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Ryabceva Yulia Sergeevna, doctor, of Philosophy (Ph. D), Head of the Scientific-Research Laboratory "Live Country", Agri Research Foundation E-mail: yr@futura.com.ua
THE EFFICIENCY OF BOMBUS TERRESTRIS (INSECTA: APIDAE) AS POLLINATORS OF SWEET CHERRIES IN UKRAINE
Abstract: The efficiency of Bombus terrestris colonies pollinating the sweet cherry orchards was studied in two locations of Ukraine: Novoselki village, Kyiv region (Institute of Horticulture, National Academy ofAgrarian Sciences of Ukraine), and Sadove village, Zaporizhia region (Producing and commercial company "Melitopol cherry" Ltd). In the study of the bumblebee flying activity, it was established that the insects remained active during the whole day in spring, if the temperature was stable. Our observations confirm that the bumblebees successfully pollinate the plants in the overcast weather, starting at the temperature threshold of 8 °C, which is especially important for pollination of the outdoor crops.
Bumblebee colonies provided a significant increase in the yield of sweet cherry by 29.93% (Sadove village), and by 503% (Novoselki village). This incredible increase in the latter yield is caused by the timely and high-quality pollination of flowers by bumblebees, counteracting to a degree the unfavorable spring weather conditions of 2017 in Kyiv region.
Keywords: pollination, bumblebees, Bombus terrestris, sweet cherry, Prunus avium, yield.
Introduction greenhouse tomatoes [12]. The demand for efficient pol-
A high-quality harvest is inconceivable without the linators contributed to the rapid growth in bumblebee participation of pollinator insects. It is through their ef- colonies sales and their active use for pollination of in-
forts that the pollen of one plant falls on the flower of another plant of the same species, i.e. there is cross-pollination. This type of pollination contributes to the development of faster-ripening, symmetrical and large fruits.
Natural pollination is provided by many insects: bees, bumblebees, flies, butterflies and various species of beetles, etc. The leader of all pollinators is the honey bee, which does up to 80% of the total crop pollination [6, 15]. However, in the last few decades, honey bees have been scarce or completely absent, causing a significant decrease in the yield of several important horticultural plants, including fruit trees.
There is no horticultural technique to compensate for the absence of natural pollination, which is why finding the alternative pollinators and studying their effectiveness are such important tasks.
More than 30 years ago, the first bumblebee colonies were grown on an industrial scale for the pollination of
door and outdoor crops [9, 11, 13, 14, 16].
Nowadays, the peculiarities of using bumblebee colonies for pollination of fruit crops remain an urgent problem. There are recent studies that describe the positive influence of the bumblebee pollination on the harvest of cherries, apricots, pears, apple trees, etc. [7, 8, 10]. However, they present fragmented data and require clarifications and additions.
Studying the use of bumblebee colonies for pollination of fruit trees will possibly allow organizing an effective pollination process of these crops and increasing their yield.
The main goal of our study was to evaluate the pollination activity of Bombus terrestris (Linnaeus, 1758) on sweet cherry Prunus avium.
The following tasks were then sat:
1. Assessing the attendance of cherries by commercial bumblebee colonies "Live Country";
2. Measuring the basic yield indicators in the areas serviced by commercial bumblebee colonies and in control areas with a natural composition of pollinators.
Materials and methods
Study of the bumblebee pollinating effectiveness on the cherry cultivar "Melitopolska Chorna".
The research was performed in spring of 2017, at the plantations of Producing and commercial company "Melitopol cherry" Ltd (Sadove village, Zaporizhia region, Ukraine).
Climate. The experiment was conducted in an area with a sharply continental and arid climate. Annual precipitation fluctuates from 370 to 430 mm.
Plant sort description
The tree is big, fast-growing. The tree habit is wide and round, raised, dense. The bark on stem and skeletal branches are gray-brown. Shoot-forming ability is strong. Shoots are straight, yellowish-greenish-gray. The buds are large, oval, 7 mm long. The foliage is quite dense.
The fruits are large, monocarpous, 6-8 g in average, rounded oval, dark red (almost black). Fruit apex is rounded, the fruit base with a shallow and wide depression. Seam is shallow and hardly noticeable. Stem is 45-49 mm, of moderate thickness, easily picked off the branch. Pitting the fruit is easy, the pulp tears off without juice loss. Skin is thin, dense, dark red, and at full maturity almost black, shining, easily separated from the
pulp. Pulp is dark red, dense, fleshy and juicy. Juice is dark red. Pit is small and rounded and. The taste is sweet and pleasantly acidic. The cultivar is self-sterile.
Six commercial bumblebee colonies ("Live Country", Ukraine) were placed at an experimental plot (0.5 ha). The orchard was planted in 2013 with "Melitopolska chorna" sweet cherry, at a planting distance of 5 x 3 m. A similar plot, without bumblebees, was used as control (Fig. 2). The distance between these plots was 150 m.
The bumblebee hives were set up in the Institute of Horticulture on April 13, 2017, when sweet cherry began to blossom.
The flying activity of bumblebees was estimated once a week for 3 weeks. Activity was defined as a mean number of bees leaving hives and returning to the nest - in the morning, at the midday and in the evening for 15 minute periods.
Two 50m*25m sites were chosen at the experimental and control plots to study the pollinating efficacy of bumblebees (Fig. 2). Each site harbored 40 cherry trees, and for each tree the number of fruits, the number of deformed fruits and the total yield weight were calculated.
Evaluating the pollinating efficacy of bumblebee colonies on the sweet cherry cultivar "Lubava".
The experiment was conducted in spring 2017 at the Institute of Horticulture, NAAS of Ukraine (Novoselki village, Kyiv region, Ukraine).
^ - bumblebee hives set up; direction of the flight openings; | - sites for assessment of bumblebee pollinating efficacy Figure 1. Design of the experiment on "Lubava" sweet cherry cultivar: A - control area; B - experimental area
H - bumblebee hives set up; ^ direction of the flight openings Figure 2. Design of the experiment on "Melitopolska Chorna" sweet cherry sort: A - control area; B - experimental area
Climate. The study area is characterized by moderate continental climate, with approx. 550 mm average annual precipitation.
Plant cultivar description
The tree is of medium height, with a dense, rounded and well-branched habit. Fruits are produced during the 4th-5th year after planting. The tree is not self-fertile. The fruits are large (8-9.8 g), rounded heart-shaped, yellow with bright red blush, tolerant to cracking.
They are easily detached from stem. The pit is of moderate size, easily detached from flesh. Pit to flesh mass ratio is 4.9%. The flesh is light-yellow, juicy, crunchy, with a nice sweet flavor. The produced yield is suitable for all purposes.
We used three commercially sourced colonies of B. terrestris ("Live Country", Ukraine) that were placed at the experimental plot (0.2 ha). The trees were planted in 1997, at the planting distance of 6 m*4 m.
The bumblebee hives were set up at the beginning of inflorescence period, on April 13, 2017. The bumblebee hive set up scheme is given in Fig. 1.
As control plot, 0.2 ha area with sweet cherry cultivar "Lubava" was selected, planted in 1997, with planting distance of 6m * 4m. The distance between these plots was 500 m.
The state of bumblebee colonies was monitored for the first few weeks after their installation. In addition to the external inspection of hives, the number of foragers flying out of the nest in 15 minutes was counted.
To assess the bumblebee pollinating efficacy, three sites were selected at the experimental plot (fig. 1). The ovary percentage, the percentage of crop damage from unfavorable weather conditions, and the ratio of crop to plant weight were determined for each site. These characteristics were also assessed at the control plot.
All obtained quantitative data was processed using the standard "PASW Statistics 17" and "Statistica 6.0" software packages.
Results and discussion
Today, bumblebees are recognized among the most effective pollinators in agriculture. About 30 years ago, it was shown that bumblebees can excellently pollinate tomatoes in greenhouses. Since then, bumblebee colonies have been successfully used not only for pollination of indoor crops, but also for raspberries, strawberries, blueberries, pears and other important outdoor plants. This increased involvement of bumblebees to a greater extent, thanks to their advantages over other insect pollinators including honey bees. Honey bees can also
pollinate most of agricultural crops, but they are often less efficient than bumblebees.
1) Bodies of bumblebees are built to carry twice as much pollen as honey bees.
2) Bumblebees provide good cross-pollination because of their unique flight process which involves frequent change of plants and tree rows.
3) Bumblebees have longer tongues than honey bees, which are unable to pollinate certain flowers because of it.
4) Bumblebees are more tolerant to unfavorable weather than other pollinator insects. They can pollinate in overcast weather and at 8-10 °C, which is especially important in the case of outdoor crops.
For pollination of outdoor fruits and berries, it is recommended to use a colony with one queen, 120-150 workers, and brood (larvae, eggs, and pupae). Higher numbers of larvae require more pollen brought by the workers in the nest. They forage more and, consequently, increase the productivity of pollination. Bumblebee pollination leads to higher fruit quality and increased total yield, and thus to a better price.
The results of experiment on the cultivar "Melitopolska Chorna".
In our study, the foraging insects could move in and out of the colony freely and follow their normal daily routine. The flying activity of bumblebees was estimated in cherry blossom period. To this end, the bumblebees' departures and arrivals were counted in the morning, at midday and in the evening for 15-min-ute periods (Table 1).
The insect is always influenced by a combination of factors. However, the factor that is most remote from its optimal level affects it most strongly [5].
The daily activity of bumblebees in nature was studied separately by D. V. Panfilov [2] and by V. I. Blinnikov [1] (on Carduuspycnocephalus L. in August). Researchers found that the insect forage all day long, with markedly higher intensity in the late morning (9-11 a.m.) and in the evening (4-6 p.m.). From noon to 2 p.m., most foragers are in the nest avoiding the danger of overheating in this most hot time of the day. According to the classification of rhythms by V. B. Chernyshev [3], the bumblebees can be classified as daytime insects with a long morning and evening activity.
Table 1.- Flying activity of commercial bumblebee colonies "Live Country" on the sweet cherry cultivar "Melitopolska Chorna"
Day of observation Time of observation Weather Insects departed Insects returned
8.00 Sunny, + 10 ° C 53 48
25.04.2017 11.00 Strong wind, + 12 ° C 14 17
16.00 Strong wind, + 8 ° C 3 4
8.00 Cold, +4 ° C 0 0
02.05.2017 11.00 Windy, + 9 ° C 0 0
16.00 Strong wind, + 7 ° C 0 0
8.00 Sunny, + 17 ° C 43 56
09.05.2017 11.00 Sunny, + 22 ° C 69 49
16.00 Light breeze, + 18 ° C 42 51
In the first week of observations (25.04), the maximum activity of bumblebees was recorded in the morning at sunny weather: 53 foragers flew out of the nest, 48 bumble bees returned to the hive during the 15 minute observation.
In the afternoon the temperature dropped. This appeared to be the decisive factor, which caused the flying activity of bumblebees to decrease to three departures.
In early May, cold and windy weather fully prevented the flight activity. However, insunnyweather and at+17 ° C,
the flight activity index increased to 43 flights in 15 minutes. At 11 a.m., the maximum number of departures in 15 minutes was 69. By 16 p.m., the insect activity declined to 42 flights.
According to the observations, the bumblebee flight activity is constant in the morning and at noon if the air temperature is moderate. If the temperature drops to + 4... + 7 ° C, the bumbles do not fly out to forage. Nevertheless, at the threshold of + 8 ° C (first week) they resume pollinating. Our results confirm that bumblebees
can pollinate in the overcast weather and at + 8 ... 10 ° C, The results ofB. terrestris bumblebees pollinating the
which is most important for outdoor growers. sweet cherry cultivar "Melitopolska Chorna" are given
in (Table 2).
Table 2.- Pollinating efficiency of bumblebee colonies "Live Country" on the sweet cherry cultivar "Melitopolska Chorna"
Yield indicators Experimental plot Control plot Difference
Number of fruits per tree 482.0 369.8 +30.33%*
Yield weight per tree, kg 38.63 29.72 +29.93%*
Percentage of deformed fruits per tree 0.69% 0.89% +0.2%**
Note: *p < 0.01; **p > 0.05 (difference is not significant)
Bumblebee pollination caused the number of fruits to grow by 30.33% (t = 2.98, df = 78, p < 0.01), to 482 fruits per tree compared to 369.8 fruits on the control plot.
The number of flowers, as a rule, much exceeds the number of ripe fruits for almost all cultivars of sweet cherry. Excess flowers and ovaries fall in the first weeks after flowering, mainly because of insufficient pollination and fertilization, and delayed development [4].
Thus, at the plot with the natural composition of pollinators, approximately 30.33% of flowers were either less or not at all pollinated compared to flowers on the plot, where commercial bumblebee colonies were active.
The percentage of deformed fruits at the experimental plot was lower by 0.2% than at the control plot.
However, this difference was statistically insignificant (t = 1.51, df = 78, p > 0.05).
As a result of bumblebee activity, the yield weight significantly increased by 29.93% (t = 2.96, df = 8, p < 0.01). The bumblebee colonies increased the overall pollination of the studied sweet cherries, thus causing the larger yield weight.
The results of experiments on the "Lubava" sweet cherry cultivar.
The bumblebee colonies were observed successfully foraging in cold weather (+ 5 ... +9 ° C) (Fig. 3). In this temperature range and in sunny weather, bumblebees much more often (up to 57 times) flew out after noon, closer to 15.15 p.m. (21.04).
The daily dynamics of bumblebee activity is most likely explained by the combined effect of considered factors.
Figyre 3. Flying activity of commercial bumblebee colonies "Live Country" on the sweet cherry cultivar "Lubava"
Table 3.- Pollinating efficiency of Bombus terrestris on the sweet cherry cultivar "Lubava"
Experimental plot
Control plot
The effect ofbumblebee activity
Percentage of damage caused by unfavorable weather conditions,%
2.03
39.5
-37.47;
Set fruits,
38.2
38.5
-0.3%%
Total yield per tree, kg
9.2
1.83
+503%'
Note: * significance level of 5% (p < 0.05); ** significance level of 1% (p < 0.01); *** not significant (p > 0.05)
At + 5 ... + 9 ° C, the foragers were relatively active all day long, making from 11 to 57 flights in 15 minutes.
The pollinating efficiency of B. terrestris is presented in (Table 3).
The -2 'C ... -5 'C frosts in April and May present the biggest danger for the sweet cherry yield. These frosts damage the reproductive buds and ovaries significantly, sometimes even killing them. The pistil stigmas are the most sensitive flower parts that can die in the buds or after the flowers start blooming.
In the study, frosts of low intensity (0 ... -2 'C) were noted in the Kyiv region when the sweet cherries were blooming. The yield loss caused by unfavorable weather was significantly higher by 37.47% (t = 2.8, df = 4, p < 0.05) on the plot with the natural pollinator combination, in comparison with the plot with bumblebee activity. It is obvious that the bumblebee colonies lessened the influence of spring frosts. If the pollination and germination of the pollen tube happened before the pistils have frozen off (at -1.5 ' C), the fruits would develop as usual. The bumblebees contributed to the timely and qualitative pollination and thus to a significant reduction in yield losses from unfavorable weather factors. Thus, the yield weight increased by 503% s(tC = 16.01, df = 4, p < 0.01).
Conclusions
It is reliably shown that the bumblebees enhance
the quantitative indicators of the sweet cherry yield. It
is found that at a relatively stable temperature in spring, the foragers remain highly active. Our observations confirm that bumblebees can effectively pollinate plants in overcast weather, at a temperature of+8 'C, which is especially important for pollination of outdoor crops.
On the example of two sweet cherry cultivars, we showed the efficiency of using bumblebee colonies for pollination of this species. Bumblebees provided the high-quality pollination, contributing to an increase in the number of fruits per tree (Sadove village, Zaporizhia region), and weakened the influence of negative weather conditions on the harvest (Novoselki village, Kyiv region).
Thus, we believe that the bumblebee colonies are promising for obtaining high yields of sweet cherry.
Acknowledgements
The authors are grateful to O. N. Yareschenko and E. A. Kyschak (Institute of Horticulture, National Academy of Agrarian Sciences of Ukraine), and M. I. Grint-sev (Producing and commercial company "Melitopol cherry" Ltd) for their helpful assistance in the course of this work.
The work was supported by "Futura" Foundation for culture and innovation.
References:
Блинников В. И. Зоология с основами экологии.- М.: «Просвещение».- 1990.- С. 68-80. Панфилов Д. В. К экологической характеристике шмелей в условиях Московской области // Учен. Зап. Пед. Ин-та им. Потемкина.- 1956.- № Т. 61.- Вып. 45.- С. 467-483. Чернышев В. Б. Экология насекомых.- М.: Изд-во МГУ, - 1996.- 304 с. Шайкин В. Г. Энциклопедия сада.- М.: Олма-Пресс, - 2002.- 351 с. Яхонтов В. В. Экология насекомых.- М.: Высшая школа, - 1964.- 460 с. Bohart G. E. Insect pollination of forage crops // Adv Agron.- 1960.- V. 12.- P. 72-58. Calzoni G. L., Speranza A. Pear and plum pollination: honey bees, bumble bees or both? // Acta Hortic.- 1996.-V. 423.- P. 83-90.
8. Chaillout S. Do commercial bumblebees (Bombus terrestris) have an added value in outdoor pollination of sweet cherry (Prunus avium) and raspberry (Rubus ideaus)? - Agricultural sciences.- 2016.- 49 p.
9. Goodell K., Thomson J. D. Comparisons ofpollen removal and deposition by honey bees and bumblebees visiting apple // Acta Hortic.- 1997.- V. 437.- P. 103-107.
10. Velthuis H. H.W, van, Doorn A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination // Apidologie, Springer Verlag.- 2004.- V. 37 (4). - P. 421-451.
11. Javorek S. K., MacKenzie K.E., Vander Kloet S. P. Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium) // Ann. Entomol. Soc. Am.- 2002.- V. 95.- P. 345-351.
12. Ravestijn W. van, Nederpel L. Trostrillers in België aan de kant: hommels doen het werk // Groenten en Fruit.-1988.- № 6 (12 februari).- P. 38-41.
13. Sampson B.J., Spiers J. M. Evaluating bumblebees as pollinators of 'Misty' southern highbush blueberry growing inside plastic tunnels // Acta Hortic.- 2002.- V. 574.- P. 53-61.
14. Thomson J. D., Goodell K. Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers // J. Appl. Ecol.- 2001.- V. 38.- P. 1032-1044.
15. Todd F. E., McGregor S. E. The use of honey bees in the production of crops // Ann Rev Ent.- 1960.- V. 5.-P. 265-278.
16. Whidden T. L. The fidelity of commercially reared colonies ofBombus impatiens Cresson (Hymenoptera: Apidae) to lowbush blueberry in Southern New Brunswick // Can. Entomol.- 1996.- V. 128 (5).- P. 957-958.
