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Standardization of managed honey bee (Apis mellifera) hives for pollination of Sunflower (Helianthus annuus) crop
⁎Corresponding author at: Unit of Bee Research and Honey Production, Biology Departement, Faculty of Science, King Khalid University, P. O. Box 9004, Abha 61413, Saudi Arabia. khalidtalpur@hotmail.com (Khalid Ali Khan)
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Received: ,
Accepted: ,
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
Peer review under responsibility of King Saud University.
Abstract
To determine the effect of honey bee (Apis mellifera L.) pollination on sunflower yield using the most appropriate number of beehives per unit area of crops is very important. By comparing the number of hives and yield components, we can satisfy optimal pollination needs and improve economic yields. For this purpose, a series of experiments were conducted at thatha Khalil farmer field Taxila Rawalpindi, under the supervision of Beekeeping and Hill Fruit Pests Research, Station Rawalpindi, Pakistan, with four treatments for comparison: 1 hive acre−1, 2 hives acre−1, 3 hives acre−1, and 0 hives acre−1 as a control. The hives were kept inside the experimental area and pollination density, pollinator’s diversity, agronomic yield, and economic yield were determined. Two acres of sunflower field were sown and four bee colonies were introduced at 5% to 10% flowering. The maximum visitation frequency of A. mellifera was recorded at the weekly interval from 24 to 09-2019 to 24–10-2019, according to which maximum visitation was observed (44.8, 38.4, and 16.5 plant−1 5 min−1) at 10:00, 12:00, and 14:00 hrs, respectively. Data regarding foraging pollinators revealed that A. mellifera was the most dominant pollinator of the sunflower crop with the highest abundance 17.11% followed by A. cerana (3.46%) and the population of A. dorsata was minimum (2.12%). Furthermore, agronomic parameters (number of seeds plant−1, 100 seed weight (g), and economic yield were significantly higher in those fields which were pollinated by more beehives in comparison to fewer beehives.
Keywords
Honey bee
Beehives
Standardization
Pollination
Sunflower
Seed yield
1 Introduction
Pollination is widely acknowledged as an important ecosystem service and a necessary activity for food security (Klein et al., 2007; Aizen et al., 2009; Khan et al., 2021b). Pollination is an important service in the ecosystem accomplished by pollinators. Insects pollinate about 85%, air and water contribute 10% and self-pollination contributes only 5% (Fattorini and Glover, 2020). Pollinators are valuable species in the animal kingdom necessary for maintaining biodiversity. Pollination increases fruit setting, enhanced capacity of seed germination, and better quality of seed or fruit (Ahmad et al., 2021; Khan and Ghramh, 2021). When quality production increases; it has a direct effect on human health. Nearly 75% of the main crop species of the world rely on pollinators for fruit and seed set (Klein et al., 2007), which include managed pollinators such as honey bees (Apis mellifera) and various wild bees (Garibaldi et al., 2013; Kleijn et al., 2015; Ahmad et al., 2021). Furthermore, pollinators supply 35% to global food volume and play a key role in supplying vital nutrients for human subsistence (Klein et al., 2007; Gallai et al., 2009; Holzschuh et al., 2012). The statistical value of insect-pollinated crops of the Himalayan region of Pakistan has reported about 954.59 million USA dollars (Abrol, 2015). Pakistan's pollination-dependent crop production value was estimated to be at 1.59 billion US$ (Irshad and Stephen, 2013). For instance, fruits account for 0.98 billion US$, vegetables for 0.32 billion, nuts for 0.15 billion, oilseeds for 0.13 billion, and spices for 0.004 billion US$ (Irshad and Stephen, 2013). Pakistan is spending millions of dollars on importing edible oil, which is a major drain on the foreign exchange reserves of the country (Shahzad and Rashid, 2006). The native oil manufacture of the country could not match the growing demand of the population. The edible oil utilization was 2.764 million tons (MT) of which 0.857 MT (31%) came from local income and 1.907 MT (69%) were imported (Anonymous, 2006). Rape and mustard groups of crops contribute about 21% of the domestic edible oil but their area is continuously decreasing. However, it has been observed that honeybee pollination enhances the yield by increasing the number of pods and seeds/pod. The pod ration in pollinated and non-pollinated was 815:349, similarly seed per pod was also 15% more in pollinated crop. Seed weight was also more in case of honey bee pollinated crop (Munawar et. al.,2009). But different authors have ranked the value of honey bees vs. other pollinators for agricultural pollination differently (Aebi et al., 2012; Ollerton et al., 2012; Khan et al., 2021a; Saleh et al., 2021).
Sunflower (Helianthus annuus L.), is a globally significant oilseed crop that has essential agronomic qualities, such as drought, cold, and heat resistance. Sunflower is the main source of high-quality edible oil (40% to 47%) and its seed contains 20% to 25% protein (Saleem et al., 2003). Its cultivation is a cost-effective crop rotation option that allows for intercropping and crop succession in seed-producing areas (Porto et al., 2007). Additionally, it requires insect pollinators on flowering, particularly the honeybees for seed production (Ali et al., 2015; Latif et al., 2019). A. mellifera is the only most abundant ecologically important introduced pollinator and is mostly managed for honey production. Therefore, there is a vast scope of improving the pollination of crops by designing and implementing strategies to manage economically important insect pollinator’s especially native bees for seed and fruit production in the agricultural ecosystem (Delaplane et al., 2013). Only if production is quantified at field scale along a pollinator gradient will an estimate of pollinator contribution be useful to farmers (Vaissière et al., 2011).
Keeping in view its economic importance, the current project was designed to examine the role of the managed honey bee A. mellifera L. pollinator in increasing seed yield of sunflower crop by providing the most suitable number of beehive need per unit area of crops to meet optimum pollination needs and better economic yields by comparing the number of hives and yield components. Therefore, the findings of this research will contribute to the definition of general guidelines to maintain or improve sunflower crop pollination concerning the beehive or bee population size.
2 Materials and methods
2.1 Study area and field selection
The study was conducted on sunflower crops in the farmer field area of Taxila (Thatta Khalil) under the supervision of Beekeeping and Hill Fruit Pests Research Station Rawalpindi, Pakistan during 2018–19. The experiments were set up in a completely randomized block design along with four replications of each treatment.
2.2 Abundance of Apis mellifera during the blooming period of sunflower
The hives were kept inside the experimental area marked in the study field. One-acre field of the hybrid variety of sunflower Suncross was sown and four bee colonies were introduced at 10% to 15% flowering. At the time of seedling emergence, sunflower plants were hand-thinned. All recommended agronomic and cultural practices along with irrigation were adopted uniformly to all treatments weakly.
During the blooming period of the crop, no insecticides were applied to the experimental area. The observations were made from the beginning of the 5% flowering session until the end of the crop's flowering session. A comparative visitation pattern of A. mellifera was noted irrespective of pollen collection and time spent on each fluorescence. This experiment consists of the following three treatments: T1, 10:00; T2, 12:00, and T3; 14:00 h.
2.3 Comparative frequencies of honeybee species during the flowering period of sunflower
Honeybee species density was measured by scan sampling 200 flower heads in each of the four plots located in each experimental site. Data were recorded weekly during the whole blooming period. The scan sampling method was not involve timing but rather the insect recorded or not depending on whether it is present at the time has given flower is first seen. Sampling was done by walking slowly on 4 set patches in the experimental area. The data was taken at 10:00, 12:00, and 14:00 h weekly throughout the blooming period of sunflower (Said et al., 2017).
2.4 Effect of number of bee colony pollination efficiency on sunflower agronomic parameters
This experiment was carried out to determine the density of A. mellifera for maximum crop pollination sunflower fields with two sets of four treatments for comparison: 3 hives acre-1, 2 hives acre-1, 1 hive, and 0 hives acre-1 as a control. To investigate total seed yield kg acre-1, sunflower heads from all treatment plots were collected, dried, and threshed. The weight of 100 pod seeds was measured using electric balance and each net treatment yield was later converted into kg acre-1.
2.5 Economic yield of sunflower
After assessing the agronomic yield of sunflower, the economic yield was calculated. The economic yield was obtained from the net income, which was found out by using the following formula (Delaplane et al., 2013):
Where:
ΔNI = Increase in number of hives
P = Price that farmer obtains from each metric tons of the crop
ΔY = Yield increased in metric tons because of addition of hives
CY = Cost of producing each ton of yield
Ch = Cost of renting hive
ΔH = Addition of hives
2.6 Statistical data analysis
All statistical data were analyzed using the SPSS statistical package (version 26). The significance of the difference between the two groups was determined using the Student's-test. Differences between means were considered statistically significant at the 95% (p < 0.05) confidence level, while differences at the 99% (p < 0.01) confidence level were considered highly significant.
3 Results
3.1 Visitation rate of A. Mellifera during the blooming period of sunflower
Our results indicated that the maximum visitation frequency of A. mellifera was recorded at the weekly interval from 26 to 09-2019 to 24–10-2019 during the whole blooming period. According to which maximum visitation frequency was observed (44.8, 38.4, and 16.5 plant−1 5 min−1) at 1000, 1200, and 1400 hrs, respectively on October 17, 2019 (Table 1). The visitation rate of A. mellifera differed significantly at 1000, 1200, and 1400 hr, respectively on 24th September, 11th, 17th, and 24th October. Whereas no significant difference was observed visitation rate on 4th October (Table 1). Means sharing the same letter are not similar at 5% probability of LSD.
Pollinators
24th Sep.
4th Oct.
11th Oct.
17th Oct.
24th Oct.
Apis mellifera
9.41a
11.41a
15.37 a
17.11a
10.78a
A. cerana
2.14b
3.3b
2.55b
3.46b
2.77b
A. dosata
2.90b
3.41cb
2.12 cd
2.00 bd
1.64c
A. florea
3.89b
3.92 d
4.44 bc
2.95 cbd
2.26b
LSD
0.53
0.36
0.44
0.68
0.47
3.2 Foraging pollinator rate of honey bee species on sunflower
Data regarding the foraging rate of honey bee species have been taken during the blooming period of sunflower. The maximum honey bee pollinators were observed on 17 October 2019 with a maximum population of A. mellifera (17.11) followed by A. cerana (3.46), A. florea (2.95), and population of A. dorsata was minimum (2.00) (Fig. 1).
Foraging activity of different honey bee species during the blooming period of sunflower on different observation dates (2019).
The foraging rate of A. mellifera differed significantly in comparison to A. cerana, A. dorsata, and A. florea on 24th September, 4th, 11th, 17th, and 24th October during the blooming period of sunflower (Table 2). Means sharing the same letter are not similar at 5% probability of LSD.
Pollinators
24th Sep.
4th Oct.
11th Oct.
17th Oct.
24th Oct.
Apis mellifera
9.41a
11.41a
15.37 a
17.11a
10.78a
A. cerana
2.14b
3.3b
2.55b
3.46b
2.77b
A. dosata
2.90b
3.41cb
2.12 cd
2.00 bd
1.64c
A. florea
3.89b
3.92 d
4.44 bc
2.95 cbd
2.26b
LSD
0.53
0.36
0.44
0.68
0.47
3.3 The effect of the number of honeybee colonies on yield parameters of sunflower
The mean comparison of yield parameters is given in (Table 3) that illustrated the effect of sunflower plants exposed to A. mellifera along with other insects, and sunflower plants kept under 1 hive acre−1, 2 hives acre−1, and 3 hives acre−1 on agro- morphological parameters of Helianthus annuus var Hysun-33. Our results reported that the number of seeds per plant was significantly in 3 hives acre−1 (1472) as compared to 2 hives acre−1 (1165), 1 hive acre−1 (9 3 4), respectively (Table 3). While a smaller number of seeds per plant were recorded in control (8 8 0). Similarly, 100 seed weight (g) was observed significantly more in 3 hives acre−1 (5.34 g) as compared to 2 hives acre−1 (4.87), 1 hive acre−1 (3.98), respectively (Table 3). At the same time, <100 seed weight (g) was noted in control (2.84 g). Means sharing the same letter are not similar at 5% probability of LSD
Modes of Pollination
Parameters
1 hive acre−1
2 hives acre−1
3 hives acre−1
Control
LSD
No. of seeds plant−1
934c
1165b
1472 a
880 cd
201.246
100 Seed weight(gm)
3.98c
4.87b
5.34 a
2.84 d
0.5653
3.4 The effect of honeybee colonies on economic yield of sunflower
After assessing the agronomic yield, the economic yield calculated. The economic yield was obtained from the net income, which was found out by using the following formula:
1 hive acre-1
= P × ΔY – CY × ΔY – Ch ×ΔH
= 80,000 × 0.2 – 62,500× 0.2 – 1000 ×1
= 16,000 – 12,500 – 1000
Net income
= 2,500/ =
2 hives acre-1
= P × ΔY – CY × ΔY – Ch ×ΔH
= 80,000 × 0.48 – 62,500× 0.48– 1000 ×2
= 38,400 – 30,000 – 2000
Net income
= 6,400/ =
3 hives acre-1
= P × ΔY – CY × ΔY – Ch ×ΔH
= 80,000 × 0.84– 62,500× 0.84 – 1000 ×3
= 67,200 – 52,500 – 3000
Net income
= 11,700/ =
Mode of Pollination
Net Income (PKR)
I hive acre−1
2,500
2 hive acre−1
6,400
3 hive acre−1
11,700
4 Discussion
Plants with appealing floral characteristics may attract more pollinators and have a better reproduction rate, resulting in more fruit and seed sets (Mallinger and Prasifka, 2017). Notably, mass-flowering crops, such as sunflower, cannot support a persistent pollinator population. It is ideal to have both managed honey bees and wild pollinators in the agricultural environment to ensure pollination (Lajos et al., 2021). Honey bees are the most important flower visitors (Hung et al., 2018), and were primary pollinators of sunflower in our study. In this study, A. mellifera was the main insect pollinator involved in increasing the agronomic yield as well as the economic yield of sunflower. Following previous findings that honey bees (A. mellifera) is the most dominant pollinator of sunflower (Riedinger et al., 2014; Sardiñas and Kremen, 2015).
On the other hand, very low foraging rates by A. dorsata was recored. Unexpectedly, we did not measure the percentage of edible oil and protein contents in the seed of sunflower in our experiments. However, a recent study by Lajos et al. (2021) revealed that foraging rates of honey bees in sunflower fileds can increase the seed set and oil content.
Dušanic et al. (2004) suggested that the diameter of head sunflower be strongly correlated with seed mass and the number of fertilized seeds. Our results elucidated that bee visitors were found throughout the day but the visitation rate of A. mellifera was significantly higher at 1000 AM in comparison to 1200 and 1400 during the blooming period of sunflower. In contrast, (Said et al., 2017) reported that frequent visitation of A. mellifera and A. florea was recorded at 1200 noon during the flowering period of sunflower. Currently extenstive use of insecticide decreased honey bee visits in sunflower (Pashte and Patil, 2017).
Further, among the honeybee species, the foraging rate of A. mellifera was statistically more than A. cerana, A. dorsata, and A. florea, respectively during the flowering period of sunflower. Our results are inline with Silva et al. (2018), A. mellifera frequently visited sunflower field as compared to wild pollinators. Similarly, other studies reported that A. mellifera is the most abundant pollinator of several crops, especially sunflower (Greenleaf and Kremen, 2006; Carvalheiro et al., 2011). Moreover, the number of seed per plant and 100 seed weight (g) were significantly higher in those filed, containing a greater number of beehives for sunflower pollination. Many previous studies reported that pollinated service in sunflower provided by various types of honey bee species significantly increased the seed size (10%-15%) and the total number of seed yield (18%-100%) depending on the cultivar of the crop (Nye and Anderson, 1974).
Similarly, the economic rate was also higher in pollinated fields by more beehives than less beehives. However, more studies are needed in the future to better understand the effectiveness of the different types of honeybee species to increase the agronomic characteristic of various cultivars of sunflower.
5 Conclusions
This present study concluded that A. mellifera was the vital insect pollinator involved in increasing the agronomic parameters as well as the economic yield of sunflower. The foraging rate of A. mellifera was significantly higher than A. cerana, A. dorsata, and A. florea during the blooming period of sunflower. Furthermore, agronomic parameters and economic yield were significantly higher pollinated fields by more beehives in comparison to less beehives. This study may help the local framers to understand the importance of bee pollination and maintain insect pollinators near to sunflower to ensure good productivity.
Acknowledgments
We thank the PARB to provide the chance of this study, thank the scientist and the staff of beekeeping station .The facilitation provide by the farmer from Taxila, the scientist help in statistical analysis from Millet Research Station and Natural Resource Division, PARC, Islamabad. The authors appreciate the support of the Research Center for Advanced Materials Science (RCAMS) at King Khalid University Abha, Saudi Arabia through project number RCAMS/KKU/002-21.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
References
- Abrol, D.P. (2015). Pollination biology, Vol. 1: Pests and pollinators of fruit crops. Springer.
- Aebi, A., Vaissière, B.E., Van Engelsdorp, D., Delaplane, K.S., Roubik, D.W., and Neumann, P. (2012). Back to the future: Apis versus non-Apis pollination-a response to Ollerton et al. Trends in Ecology and Evolution.
- Effects of native pollinator communities on the physiological and chemical parameters of loquat tree (Eriobotrya japonica) under open field condition. Saudi J. Biol. Sci.. 2021;28(6):3235-3241.
- [Google Scholar]
- How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot.. 2009;103(9):1579-1588.
- [Google Scholar]
- Insect visitors and abundance of four species of Apis on Sunflower Helianthus annuus L. in Pakistan. Acta Zool. Bulg.. 2015;67(2):235-240.
- [Google Scholar]
- Natural and within-farmland biodiversity enhances crop productivity. Ecol. Lett.. 2011;14(3):251-259.
- [Google Scholar]
- Standard methods for pollination research with Apis mellifera. J. Apic. Res.. 2013;52(4):1-28.
- [Google Scholar]
- Dušanic, N., Miklic, V., Joksimovic, J., Atlagic, J., and Crnobarac, J. (Year). “Path coefficient analysis of some yield components of sunflower”, in: Proceeding of 16th International Sunflower Conference II), 531-537.
- Molecular mechanisms of pollination biology. Annu. Rev. Plant Biol.. 2020;71(1):487-515.
- [Google Scholar]
- Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ.. 2009;68(3):810-821.
- [Google Scholar]
- Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. 2013;339(6127):1608-1611.
- [Google Scholar]
- Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl. Acad. Sci.. 2006;103(37):13890-13895.
- [Google Scholar]
- Landscapes with wild bee habitats enhance pollination, fruit set and yield of sweet cherry. Biol. Conserv.. 2012;153:101-107.
- [Google Scholar]
- The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B: Biological Sciences. 2018;285(1870):20172140.
- [CrossRef] [Google Scholar]
- Value of insect pollinators to agriculture of Pakistan. Int. J. Agron. Agric. Res.. 2013;3:14-21.
- [Google Scholar]
- Foraging behavior of western honey bee (Apis mellifera) in different time intervals on Brassica campestris L. Fresenius Environ. Bull.. 2021;30(3):2607-2612.
- [Google Scholar]
- Pollen source preferences and pollination efficacy of honey bee, Apis mellifera (Apidae: Hymenoptera) on Brassica napus crop. Journal of King Saud University-Science. 2021;33(6):101487.
- [CrossRef] [Google Scholar]
- Honey bee (Apis mellifera) preference towards micronutrients and their impact on bee colonies. Saudi J. Biol. Sci.. 2021;28(6):3362-3366.
- [Google Scholar]
- Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun.. 2015;6(1)
- [CrossRef] [Google Scholar]
- Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B: biological sciences. 2007;274(1608):303-313.
- [Google Scholar]
- Landscape structure affects the sunflower visiting frequency of insect pollinators. Sci. Rep.. 2021;11(1):1-11.
- [Google Scholar]
- Diversity of pollinators and their role in the pollination biology of chickpea, Cicer arietinum L. (Fabaceae) J. Asia-Pac. Entomol.. 2019;22(2):597-601.
- [Google Scholar]
- Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar sugars. J. Appl. Entomol.. 2017;141(7):561-573.
- [Google Scholar]
- Insect pollinators frequenting strawberry blossoms and the effect of honey bees on yield and fruit quality. J. Am. Soc. Hortic. Sci.. 1974;99(1):40.
- [Google Scholar]
- Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011) Trends Ecol. Evol.. 2012;27(3):141-142.
- [Google Scholar]
- Impact of different insecticides on the activity of bees on sunflower. Research on Crops. 2017;18(1):153-156.
- [Google Scholar]
- Porto, W.S., de Carvalho, C., and Pinto, R. (2007). Adaptability and stability as selection criteria for sunflower genotypes. Pesquisa Agropecuaria Brasileira (Brazil).
- Early mass-flowering crops mitigate pollinator dilution in late-flowering crops. Landscape Ecol.. 2014;29(3):425-435.
- [Google Scholar]
- Studies on visitation pattern of honeybee (Hymenoptera: Apidae) and its impact on the yield and oil contents of sunflower (Helianthus annuus L.) seed in Peshawar valley, Pakistan. Pakistan. J. Zool.. 2017;49(3)
- [Google Scholar]
- Bio-economic assessment of different sunflower based intercropping systems at different geometric configurations. Pak. J. Biol. Sci. (Pakistan). 2003;6(13):1187-1190.
- [Google Scholar]
- Onion flowers anthesis and insect pollinators preferences on onion (Allium cepa L.) Crop. Fresenius Environ. Bull.. 2021;30(3):2580-2585.
- [Google Scholar]
- Pollination services from field-scale agricultural diversification may be context-dependent. Agric. Ecosyst. Environ.. 2015;207:17-25.
- [Google Scholar]
- Determination of pollen viability and role of honey bees Apis cerana in the pollination of sunflower CMS lines in isolated tunnels. Pak. Entomol. 2006;28(2):69-72.
- [Google Scholar]
- Bee pollination highly improves oil quality in sunflower. Sociobiology. 2018;65(4):583.
- [CrossRef] [Google Scholar]
- Protocol to detect and assess pollination deficits in crops: a handbook for its use. FAO. 2011
- [Google Scholar]
