 66.41 | 75.26 | 0.91110.0103a |
12 | 68.2 | 75.21 | 0.90760.0094a |
18 | 67.65 | 74.28 | 0.88210.0121a |
Number of bee varieties used (each tree) | Total number of seeds |
Plump seed | Plumpness () | Irregular fruit rate () |
---|---|---|---|---|
6 | 140 | 134 | 95.7 | 56a |
12 | 247 | 243 | 98.38 | 26b |
18 | 290 | 288 | 99.31 | 18c |
In the absence of pollination partners the number of bee varieties used for pollination and the fruitsetting rate are shown in figure 11.
The configuration of pollination partners is a major factor affecting the number of bee varieties to be used for pollination. A good configuration will allow employment of six varieties of pollination bees, enough to guarantee production requirements. If the configuration leads to insufficient pollination partners, it will be necessary to increase the number of varieties of bees to at least 12 for pollination purposes. In the absence of pollination partners, 16 varieties of bees will be needed to achieve a fruitsetting rate of 9.12.
3.3.4. Scale of the pollination apiary
The distance between buzzers and fruit trees had a significant effect on pollination. Foraging bees and fruiting percentage at different distances using 20 colonies are shown in tables 9 and 10.
Distance (m) | Number of foraging bees | Flower number | Fruit number | Fruiting percentage |
---|---|---|---|---|
354 | 715 | 138 | 19.30 | |
246 | 610 | 94 | 15.41 | |
227 | 764 | 97 | 12.70 | |
194 | 935 | 112 | 11.98 | |
86 | 1,825 | 126 | 6.90 |
Distance (m) | Flower number | Fruit number | Fruiting percentage | Pollen amount on stigma |
---|---|---|---|---|
1,723 | 286 | 16.6 | 6,050 | |
1,843 | 304 | 16.49 | 5,450 | |
3,090 | 417 | 13.5 | 6,889 | |
1,738 | 228 | 13.12 | 5,850 | |
1,790 | 202 | 11.28 | 6,050 |
With increase of the distance between fruit trees and bee colonies the number of foraging bees gradually reduced. Bee pollination at a distance of 150 m between bee colonies and fruit trees was found to give the ideal fruiting percentage; therefore, the bee pollination effective radius was 150 m when 20 colonies are employed.
With increase of the distance in the 0 to 200m range using 20 colonies the fruiting percentage decreased from 16.60 to 11.28; however, neither the trend nor change in the pollen count on the stigma were obvious. Despite there being more foraging bees and the fruiting percentage increasing with decrease in the distance from the colony within the 0 to 200m range, 2010 was an offyear with low apple tree yield, reduced flower total quantity, and enlarged bee gather distance.
The number of foraging bees and fruiting percentage at different distances using 50 colonies are shown in tables 11 and 12.
Distance (m) | Number of foraging bees | Flower number | Fruit number | Fruiting percentage |
---|---|---|---|---|
907 | 1,070 | 339 | 31.68 | |
593 | 1,775 | 236 | 13.30 | |
600 | 1,250 | 140 | 11.20 | |
342 | 1,865 | 208 | 11.15 | |
262 | 1,400 | 148 | 10.57 | |
241 | 1,255 | 70 | 5.58 | |
189 | 1,580 | 97 | 6.14 |
Distance (m) | Flower number | Fruit number | Fruiting percentage | Pollen amount |
---|---|---|---|---|
1,561 | 309 | 19.8 | 5,400 | |
592 | 93 | 15.71 | 5,050 | |
1,200 | 135 | 11.25 | 5,167 | |
1,425 | 203 | 14.25 | 4,800 | |
1,097 | 215 | 19.60 | 4,000 | |
1,373 | 202 | 14.71 | 4,000 |
With increase of the distance in the 0 to 300m range using 50 colonies, in 2009 fruiting percentage decreased from 31.7 to 6.1, fruiting percentage at 200 m was 10.2, and fruiting percentage at 250 m was 5.6; therefore, the bee pollination effective radius was 200 m when 50 colonies are employed. In 2010, apple pollen counts on stigmas overall declined with increasing distance. This shows that foraging bees were fewer with increasing distance, yet fruiting percentage showed no significant change in trend.
The bee pollination effective radius was 150 m with 20 colonies and 200 m with 50 colonies. When apple trees gave onyear yields, production practice chose 50 colonies for bee pollination. When apple trees gave offyear yields the bee pollination effective radius was larger than apple trees in onyear yields and production practice chose 20 colonies for bee pollination.
3.3.5. Technology behind getting bees to visit fruit trees
The attraction of pollinators to some fruit trees is poor; one such is pear. When there are other plants such as rape, dandelion, and paulownia flowering near the target trees at the same time, foraging insects rarely alight on pear trees[29]. Artificially inducing bees to pollinate fruit trees when more desirable plants are available is a problem that must be solved. Many fruit trees bloom early in the year and flowering time is short; for example, apple trees flower for between 10 and 15 days and pear trees flower over a shorter period (about 710 days). Another technical difficulty is activating the foraging enthusiasm of the swarm.
In an effort to improve the foraging enthusiasm of bees, our team studied foraging behavior after using attractants.
The weight of pear pollen load collected in a day is shown in figure 12. All treatments enhanced the foraging ability of bees for pear pollen. The foraging effect of hanging attractant I in hives (77.56 1.59 g/group) was significantly higher than other treatments. Those treatments that involved feeding the bees Arg (62.05 / 2.01 g), Lys (62.2 2.3 g), 8BrcGMP (64.45 4.55 g) and hanging attractant II in hives (64.20 2.72 g) were better than the control treatment (49.11 1.03); other treatments showed no significant difference from the control treatment.
Pear pollen was sorted from total pollen. The percentage of pear pollen in total pollen load collected in a day is shown in figure 13. The results show that treatment groups fed pear syrup and methionine showed no significant difference from the control group; the other seven groups were higher than the control group. Feeding lysine (76.3), hanging attractant I in the hives (79.3), and hanging attractant II in the hives (80.2) were all significantly higher than other treatment groups (
Cameras were installed at the entrance to the hive, worker bees returning to the hive were recorded for 5 minutes every hour. The percentage of foraging bees on pear flowers out of total foraging bees is shown in figure 14. The results showed that treatment groups fed pear syrup, gallic acid, and methionine were significantly lower than the control group, whereas the group fed arginine and 8BrcGMP showed no significant difference from the control group. The groups fed lysine (85.81), hanging attractant I (86.74), attractant II (87.27), and attractant III (85.67) were significantly higher than the control group. The percentage of foraging bees improved by 3 to 4.5 after application of attractants I, II, and III.
The above results show that feeding bees lysine brings about the best effect of all the feeding treatments, increasing both the percentage of pear pollen load and the number of foraging bees on pear flowers. The effect of hanging attractant in the hives is better than feeding treatments. Hanging attractant II in the hives resulted in the highest percentage of pear pollen load, whereas hanging attractant I in the hives resulted in the highest weight of pear pollen. Both treatments can effectively increase foraging behavior.
3.3.6. Technology underlying bees carrying pollinizer pollen
Since some pear orchards have no pollinizers whatsoever, we developed a kind of beecarrying powder device (figure 15). This device is installed at the entrance to the hive, fresh pollen is put in the upper part of the device, and pollen will leak out from the bottom when bees leave the hive. Bees that carry pollinizer pollen will pollinate leading cultivars.
4. Industrialization of fruit tree pollination
4.1. Professional bee breeding for pollination
4.2. Induced bee pollination technology: The need for further research
Researchers have cultivated a special colony used exclusively for fruit tree pollination, developed a pollination technology that does not depend on a queen bee, and solved the bee-butting-greenhouse problem in facilities crop . Although many advances have been made in bee pollination, There are remain many technical problems that must be solved such as how to get bees to visit fruit trees they do not favor or how to get the bees to improve pollination? Answers to these questions involve the study of the correlations between plants and bees, as well as the relationship between the spatial layout of fruit trees and the spatial distribution of foraging bees.
4.3. Pollination professional development is slow
At present, some areas in China have established bee pollination intermediary service agencies, bee industry cooperatives, pollination professional companies, and a few corresponding pollination intermediary services. However, these organizations have failed to provide the necessary market supplyanddemand information and technical training, or to set up a bee pollination service and relevant policies. There are a number of reasons for this: The scale of the industry in China is small, specialist companies are few in number, the degree of organization is low, and it is difficult to form a pollination network.
Acknowledgments
We are grateful to Professor Liu Fanglin from the Hefei Institute of Material Science, Chinese Academy of Sciences for modifying and improving the manuscript.
References
- 1.
Zhang YX (Ed.) General fruit cultivation. Beijing: China Agriculture Press; 2014. - 2.
State Statistics Bureau, (Ed.) Statistical year book of rural China in 2012. Beijing: Chinese statistics press; 2012. - 3.
Available from: http://faostat.fao.org/browse/QQC/E - 4.
Guo GN, Yan ZL, Zhang HT, et al. Current situation of production of early and mid season apple cultivars in China and progress in breeding for early and mid season apple cultivars. Journal of Fruit Science. 2009; 26 (6):871–877. - 5.
Chen CG, Zhao DY, Xuan JH. The suggestion to apple varieties development in our country. Northern Fruits. 2015; xx (3):52–53. DOI: 10.16376/j.cnki.bfgs.2015.03.027 - 6.
Ou XQ, Zhou Y. The analysis of concept of plants self‐pollination and cross pollination. Biology report. 2007; 42 (11):23–25. - 7.
Roubik DW. Pollination of cultivated plants in the tropics. FAO Agricultural Services Bulletin. 1995; 118 :1–196. - 8.
Roubik DW (Ed.) Diversity in the real world: Tropical forests as pollinator reserves. In: Bees and the Environment (ed. Mardan M). Malaysia: South Bound Press; 1995. - 9.
Shen JS, Wu WQ, Song HL, et al. The study of pollinating insects and their flower‐visiting behavior on Malus pumila Mill. Journal of Environmental Entomology. 2015;37 (4):720–725. DOI: 10. 3969 /j. issn. 1674‐0858. 2015. 04. 4 - 10.
Lu YG, Qi WZ, Zhang SW, et al. Observational study on the insect visiting apple flowers in the central loess plateau petitions. Apiculture of China. 2012; 63 :27–29. - 11.
Yang LL, Wu YR. The preliminary research on the kiwi pollinator. China apiculture. 1990;( 3 ):2–4. - 12.
Zhang YY, Wu WQ, Ma WH. The Investigation of Cherry Pollinator. Chinese Agricultural Science Bulletin. 2012; 28 (25):272–276. - 13.
Li J, Zhu CD, Wang FH, et al. Current research on the status of wild bees and their pollination roles. Biodiversity Science. 2007; 15 (6):687–692. DOI: 10.1360/biodiv.070080 - 14.
Xie ZH, Xu HL, Yang P. Notes on monitoring, assessing and conserving pollinator biodiversity. Chinese Journal of Applied Entomology. 2011; 48 (3):746–752. - 15.
Huang DY, Hao JS, Yu JF, et al. Impact of Human Activities on Pollination of Economic Crops. Nonwood Forest Research. 2008; 26 (4):114‐120. - 16.
Steffan‐Dewenter I, Potts SG, Packer L. Pollinator diversity and crop pollination services are at risk. Trends in Ecology and Evolution. 2005; 20 :651. - 17.
Kearns CA, Inouye DW, Waser NM. Endangered mutualisms: The conservation of plant–pollinator interactions. Annual Review of Ecology and Systematics. 1998; 29 :83–112. - 18.
Wu WQ, Guo Y, Shen JS, et al. Present situation investigation of bee pollination for pear. Apiculture of China. 2011; 62 :40–44. - 19.
Li MH, Cong B, Li JP, et al. Mason Bee and Its Application on Fruit Tree Pollination. Journal of Jilin Agricultural University. 2004; 26 (4):422–425. - 20.
Zhang GQ, Tian ZZ, Shen RM, et al. The effect of Apis mellifera pollination for Fuji and golden apple. Agricultural science technology and information. 2013;xx (1):23–25. DOI:10.15979/j.cnki.cn62‐1057/s.2013.01.025 - 21.
He WZ, Zhou WR. The effect of Osmia excavata Alfken,Apis mellifera and artificial pollination for apple. Apiculture of China. 2009;60 (11):9–11. - 22.
Lou DL, Jiang FT, Wang SQ. Study on for [ sic ] Apple Bee Pollination. Apiculture of China. 2013;64 :35–37. - 23.
Zhang ZH, Yang PY, Li P, et al. The integrated application and demonstration effect of bee pollination and green early prevention and control production technology. China Plant Protection. 2015; 35 (4):43–45. - 24.
Yuan F, Wei YP, Zhang YL. Research on the result of pollination of apple by Osmia bees. Acta Agriculturae Boreali‐occidentalis Sinica. 1992;1 (3):93–96. - 25.
Liu JL, Cui LX, Le WQ. The pollination effect of Osmia excavata Alfken for different varieties of pear tree. Hebei Fruits. 2014;xx (1):44 –45. - 26.
Guo Y, Shao YQ, Ma WH, et al. Study on Physiological Activity and Pollination Characteristic of Stigma and Pollen of ‘Dangshansuli'. Chinese Agricultural Science Bulletin. 2013; 29 (16):110 –114. - 27.
Dong J, An JD, Huang JX, et al. Effects of pollination by different bees on peach fruit development and quality under greenhouse conditions. Chinese Journal of Eco‐Agriculture. 2011; 19 (4):836-842. - 28.
Mu HJ, Sun ZP, Zhang SH, et al. The test of bumblebee pollination for facilities fruit trees. Hebei Fruits. 2006; xx (6):6–7. - 29.
Teng TZ, Huo YG, Li Y. The relationship of pear fertilization and bee pollination. Apiculture of China. 2011; ZA :19–21. - 30.
Peng WJ, Wu J, An JD, et al. Comparative studies on pollination biologies of Bombus lucorum andApis mellifera ligustica in Katy apricot greenhouse. Journal of Fujian Agriculture and Forestry University (Natural Science Edition). 2007;36 (3):302–306. - 31.
Wu J, Shao YQ (Eds.) Wonderful efficient crop production technology—honeybee pollination. Beijing: China Agriculture Press; 2011.