**Fruit Tree Pollination Technology and Industrialization in China**

Guo Yuan, Ma Weihua, Wu Wenqing and Song Huailei

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/62854

#### **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 domesticat‐ ed 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 *Apis mellifera*. The most prominent example can be found in southwest China where the cultivated area devoted to apple and pear trees is being expanded year by year, but at the cost of decrease in the number of wild pollinators because of environmental degradation, air pollution, pesticide usage, and so on. This means that crops cannot get sufficient pollina‐ tion. Those places where there is a serious shortage of pollinators even make use of manpow‐

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er to replace insect pollination, which increases the cost of production dramatically. To reduce the cost of pollination and improve the efficiency of pollination, this study looks at how best to get bees to pollinate apple and pear trees, including such factors as how to attract bees to pollinate, selection of optimum bee species, and optimum bee configuration. The work provides a basis for the application of bee pollination technology for crops.

## **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 cultiva‐ tion 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, *Phyllanthus emblica* (Indian gooseberry), banana, pineapple, durian, mangosteen, breadfruit, cocoa, and betel nuts, the majority of which are widely distributed throughout China. The area devoted to fruit cultivation and fruit yield are among the highest in the world.

Apple trees have a wide distribution in China, can be evergreen or deciduous, and are widely grown across the Yunnan–Guizhou 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].

**Figure 1.** Distribution of fruit trees in China.

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 Yunnan– Guizhou Plateau. They too can be evergreen or deciduous. They can be broken down into evergreen and deciduous mixed, temperate deciduous, dry‐temperature 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 envi‐ ronment, 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 cross‐pollinated 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 apple‐producing 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 (An‐ thophoridae), leafcutting bees (Megachilidae), an andrenid bee (Andrenidae), and a dipteran (Diptera, Syrphidae). Among them, the Italian bee (*Apis mellifera ligustica*), which accounts for 61.5 to 99.4% of pollinators, is the apple's main pollinator. The foraging peaks of the Italian bee and *Anthophora plumipes* (Pallas, 1772), another local pollinator known as the hairy‐footed flower bee, stagger, reducing competition between each other[9]. Lu Yanguo et al. visited insect‐ pollinated apple blossom in central and southern loess plateau regions. The results show that the bee is the main pollinator in Tianshui and Liangdi, where it accounted for 92.6 and 60%, respectively, of all insect pollination[10]. Yang and Wu surveyed the number and species of insects pollinating kiwi fruit flowers. They identified 16 species of pollinator, including bees (11), food aphid flies (4), and a dung beetle (1). Statistical analysis of the pollination behavior and pollination frequency showed that the bee *Apis cerana cerana* and the Italian bee are the best pollinators, with other insects much less active, carrying less pollen, and having much less of an impact[11]. Zhang Yunyi et al. investigated species of pollinators and the quantity of large cherry trees in Shanxi, and found that hymenopterans accounted for 64.83 to 74.81% of the pollinators. Hymenopteran pollinators are the most important. Interestingly, pollinators in mountainous area are richer in species than those in the plain[12].

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, large‐scale 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].

**Figure 2.** Artificial pollination.

## **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**).

**Figure 3.** Literature about bee pollination from 1980 to 2011.

**Figure 4.** Bee pollination literature by research content.

Between 2001 and 2011, nine books were published on insect pollination technology research and application (**table 1**).


**Table 1.** Monographs on bee pollination in China.

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 bees—bumblebees, osmia bees, and leafcutters—bumblebee research was the most impotant. From the point of view of achieve‐ ments, 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, demon‐ stration, 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 *Osmia cornifrons* (Ra doszkowski) was imported by the Biological Control Research Institute of the Chinese Academy of Agricultural Sciences from Japan in 1987 the pollination effectiveness of the fruit‐setting rate and fruit quality of apricot, cherry, peach, pear, and apple in Hebei and Shandong were remarkable.

After using *Apis mellifera ligustica* for apple pollination, Zhang Guiqian et al. found that, compared with natural pollination, bee pollination increased the "Red Fuji" apple fruit yield by 46.8%, reduced the misshapen fruit rate by 22.4%, and increased yield to 14,124 kg/hm2 [20]. He Weizhi and Zhou Weiru researched the use of the concave‐lipped bee *Osmia excavata* Alfken, the Italian bee, and artificial pollination for "Red Fuji" apple pollination. The results showed the apple fruit yield of the six kinds of pollination was significantly higher than that of natural pollination; the pollination effect of osmia bees combined with Italian bees was best with a high inflorescence fruit rate of 99.6% [21]. Lou Delong et al. found that the "Red Fuji" apple fruit yield, production, and coloring index of bee pollination were higher than those of natural pollination by 15, 36.26, and 17.07%, respectively[22]. Using bee pollination for apple and pear, Zhao Zhonghua et al. found that fruit yield was more than 20% higher than artificial pollination and the average production of each acre was 224.4 kg, 335.3 kg with the increase rate of 8.7% and 11.3% [23]. Yuan Feng et al. used osmia bees and honeybees to pollinate "Red Fuji" apple trees and found that fruit yield increased by 14.68 and 10.95%, respectively, over the natural pollination yield and the fruit abscission rate reduced by 32.9 and 20.27%, respec‐ tively[24].

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 concave‐lipped 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 *Bombus hypocrita* to pollinate peach trees; the results showed that any difference in peach fruit yield and fruit nutritional quality of the two kinds of bee pollination was not significant and that both were significantly better than that of artificial pollination[27]. Mu Hongjie used bumblebees and bees to pollinate fruit trees; the results showed that the fruit yield of bumblebee pollination was higher than that of bee pollination, with an increase of 25.5% in the nectarine yield[28]. Means within a column followed by the different letters are extremely significant different at P 0.01 level.

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 fruit‐setting rate (**table 2**).


**Table 2.** Fruit‐setting rate by bee and natural pollination.

**Figure 5.** Fruit‐setting rate by number of pollination visits.

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**.


*Notes:* Fruit shape index: The ratio of longitudinal diameter to transverse diameter. Color index=Σ(Fruit number of each class×Extreme value)/(Total fruit number×The highest series)×100%. TSS, total soluble solids.

**Table 3.** Different pollination patterns.

## **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 pollina‐ tion. 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 self‐incompatibility occurs when pear trees have the same S‐type 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 polli‐ nation partners.



**Table 4.** Configuration of main pear variety and appropriate pollination partners in Shanxi.

The ratio between pollination partners and the main variety can be 1:4–1:8; 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**).

**Figure 6.** Central branch grafting of pear pollination partners.

## *3.3.2. Selection of pollinating bee species*

*Apis mellifera* cv. "Kaqian Black Ring Bee", *Apis mellifera* cv. "Mr. Northeast Black Bee", *Apis mellifera caucasica*, *Apis mellifera* cv. "Honey‐proplis 1 Bee", *Apis mellifera* cv. "Carpathian Bee", *Apis mellifera* cv. "Heimeiyi", *Apis mellifera carnica*, the Italian bee, and *Apis cerana cerana*

**Figure 7.** Temperature of outflying and backflying bee varieties.

Fabricius were usually used for pollination. However, the nine varieties differ in their life habits (**figure 7**), their ability to carry pollen (**figure 8**), and their collection of pear flower powder proportion (**figure 9**). Therefore, in the process of pollination we need to choose appropriate bees for pollination according to different fruit trees.

**Figure 7** shows that the outflying temperature of *Apis cerana cerana* Fabricius was 8.2°C, which was significantly lower than western bees (9.2– 10°C). *Apis mellifera carnica* can fly out of the nest at 9.2°C; there were no significant differences among western bees. The average backflying temperature of all bee species was 12.1°C and the average pollen‐carrying temperature of *Apis mellifera* cv. "Kaqian Black Ring Bee", *Apis mellifera* cv. "Northeast Black Bee", *Apis mellifera* cv. "Honey‐proplis 1 Bee", *Apis mellifera carnica*, and *Apis cerana cerana* Fabricius was significantly lower than *Apis mellifera caucasica* and the Italian bee.

The weight of total pollen and pear pollen collected by bees in one hour was compared and analyzed (**figure 8**). *Apis mellifera carnica* collected more pollen than the others, and *Apis cerana cerana* Fabricius collected the least. *Apis mellifera* cv. "Kaqian Black Ring Bee" collected the most pear pollen in one hour and *Apis mellifera* cv. "Honey‐proplis 1 Bee" and *Apis cerana cerana* Fabricius collected the least pear pollen. *Apis mellifera* cv. "Kaqian Black Ring Bee" and *Apis mellifera carnica* were much the same but they both collected more pear pollen than the others. They can collect five times more pear pollen than *Apis cerana cerana* Fabricius.

**Figure 8.** Total pollen and pear pollen collected by different bee varieties in one hour.

The proportion of pear pollen collected by *Apis mellifera carnica* was highest (45.2%) and *Apis mellifera* cv. "Kaqian Black Ring Bee" was the second highest (42.4%). Nevertheless, there was no significant difference among the species (**figure 9**).

**Figure 9.** Pear pollen collected by different bee varieties.

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, *Apis mellifera* cv. "Kaqian Black Ring Bee" and *Apis mellifera carnica* adapted best to the environment and were best at collecting pollen, especially pear pollen. So they can be recommended to pollinate pear trees.

#### *3.3.3. Control of pollination bees*

Insect pollination can be used to improve the fruit‐bearing rate and yield, but it does not follow that the higher the fruit‐bearing rate the better the yield. If the fruit‐bearing rate is too high, nutrients will be depleted resulting in small‐sized fruit and poor yield. Therefore, the key technical problem is to adjust the number of bees to control the fruit‐setting rate.

**Table 5** shows that the greater the varieties of bees the greater the subsidence on stigma pollen, the higher the fruit‐setting rate, and the greater the yield. The fruit‐setting 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.


*Notes:* Experiments were conducted in net houses. The ratio between pollination partners and main varieties is 1:4.

**Table 5.** Stigma pollen count, fruit‐setting rate, and yield employing different numbers of varieties of pollination bees.


Note: TSS, total soluble solids. Means within a column followed by the different letters are significantly different at P 0.05 level.

**Table 6.** Fruit quality employing different numbers of varieties of pollination bees.

**Figure 10.** Number of varieties of pollination bees employed and fruit‐setting rate.

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.


**Table 7.** Relation between number of varieties of pollination bees employed and fruit shape index.


**Table 8.** Relation between number of varieties of pollination bees and fruit seed number and irregular fruit rate.

In the absence of pollination partners the number of bee varieties used for pollination and the fruit‐setting rate are shown in **figure 11**.

**Figure 11.** Fruit‐setting rate of "Red Fuji" apple trees by bee pollination in the absence of pollination partners.

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 fruit‐setting 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**.


*Notes:* 20‐colony treatment involved setting up 5 survey spots, 1 every 50 m from the colony out to 300 m. At every spot one apple tree of consistent variety, tree potential, on‐year yield (high), and off‐year yield (low) was selected. At every spot foraging bees were counted for 45 minutes and the fruiting percentage after 15 days was calculated.


**Table 9.** Number of foraging bees and fruiting percentage at different distances using 20 colonies in 2009.

**Table 10.** Fruiting percentage at different distances using 20 colonies in 2010.

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 200‐m 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 200‐m range, 2010 was an off‐year 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**.


*Notes:* 50‐colony treatment involved setting up 7 survey spots, 1 every 50 m from the colony out to 300 m. At every spot one apple tree of consistent variety, tree potential, and on‐year and off‐year yields was selected. At every spot foraging bees were counted for 45 minutes and the fruiting percentage after 15 days was calculated.


**Table 11.** Foraging bees and fruiting percentage at different distances using 50 colonies in 2009.

*Note:* There were no 150‐m data because tree vigor was poorer.

**Table 12.** Fruiting percentage at different distances using 50 colonies in 2010.

With increase of the distance in the 0 to 300‐m 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 on‐year yields, production practice chose 50 colonies for bee pollination. When apple trees gave off‐year yields the bee pollination effective radius was larger than apple trees in on‐year 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 7–10 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. *Apis mellifera* 30 hives with six combs every hive had a consistent colony structure. The test involved 10 treatments and 3 colonies. Three treatments, respectively, used attractant I, II, and III, which our team prepared. Nine treatments involved feeding six compounds to bees: 1‐mM methionine, 1‐mM lysine, 1‐mM arginine, 1‐mM gallic acid, 500‐ μM 8‐Br‐cGMP, and pure syrup as a control treatment. Attractants were start‐fed to *Apis mellifera* once every evening before the pear blossom appeared and then every 2 days until the end of the flowering. Pear flower load after sorting from total pollen was weighed, number of foraging bees on pear flowers were recorded, and percentage pear flower load and foraging bee number on pear flowers were calculated.

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), 8‐Br‐cGMP (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.

**Figure 12.** Weight of pear pollen collected in a day.

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 (*P* < 0.05). Hanging attractant II in the hives was the most effective and had the highest percentage of pear pollen; hanging attractant I in hives coupled with the lysine groups was the next best.

**Figure 13.** Percentage of pear pollen in total pollen.

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 8‐Br‐cGMP 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.

**Figure 14.** Percentage of foraging bees on pear flowers out of total foraging bees.

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 bee‐carrying 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.

**Figure 15.** Device for bees to carry pollen.

## **4. Industrialization of fruit tree pollination**

## **4.1. Professional bee breeding for pollination**

*Apis mellifera* and *Apis cerana cerana* are the foremost pollination bees, primarily employed for the production of bee products (like honey), although they are sometimes used to pollinate fruit trees. However, they are not ideal pollination bees[30]. In the 1990s, researchers in China made a breakthrough in the artificial breeding of wild bumblebees, mastered the key technol‐ ogy to breed bumblebees indoors, domesticated six kinds of bumblebees, and established several production bases that could be gradually applied to facilities for orchard pollina‐ tion[31]. In an effort to fill the gap in agricultural practical development needs, researchers have bred and domesticated osmia bees, stingless bees, and andrenids in recent years. Our hope is that these technologies might play an important role in fruit tree pollination in years to come.

## **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 beebutting-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 supply‐and‐demand 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 organi‐ zation is low, and it is difficult to form a pollination network.

## **Acknowledgements**

We are grateful to Professor Liu Fanglin from the Hefei Institute of Material Science, Chinese Academy of Sciences for modifying and improving the manuscript.

## **Author details**

Guo Yuan\* , Ma Weihua, Wu Wenqing and Song Huailei

\*Address all correspondence to: yysgy3@163.com

Horticultural Institute, Shanxi Academy of Agricultural Sciences

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## **Chapter 7**

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Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/62506

#### **Abstract**

The purpose of this study was to analyze the socioeconomic factors that influence the beekeeping process and describe the current situation in beekeeping technology development in the south and southeast regions of Jalisco. The study was conducted by reviewing secondary sources of documentary information and the primary information was obtained by means of a survey, analyzing demographic, social, technological, and economic variables. From January to April 2011, a stratified sampling was conducted of six strata of beekeepers, with a final sampling of 183 beekeepers. We applied a frequency analysis, ANOVA (Waller-Duncan), and contingency tables (χ<sup>2</sup> ). The average age observed for the beekeepers was 47 years, with fewer women participating in the activity, and an above national average level of education. The majority keep their apiaries in rented premises, a high percentage outside the municipality where they live. The honey obtained is multiflora and the main harvest is in the autumn, with a honey yield per hive below the national average. A number of problems affect the production sector including environmental factors, production costs, and varroa. We observed little diversification; in addition to honey only beeswax is recovered, and only a minority keep a record of production costs. There is wide participation in beekeeping associations and in training provided by different public and private bodies. There is a willingness to adopt new technologies and equipment for honey production with good practice standards.

**Keywords:** beekeepers, management, innovation, technology, socioeconomic aspects

## **1. Introduction**

Apiculture is a production area that has been carried out under a broad mosaic of systems and vertical and horizontal integration of the production process. It is an important activity in Mexico

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within the food, economic, social, and ecological areas and has developed in different parts of the country, through small and medium producers with an important share of the internation‐ al market and local consumption of 190 grams per capita during the nineties, increasing to 320 grams in 2010. This increase is because of its use as a raw material in the preparation of foods suchas yoghurt, cereals, confectionery, bakedgoods, andcosmeticproducts.[1]In2010,Mexico was the sixth largest honey producer in the world with 1.8 million hives producing 56,883 tons ayear,andthethirdlargestexporter,exporting25,000tonsthatsameyear,mainlytotheEuropean market,[2]positioningapicultureamongthetopthreesourcesofforeigncurrencyinthenational livestock field.[3] More than 2,400 tons of beeswax and close to 8 tons of royal jelly are pro‐ duced each year.[4] Apiculture directly benefits 400,000 people who form part of the beekeep‐ ing production chain by constructing beekeeping equipment and packaging and marketing honey and other bee products. In addition to benefiting agricultural crops through pollina‐ tion, with an estimated value of 2 billion dollars a year, beekeeping also helps to maintain the ecological balance in various ecosystems, through the pollination of wild plants.[5]

The state of Jalisco is one of the main honey producers in Mexico, with a census of 157,827 hives producing an average of 5,698 tons of honey per year between 2005 and 2009 and a 10% market share positioning it in third place nationally behind only Yucatán with close to 10,000 tons (15%) and Campeche with 7,500 tons (12.9%). There are almost 1,000 beekeepers in the state, of whom 50% are in the south and southeast, the main regions in this productive environment; the activity is mainly a sideline to agriculture and livestock.[1,6,7]

In recent decades, the beekeeping sector has faced substantial changes, the result of urbani‐ zation, globalization, and population growth, thus developing a new environment in itself.[8, 9] Actions have been taken to improve production, increase diversity in the end product, and try new schemes of organization, giving rise to new commercial dynamics and methods of insertion into the world market.[1] Government actions have focused on promoting productive restructuring, diversification of traditional crops, technological assessment, and the generation of infrastructure and technology innovation.[9,10]

Several studies have drawn attention to the fact that national apiculture is affected by a wide range of issues, including Africanized bees, global climate change (encompassing factors such as erratic rainy seasons, drought and extreme heat, and freezing temperatures), in addition to the lack of training and organization of beekeepers, and not least diseases such as varroa and foulbrood. Middlemen and competition on the international market have also contributed to a worrying instability.[3,6,11]

Honey was already shaping up with major annual sales projections until 2007.[12] This positive forecast has a growing international honey market as current production does not satisfy total demand.[13] However, marketing is another of the core problems within this production sector. In terms of product development, there need to be changes in the collection process, presentation, and business dynamic for it to be considered a primary activity and not just an additional source of income. In general, honey in Mexico is considered a by-product and few producers and companies have invested in research and development, conservation, and quality improvement, as well as differentiated forms of sale and marketing strategies and channels.[14]

Within Mexican apiculture, more than 75% of beekeepers are low-income farmers who see apiculture as a means of boosting their income; they have on average fewer than 100 hives,[6] numbers that are declining because of the problems already mentioned. The way these small producers carry out the activity does not follow business logistics, making it difficult to obtain reliable data regarding the income they perceive; they keep no records of production, spend‐ ing, or income.

Given the economic and social importance of apiculture in the south and southeast regions of Jalisco as already described, and a scenario of constant change, it is important to characterize beekeepers and agents of innovation taking into account socioeconomic, technological, and productive variables. Thus the aim of this work was to identify the influential socioeconomic factors within the beekeeping process and describe the current situation in the technological development of beekeepers in the south and southeast regions of Jalisco, to have an updated, objective view of the situation of the apiculture sector that allows the development of a frame of reference, a fundamental decision-making tool within government support programs for the benefit of beekeepers.

## **2. Materials and methods**

The documentary information was obtained from secondary sources to get a frame of reference about aspects of production and commercial statistical behavior of the apiculture production chain, as well as the methodological framework.

The study design is exploratory and quantitative. Exploratory investigation is used to define the study problem and its context through the analysis of secondary data. The quantitative investigation was descriptive and cross-sectional, applying a person-to-person nominal scale survey and a single sampling. The primary information was obtained by means of a survey using a structured questionnaire (See Appendix 1).[15,16] We analyzed demographic, social, technological, and economic variables, which included questions such as gender, age, how often hives were inspected, treatments for varroa, price of honey per kilo, apiculture products, type of extraction equipment, labeling, and marketing the honey, main diseases and their treatments, type of feed and frequency, extraction equipment and production costs, among others.[17]

A pilot survey was applied beforehand to 30 people to make adjustments to the final ques‐ tionnaire. A stratified sampling of beekeepers was made in six strata: 1 to 25 hives, 25 to 50 hives, 50 to 100 hives, 100 to 500 hives, 500 to 1,000 hives, and over 1,000 hives. From a population of 1,000 beekeepers in Jalisco, 50% live in the study zones, resulting in a population of 500 beekeepers. The final sampling was of 183 beekeepers surveyed, with a 95% confidence level, 3% accuracy, 5% participation, and sample size adjusted to 15% losses. For the data analysis we used a descriptive and quantitative method to identify, understand, correlate, and prove the hypothesis of the study. To analyze the information collected, it was processed using SPSS version 19® statistics software. We applied frequency analysis, ANOVA (WallerDuncan), and contingency tables (*χ*<sup>2</sup> ) to find whether or not there is an association between the social, economic, and technological profile variables in the apiculture production chain.

## **3. Results and discussion**

#### **3.1. Demographic aspects**

The majority (59%) of beekeepers in the study region manage fewer than 100 hives, although some were observed to have more than 1,000 hives ([**Figure 1**). The average age of the beekeepers in the study zone was 47 years for men and 45 years for women. Only 3% were younger than 20 years, and the beekeepers with most hives were also the oldest, evidence of the lack of interest in beekeeping among young people. In the peninsula of Yucatán, the average age is 47 years,18] unlike Michoacán where a 2004 study mentioned 43 years.[19,20] In contrast, on the island of Tenerife, Spain, the average age is reported as 59 years.[21] Age is an important factor to consider in terms of the present and future management skills of beekeepers; older beekeepers are less willing to change their traditional production methods and learn new production or management techniques. Likewise, working on projects with young beekeepers under 25–30 years increases instability because of temporary or definitive migration because of a lack of sources of work in the field or perhaps for reasons of study.[22]

**Figure 1.** Distribution of beekeepers by strata. (Livestock Research Laboratory, Department of Agriculture Production, CUCSUR, University of Guadalajara).

#### **3.2. Location of apiaries**

As far as access to land for beekeeping, there is a significant difference (*p* = 0.046, *χ*<sup>2</sup> ) where 61.2% of beekeepers rent the premises where they have their apiaries and the rest use small‐ holdings and, to a lesser extent, *ejido* or common ground. Beekeepers with 101 to 500 hives are more likely to rent, a similar situation to that reported in communities in Michoacán, where the majority of beekeepers do not own the premises where they set up their apiaries.[23] This situation limits apiculture development as producers must pay, either in cash or kind, for the lease of the lands, and also limits the assurance of the availability of the space to maintain the apiaries; this, in addition to competition for better spaces not only among beekeepers but also farmers and other branches of livestock. In Turkey, 90.59% of beekeepers have their apiaries installed on private property.[20]

Some 60% of beekeepers installed their apiaries in the municipalities where they were born and the rest look elsewhere for suitable flowering spaces, showing a significant difference (*p* = 0.000, *χ*<sup>2</sup> ) where beekeepers with more than 100 hives have greater mobility in search of better yields. They also mention a wide saturation of hives in their municipalities, this being another of the main issues raised within the beekeeping production system. This is related to the average distance of 25 km they have to travel to inspect the apiaries (in a range from 1 to 200 km), where a significant difference (*p* = 0.000, *χ*<sup>2</sup> ) was observed, beekeepers with less than 50 hives traveling less than 10 kilometers to install their apiaries, while those with over 500 hives travel distances in excess of 60 kilometers. Such a situation is unique to this region; a study in Chile describes a high concentration of apiaries in certain zones,[22] a fact that goes against the environmental management requirements for good farming practices. A different situation exists in Yucatán, where close to 50% of beekeepers travel more than 10 kilometers to reach the apiary, while 22.2% travel less than 2 kilometers, which leads to strong competition among the bees to obtain food, since 88.9% have apiaries at a distance of less than the recom‐ mended 3 kilometers.[24]

## **3.3. Months of honey production**

About 100% of the beekeepers refer to honey harvested is multiflora origin, since flowering of the area is varied in the area, and production depends on environmental conditions and the availability of floral resources producing pollen and nectar. The main honey harvest occurs in autumn; 30.1% of the beekeepers in the study area harvest in October, 74.5% harvest in November, the strongest month, and 48.1% in December. The secondary harvest, with less production, is done in the spring starting in March with 12%, rising to 27.9% in April, with a significant reduction in the activity in May with 11.5%.

The seasonality of honey production is marked at two different times of the year in most of the country, in the southeast and coastal regions it is obtained from March to May (springsummer), generating 40% of production. The second harvest is obtained in the Altiplano and north of the country between September and November (autumn-winter), obtaining the remaining 60% of production. Honey production in the Yucatán Peninsula occurs during winter and spring from December to June and comes from toothleaf goldeneye (*Viguiera dentata*), tzitzilché (*Gymnopodium floribundum*), and some vines (1, 25). In Michoacán, most beekeeping activity takes place in spring and summer (August and September), with the most significant peak during June. This variation in seasonality by zone around the country allows honey to be available throughout the year.

## **3.4. Problems in honey production**

There is a significant difference (*p* = .000, *χ*<sup>2</sup> ) among the complaints of beekeepers where those with more than 500 hives express the lack of available spaces for placing the apiaries; in recent years, new beekeepers have emerged who establish their apiaries less than 2 kilometers away, thus invading flowering spaces, which decreases production. Meanwhile, beekeepers with less than 500 hives give priority to environmental factors, mentioning situations of high defores‐ tation and fires, reduced and erratic seasons, the indiscriminate use of pesticides with the resulting damage to bee populations; followed by production costs, which have increased because of the high cost of sugar, one of the basic inputs, the purchase and exchange of queens because of Africanization, as well as the cost of the treatment of diseases, lack of support for the purchase of extraction equipment and hive management, and roads and tracks in poor condition, which affects the beekeeper going to inspect the hives, and the fact that where support does exist it is insufficient (**Figure 2**).

**Figure 2.** Problems facing beekeepers for honey production (Livestock Research Laboratory, Department of Agricul‐ ture Production, CUCSUR, University of Guadalajara).

As far as disease, attention is focused on the varroa mite to control the health problem. A similar situation is found in Yucatán, where beekeepers also complain of lack of training and unfav‐ orable market conditions, not unlike the situation in the study zone. This is in contrast to the problems described in Nigeria, where beekeepers are affected by theft of the hives, fires, abandonment of hives, lack of better technology, lack of technical assistance, and the aggres‐ siveness of the bees.[25]

#### **3.5. Bee products**

In the productive field, all (100%) beekeepers obtain conventional honey; in first place as an alternative product is beeswax, produced by 58.6%. This is followed in second place by nucleus colonies and propolis, and to a lesser extent, royal jelly, queens, and pollen, with little or no participation in the pollination process (**Table 1**). Although pollination is not a product but a service provided by apiculture, in many parts of the country it is an alternative source of income. In fact, in the states of Sinaloa, Chihuahua, and Coahuila, it is the main purpose of bee exploitation, honey production being a secondary activity,1] and in Michoacán pollination generates important economic income for 32.4% of beekeepers. In contrast, only 29.1% of beekeepers in Michoacán recover beeswax, whereas in the study zone this figure is more than double (58.5%).[19]


**Table 1.** Products other than honey obtained by beekeepers in the south and southeast regions of Jalisco (Livestock Research Laboratory, Department of Agriculture Production, CUCSUR, University of Guadalajara).

Although obtaining organic honey generates higher economic profits, it implies additional costs both for equipment and the necessary certification processes as well as the application of different production protocols to guarantee a product free of chemical substances. Organic bee farming also presents strategic technical challenges in training to obtain quality products and resource management for the acquisition of processing equipment and physicochemical product analyses which, when done professionally, make the activity more competitive. Organic honey is an area of opportunity for beekeepers in the study zone; the best price for organic honey may be 30% more than the price of conventional honey.[1,19] The obtaining of other products and pollination could improve the producers' income; however, these activities require the investment of more time and as this is not the main economic activity of more than 50% of the beekeepers in the study regions, further diversification is stifled and they remain within traditional exploitation with the production of primarily honey, beeswax, and bee nucleus colonies, which is contrary to the so-called integral exploitation.

#### **3.6. Economic aspects**

No differentiation is made in the management of the honey whether sold by the bottle or by the bucket as only 14% of beekeepers sell their products with a label. However, a 2012 study mentions that in Jalisco, sales of private label bottled honey are less than 1% of the production sold by those producers, an action that represents an important step toward the end consumer and the added value of the product.[26]

This form of commercialization has facilitated the sale of adulterated honey and even highfructose corn syrup as if it were honey, thus deceiving many people who purchase it believing it to be real honey at a very low price.[1] Limited classification of the product by color and/or flowering, bulk sale, and the lack of technology to enable value-added export position the honey industry as a commodity.[27]

In terms of the sale price per kilo of honey, a significant difference is observed in the analysis of variance Waller-Duncan of 0.000; beekeepers in strata 1 with up to 25 hives receive an average of 52.71 pesos while those in strata 5 with 501 to 1,000 hives receive 37.42 to 40 pesos. The trend observed is that the fewer the hives, the higher the sales price, which is because of the sale being made directly to the consumer while big producers sell their product wholesale and often receive a price close to 40 pesos per kilo (**Table 2**). In 2008, however, Jalisco was considered the best paid state, in that year receiving a price of 30.57 pesos per kilo, above the national average of 24.52 pesos. It should be noted that the price quadrupled in the decades from the nineties to 2008 going from 5.86 to 24.54 pesos nationally, which is attributed to the issues this production sector faces.19]


**Table 2.** Sales price of honey per strata in the south and southeast regions of Jalisco (Livestock Research Laboratory, Department of Agriculture Production, CUCSUR, University of Guadalajara).

As far as the export of honey, only 6.55% of beekeepers mention exporting honey to Germany. The beekeepers in strata 6 with more than 1,000 hives are the ones who export the most, there being a significant difference (*p* < 0.001 using *χ*<sup>2</sup> ) compared with strata 2 with 26 to 50 hives. One of the problems observed in the states in the study is that the production is bought by intermediaries who often pay for the harvest in advance and are responsible for positioning the product on the European market. This is a situation that prevails in countries such as Argentina, where it is reported that more than 95% of honey production is for exportation, and which is handled by only a few actors (three or four companies); the crucial points applied to exportation, such as quality control, storage, transport, and retail outlets form part of the marketing and supply strategies of the exporting companies in the area.[27]

Only around 30% of beekeepers know the quality standards required on the international market. Beekeepers in strata 4, 5, and 6 (more than 100 hives) are better trained in these aspects (*p* < 0.66, *χ*<sup>2</sup> ) compared with beekeepers with fewer hives, who also show little interest in the export process considering it to involve too much bureaucracy. Producers need to know the quality standards required by the international market, as well as packaging, packing, and prices be competitive.[28]

## **3.7. Honey marketing problems**

Close to 40% of beekeepers interviewed expressed problems in marketing the honey, and among the problems they face are low prices, mentioning that sometimes they recover only the production costs. Likewise, street vendors (carts) of adulterated honey at low prices have become unfair competition for beekeepers, as consumers have no knowledge of the quality and purity of the honey. A similar problem occurs in Argentina, where adulterated honey is rife on the local market. In addition, the abundance of red tape for exporting and the need for intermediaries demotivates producers from exploring the international market. In strata 1, 2, and 3 beekeepers express their concern about the low per capita consumption of honey, which only reaches 320 grams per year.[27]

Within the production process, 43.7% of those interviewed keep a record of production costs. It is mostly the beekeepers in strata 4, 5, and 6 (more than 100 hives) who carry out this activity to a significant extent (*p* < .028, *χ*<sup>2</sup> ). Similarly, Torres[22] observed in Chile that 50% of those interviewed said they did not maintain written accounts or sales records.

Of those beekeepers who do maintain records, not all were able to provide complete informa‐ tion, hence only 38.25% (70) of those interviewed were considered in the calculation of production costs, which include containers, treatments, gas, electricity, equipment repair and maintenance, vehicle maintenance, queen bees, beeswax, labor, feed (sugar, and others), protection equipment, and hive management equipment. In this area, there were significant differences (*p* < 0.43, Waller-Duncan) between the strata, observing that beekeepers with more than 500 hives (strata 5 and 6) have lower production costs (16.43 and 19.62 pesos, respectively), while beekeepers with less than 50 hives (strata 1 and 2) have higher production costs at 46.87 and 34.47 pesos, respectively. Lower production costs in strata with more hives may be directly related to the high volumes of inputs purchased to carry out the beekeeping activity and to group purchases to obtain better prices by buying wholesale.

The exploitation of bees that are more defensive, swarming, and evasive leads beekeepers to make changes in the way they are managed, such as relocating apiaries to more distant locations, thereby increasing the costs of transportation and labor (each worker manages fewer hives per day than when working with European bees), and also the protective equipment required against more defensive bees (coveralls and gloves),[29] and the purchase of queens, which before Africanization was minimal. In addition to this is the cost of bee feed, which in recent years has become one of the major costs, given the excessive increase in the price per kilo of sugar. It is estimated that production costs in managed colonies have increased around 30% in comparison with European bees[4] and because of treatments, particularly for the varroa mite*.* In spite of this, 66.6% of beekeepers believe bee farming is profitable. However, profit margins vary widely in a range from 5% to 200% as a consequence of such great differences between beekeepers.

## **3.8. Social aspects**

About 90% of beekeepers are members of a beekeepers association; 52% belong to 4 of the 11 associations registered in the study regions (Table 3).


**Table 3.** Participation in beekeeper associations in the south and southeast regions of Jalisco (Livestock Research Laboratory, Department of Agriculture Production, CUCSUR, University of Guadalajara).

A strategic challenge in the technology field is for small beekeepers to communicate clearly with research bodies, to generate a greater degree of professionalism and scientific rigor to meet the competitive challenges emerging in the industry; such communication is more feasible with producers who participate in organizational bodies. This is an important factor to push the competitive development of apiculture production units toward higher levels of social engagement for economic and productive purposes. It is also important to carry out coordinated actions to achieve a common goal, through the identification and planning of collective actions, and confront the control exerted by intermediaries, which would allow better prices for bee products and lead to the activity no longer being considered as merely for subsistence.[19,30]

Associated beekeepers in the study zones indicate that the support they have received from the association to which they belong consists of guidance for obtaining technical resources and training. Through the producers' alliance, they have been able to obtain government economic resources for the construction and equipping of extraction rooms based on the safety require‐ ments within the honey production process. Beekeepers have opted to associate in various ways to deal with their lack of resources and knowledge; however, the way in which they have become associated has often been linked to obtaining government support, as in the Yucatán Peninsula, beekeeping organizations and cooperatives facilitate the adoption of technology, equipment acquisition, storage, and sale of better quality honey, and are promoted by public institutions and civil organizations.[24]

Associative schemes, whether for productive or commercial purposes, are a valuable tool for beekeepers to achieve their objectives; however, these alone are no guarantee of success; any tool has advantages and disadvantages and being aware of these and analyzing them will avoid any false expectations.

Among the associated beekeepers, 26% think it is unnecessary to make any changes within the operation of the association; however, others mention that changes are required, such as better organization and integration among the members of the associations, referring to greater responsible participation of the assemblies. They also express the need for more resource management and technical support. Nevertheless, they recognize that they have obtained an important benefit by participating in the organization, namely training, and they believe that the honey they produce is recognized for its excellent quality because of their training in best practices in apiary management.

Regarding participation in programs or institutions for support management, close to 80% of beekeepers mention having obtained support from the Secretariat of Agriculture, Livestock, Rural Development, Fisheries and Food (*Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación*, SAGARPA), followed by the Secretariat of Rural Development (*Secretaría de Desarrollo Rural,* SEDER), with 13.1%. In addition, 6.6% have received support from the Livestock Productivity Incentive Program (*Programa de Estímulos a la Productividad Ganadera*, PROGAN), which provided economic resources, support for hive identification and payment for technical assistance and training, as well as direct support of 75 pesos per hive to beekeepers of 10 to 175 hives and 75 pesos per hive from 175 to 1,500 hives. This contrasts to the partici‐ pation in the Secretariat of Social Development (*Secretaría de desarrollo Social*, SEDESOL) program, with 2.7%, which unlike the others promotes social and micro business development. Of the 26% who have not received support from any institution, the majority have less than 50 hives (Table 4).


**Table 4.** Institutions that have provided support to beekeepers in the south and southeast regions of Jalisco (Livestock Research Laboratory, Department of Agriculture Production, CUCSUR, University of Guadalajara).

Similar participation in support programs is observed in Michoacán and Yucatán, which beekeepers consider is mainly because of there being no requirement for guarantees.[19,24]

#### **3.9. Technological aspects**

Of the beekeepers interviewed, 84% have access to training including support by the SEDER through PSP technicians. Of these, 80% say they have put into practice the knowledge obtained both in congresses and during training with technicians, mainly in disease control, feeding, and honey production with good practices. This is interesting as the percentage of beekeepers with technical or higher education is very low. This coincides with what happens in the Alhué commune in Chile, where 70% are interested in training on beekeeping topics, as indicated by Torres,[22] who reports that 80% of beekeepers mention having attended training courses and the rest consider themselves self-taught.[31] This is in contrast to what happens in Santa Catarina in Brazil, where beekeepers do not put into practice knowledge obtained in different forums because the majority engage in beekeeping as a secondary activity, in addition to financial difficulties.[32] It should be mentioned that in the study zones, 47% engage in beekeeping as a primary activity, which is perhaps why they are more likely to put innovation into practice.

Of those interviewed, 94.5% carry out pest and disease control in January, February, June, and August ([Table 5). Varroa is the main problem affecting 91% of their bees, with foulbrood to a lesser extent at 24%, and chalkbrood at 16%. Yucatán presents similar figures for Varroa but with chalkbrood at 44.4%.30] In India, treatment is provided to 86.7% of hives, mainly against varroa and moths.[33] Similarly, in Canada it has been reported that varroa is the main cause of death for bee colonies during winter, being associated with 85% of cases of mortality.[34] Furthermore, in the United States, Europe, and Japan bee colony deaths have also often reported (*Apis mellifera* L.). The *Varroa destructor* mite and the combination of some viruses have been implicated in recent disappearances of bee colonies, making it a particularly serious threat to the health of bees.[35]



**Table 5.** Feeding and disease control by month in the south and southeast regions of Jalisco (Livestock Research Laboratory, Dept. of Agriculture Production, CUCSUR, University of Guadalajara).

Given that varroa is the main pathological problem in the study zones, 45% of producers have focused on controlling mite infestation in bee colonies using mainly Bayvarol®, 28.4% use natural products, and 16% use Apivar®. Only 7.7% did not apply any treatment. There are few studies in Mexico that show the detrimental effect of varroa on honey production; however, in Valle de Bravo in Mexico State, colonies treated with an acaricide against *V. destructor* were observed to produce significantly more honey than untreated colonies,[36] but it should be noted that environmental conditions and the type of bee may influence the effect of varroa on the productivity of the bees.[37]

## **3.10. Feeding frequency and feed type**

Of the beekeepers interviewed, 96.7% provide maintenance feed to their bees; 81% of these provide energy feed mainly in syrup, and only 33% provide protein feed, unlike Brazil, where 63.6% provide maintenance feed and only 9% protein feed.[38] The use of fructose and confectionery waste is an uncommon practice. In Yucatán, 77.8% feed their bees with a sugar syrup, while only 14.8% feed them with honey, the rest use granulated sugar.[28] In California, the use of honey and sugar syrup is described,[39] and in Chile feeding with honey is also practiced;[31] however, this practice endangers the health of the colonies if the honey does not come from safe sources.

The frequency of feeding is from 7 to 10 days (36.1%), 11 to 15 days (45.4%), and 16 to 30 days (17.5%). Various types of feeders are used to feed, the most popular being a plastic bag (close to 27%), followed by a 1-liter tub (25.7%), the Doolittle feeder (18.6%), and less frequently the Miller feeder (14.2%) and plastic soda bottle (13.7%). Feeding and feeding frequency is a management practice that guarantees vigorous colonies when the nectar is flowing, which translates into higher production levels. Feeding is one of the main production costs and beekeepers indicate that in recent years bees need to be fed for longer periods because of changes in rainfall cycles and lack of flowering. In this respect, the practice of migratory beekeeping, which is negligible in these regions, could reduce feeding costs, however, the costs of moving the hives and the wide competition for spaces to place apiaries would have to be considered.

The majority of the beekeepers in the study manage modern jumbo or Langstroth hives. In contrast, beekeepers in Ethiopia use predominantly rustic hives even though they mention having adopted technological innovation (86%) and notice production increases; nevertheless the modern hive has not gained popularity because of its high cost and lack of awareness.[40] In the north of Ethiopia, an average of 33 and 16 kg of honey per colony was observed in modern and traditional hives, respectively; production is more than doubled with just the transition to a modern hive.[41]

#### **3.11. Quality control**

As far as the implementation of a quality system, 66% carry out some practice for this purpose, mainly maintaining hygiene in the equipment, harvest and post-harvest, and avoiding the use of pollutant fuels and to a lesser extent using vegetable oil instead of paint to protect the hives.

Within the honey harvesting process, 82% of beekeepers interviewed use a smoker to remove the bees from the racks, either alone or in combination with shaking or brushing. The fuel they use is wood chips and corn cobs. This is consistent with the authorized physical means to repel the bees from combs for harvesting (air, shaking, brushing, and smoke through the use of clean fuels). Only a few (4.9%) use chemical repellents (carbolic acid, propionic anhydride, and benzaldehyde), which are restricted because of their residual action on honey and because they are considered carcinogenic. It is also inadvisable to use hydrocarbons and their derivatives (diesel or liquid gas) or materials impregnated with chemicals, paints, resins, or organic waste such as manure as fuels.[9] These are important aspects to consider in the honey production process to preserve and even improve Mexico's privileged position on the international market.

Among honey processing equipment, 60% of beekeepers said they had an extraction room, and the rest mention having a prepared space or resorting to the rental or loan of a room to carry out the extraction: 66% of the beekeepers say the rooms in which they work are equipped with running water. Close to 70.5% of the beekeepers in the study have stainless steel equip‐ ment (extractor and settling tank), an indispensable requirement within the good practices of honey production. In addition, 16.4% of beekeepers claim to have galvanized metal extractors and 11% mention other types of materials, among which some are made by the beekeepers themselves; 64.5% of the beekeepers use drip trays in the honey harvesting process in the field, with which they protect the supers from possible field contamination; and 66. 7% of beekeepers in Michoacán have an extractor and only 39.5% a settling tank, but the kind of materials these are made from are not described, and although they have incorporated technology, they have not updated it in accordance with current demands for safe food products.[19]

About 63.4% of beekeepers sieve or strain the honey as part of the process once it is extracted, while the rest mention only letting it settle for a period of 48 hours in the tank, and bottling it from there. On the other hand, it was observed that 87% of Michoacán producers filter the honey.[19] The technological level is a competitive factor intended to speed up the production process.[38] This leads to an increased volume of honey and reduces costs by improving equipment and tools with the innovation of the beekeeping production system.

## **4. Conclusions**

In the south and southeast regions of Jalisco, beekeeping is practiced by older people, with little appeal to the young and few women participants. Small and large producers with over 1,000 hives participate in the activity, although the majority are small producers who do not have enough hives to justify a full-time commitment. This is reflected in a considerable reduction in honey production that is below the national average, due mainly to environmental factors, high production costs and health problems in which varroa is the producers' major challenge. There is little diversification and differentiation between bee products, so it is necessary to work on strategies to differentiate the quality of honey to maintain their position as global exporters. The beekeepers in general are unaware of the destination of the production, and only have general references of those who buy large quantities, the destination being simply exportation. Similarly, there is little knowledge of the quality standards demanded by export markets. The level of education of producers has encouraged them to attend various training and technical assistance forums, as well as the assimilation of technological innovation both in hive management and harvest and post-harvest of honey and derivatives, through the incorporation of stainless steel equipment in the extraction rooms.

## **Author details**

Contreras-Escareño F1\*, Echazarreta CM2 , Pérez-Armendáriz B3 , Cavazos Arroyo J3 , Macías-Macías JO4 and Tapia-González JM4

\*Address all correspondence to: franciscacon@cucsur.udg.mx

1 Department of Agricultural Production of the Costa Sur University Center of the University of Guadalajara, Av. Independencia Nacional No. 151, Autlán, Jalisco, México

2 Autonomous University of Yucatan, Calle 60 No. 491-A por 57, Centro, Mérida, Yucatán, México

3 Popular Autonomous University of Puebla State, Interdisciplinary Center for Postgraduate Research and Consulting, Santiago, Puebla, México

4 Sur University Center, Av. Enrique Arreola Silva, Colonia Centro, Cd Guzmán, Jalisco, México

## **References**

[1] Coordinación General de Ganadería. (2010). Situación actual y perspectiva de la apicultura en México. SAGARPA, *Claridades Agropecuarias*, 34 p.


## **Appendices**


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#### **5. What is the average yield per hive? (Indicate unit of measurement)**

#### **6. What are the problems you face in producing honey? (In order of importance)**

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#### **16. Indicate under each heading your expenses for producing honey (per year)**


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**20. What changes do you think are necessary to improve the functioning of beekeepers associations?**

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**21. Which organizations or government programs have given you support?** a) SAGARPA b) Local livestock associations c) FIRA d) Other (Specify)


