Foraging behavior of the giant honey bee , Apis dorsata F . ( Hymenoptera : Apidae ) in sunflower ( Helianthus annuus L . ) at Peshawar District of Pakistan

Foraging of honey bee is of great importance from pollination point of view, as sunflower production mainly depends on insect visitors in common and honeybee in particular. Keeping in view the importance of pollinators, foraging behavior of the Giant Honey bee, Apis dorsata in sunflower, Helianthus annuus L. at Peshawar District was studies at New Developmental Farm (NDF), The University of Agriculture Peshawar, (34.01° N, 71.53° E) Khyber Pakhtunkhwa (KP), Pakistan during 2012 and 2013. Observation on foraging activities of honeybee recorded from morning hours i.e. 0800 hr and continued until 1800 hr of the day. It was found that foraging of honey bee varied greatly during different hours of the day. Maximum foraging of A. dorsata species recorded at 1600 hr and followed by another peak foraging activities of bee visitors at 1200 noon. Minimum foraging activities found at 1800 hr. It was also learnt that foraging of bee visitors’ greatly affected by the amount of pollens and nectars on blossoms of sunflower. During 20 and 25 days after flowering on the crop, maximum individuals of A. dorsata recorded since numerous plants were in full bloom. Similarly, less number of bees found while foraging as the crop moved toward maturity. It was concluded that sunflower is such a crop that attracts honeybees which helps in cross-pollination of the crop and ultimately increase grain yield as well as enhance quality of the produce as well. Farmer communities hence should advise to avoid extensive use of insecticides during blossoming stage in order to protect honeybees and other natural enemies.


Introduction
Insect visitors pollinate more or less 90% of various flowering plant species across the world [1].Pollinators have been the major source while determining the mating prospects of crops.In terms of pollination, many plant species are generalists [2, 3] and rely on numerous pollinator species.Among pollinators, honeybees (Apis spp.) are generally considered the most important and leading pollinator species associated with a wide range of economically important crop species worldwide.Wide range of host range enables honeybees to pollinate several types of crops.As compared to many other insect visitors, honeybees have longest visit time to flowers and less affected by adverse weather conditions.Their close relation to a lot of of imperative crops and its foraging behavior makes them successful insect pollinators.Honeybees are reported to have an indispensable role in enhancing the competence level of many crops including most of seed species crops [4][5][6].The improved quality of grains and fruits in different crop has been observed when these crops were visited by managed honeybee colonies [7].Honeybee pollination may increase fruit set percentage by 10 to 25 per cent and fruit yield by 18 to 100 per cent depending upon the cultivar [8,9].Sunflower is such a crop that is generally fertilized by wind, even though, the wind is considered as the chief pollinator for many flowering plants, yet it is not enough for pollination on many kinds of plants including sunflower (H.annuus L.) because it is not competent to offer homogenous pollination as well as not being able to carry heavy pollens [10][11][12].Worker bees of A. dorsata forage less number of pollens from different flowers than that of A. mellifera, which forage and carry huge pollen loads from flowers.However, A. dorsata individuals forage heavier pollens during early morning hours [13].According to [14] Population density of A. dorsata species is declining due to many reasons like widespread insertion and endorsement of A. mellifera individuals by public and private sector through developmental intrusion, alteration in their habitat and biodiversity.Non-judicious application of chemical pesticides, diseases and parasites attack etc are also mainly responsible for low incidence of A. dorsata species.As per report of [15] among different species of honeybee, such as domesticated bee species Apis mellifera and Apis cerana have extraordinary significance since their inhabitants can be easily managed accordingly to need of crops and duration of blooming period.In addition to these domesticated honeybee species, wild honeybee, Apis dorsata also play essential role in many fruit and seed crops.Keeping in mind the importance of bee visitants, the present research study was therefore, conducted with the intention to determine the foraging pattern and population density of the Giant honeybee (A.dorsata) in Peshawar District of Khyber Pakhtunkhwa (KP).

Materials and methods
Present investigation on foraging behavior of Giant Honeybee, A. dorsata on sunflower was carried out at the New Developmental Farm (NDF) of the University of Agriculture Peshawar (34.01°North latitude and 71.53°East longitude) during 2012 and 2013.Sunflower Hybrid Hysun-33 was grown during spring and autumn seasons and standard agronomical practices were adopted while sowing the crop.The experimental area was kept free from any pesticide application during the flowering period of the crop.The experiment was laid out in Randomized Complete Block (RCB) design and was replicated four times.Plot size was kept 3 × 3 m 2 with 5 rows that were 60 cm apart from each other.Plant-to-plant distance was maintained 30 cm respectively.The following parameter was studied during experiment:

Population density of Apis dorsata on sunflower Hysun-33
As per procedure adopted by [16] observation on bee visits to sunflower blossoms was taken from commencement of 5 per cent flowering on the crop and last until 35 th days after inflorescence.Daily observation of bee visitors after a gap of 5 days was recorded 6 times at 0800, 1000, 1200, 1400, 1600 and 1800 hr of the day.Observations were recorded on total number of bee individuals for 5 minutes on 10 randomly selected capitula in four different spots having area of 3 × 3 m 2 and thus mean bee visits was calculated.

Statistical analysis
After recording observations, the collected data were analyzed according to the procedure appropriate for randomized complete blocked design (RCBD) combine over year and season by using statistical software, Gen-Stat third edition.Least significance test was performed for separation of means when the F-test was found significant, as outlined by [17].

Foraging activity of Apis dorsata on sunflower Hysun-33 during spring 2012-13
Data on foraging behavior/ pattern of honeybees on selected crop at different time intervals revealed that 5 days after initiation of flowers on the crop, it was found that individuals (4.37) of A. dorsata were most active during noon at 1600 hr, which was followed by second peak (3.62) of foraging activities at 1200 hrs.Lowest (1.37) foraging activity was found at 1800 hrs of the day (Table 1).After an interval of 10 days of 5 percent blooming on the crop, inhabitants of A. dorsata constituted maximum (4.75) density at 1600 hr, which was followed by mean frequency of 4.12 at 1200 noon.Minimum foraging activities of honeybee recorded with 1.75 bee visitors at 0800 hrs.15 th day after flowering, the foraging activity of A. dorsata started at 0800 hr with 2.87 bees/m 2 /5min.population density of honeybee recorded on its peak (5.37) at 1600 hr.Second peak foraging of bee visitors observed with average population of 4.50 at 1200 noon.Minimum strength was recorded with 2.25 bees at 1800 hrs of the day.On 20 th day of 5 per cent of flowering on the crop, A. dorsata individuals foraging activities were observed with 5.25 bees per 3 m 2 area for 5 minutes at 1600 hr that was followed by 5.25 and 4.62 count of bee visitants at 1200 and 1000 hr respectively.The foraging activities declined to least count of 2.75 bees at 1800 hr during evening hours of the day.It is evident from (Table 2) that 25 th day after flowering, the first peak (5.87) of foraging activities of A. dorsata recorded at 1600 and second peak of bee visitants noticed with mean count of 5.25 honeybees at 1200 noon.Similarly, the least activity was found at 1800 hr, which recorded only 2.50 bees/m 2 /5min.On 30 th day after crop blooming stage, it was noticed that highest bee visitation was occurred at 1600 noon with average number of 4.37 bees, which was followed by a second peak of 3.75 individuals of A. dorsata at 1200 hrs of the day.Less foraging activities of bees were observed during late hours and was found that mean number of 1.12 bees were engaged in foraging at 1600 hrs.Foraging activities of A. dorsata on sunflower after 35 days of crop flowering stage showed that their incidence declined due to maturity of crop and less availability of pollens and nectar on flowers.However, highest (3.25 and 2.87) mean counts of bee individuals were made at 1600 and 1200 hr respectively.Lowest (0.87) foraging was found at 1800 hrs of the day.

Foraging activity of Apis dorsata on sunflower Hysun-33 during autumn 2012-2013
A. dorsata was most prevalent (3.00 bees/3m 2 /5min) at 1600 hr. of the day that was followed by 2.37 at 1200 noon.Minimum count of honeybees was recorded with 0.87 bees/3m 2 /5 minutes at 1800 hrs of the day.On 10th day after flowering, A. dorsata foraging activities were observed with highest count of 3.25 bees per 3 m 2 area for 5 minutes at 1600 hrs of the, which was further followed by a mean population of 3.00 bees at 1200 hr.minimum incidence recorded with 1.25 at 1800 hr during evening hours of the day.Data regarding mean incidence of bee visitors recorded on 15 days after flowering revealed that first peak of A. dorsata foraging activity recorded at 1600 hr of the day with 3.62 bees whereas second peak foraging activity was found at 1200 hr with 3.25 bees.Minimum activity of bees was found at 1800 hrs, which recorded only 1.75 individuals of A. dorsata.After 20 th day of flowering, it was found that highest (4.50) mean frequency of A. dorsata individuals were recorded at 1600 hr of the day.The next peak foraging observed with 4.02 bees/3m 2 /5 minutes at 1200 hr.Lowest (2.25) population of bees was found at 1800 hr of the day.On 25 th day after crop, blooming stage maximum foraging recorded at 1600 hr with mean number of 4.25 bees, which was followed by a second peak of 3.87 individuals of A. dorsata at 1200 hrs of the day.Minimum counts with 2.37 bees/3m 2 /5 minutes noticed at 1800 hrs of the day.On 30 th day after flowering, the first peak (3.37 bees/3m 2 /5minutes) of foraging activities of A. dorsata found at 1600 hr.second peak of bee visitants observed with a mean count of 3.00 individuals at 1200 noon.An average count on only 1.12 bees recorded at 1800 hr of the day.On 35 th day after crop blooming stage, it was found that significantly more (2.75)number of bee recorded at 1600 hr, which was followed by 2.37 bees at 1200 hr.Minimum (0.75) foraging activity was recorded at 1800 hrs of the day.

Table 2 . Population density of Apis dorsata on Sunflower during autumn 2012-2013
Honeybees play a vital role in successful production of sunflower seeds, which not only increase grain yield but also improve quality of the grains significantly.Highest density/foraging of A. dorsata individuals were recorded during 1600 and 12000 noon of the day that greatly helped in cross-pollination of the crop.Pollination services provided by honeybees may be helpful in enhancing seed yield in sunflower and possibly in many other fruit and seed species crops.Since large number of honeybee's forage sunflower capitula during its blooming stage, which not only enhance grain yield but also improve quality of the produce as well.Farmer communities therefore, should advise to avoid widespread use of insecticides when crops are in blossoming stage to protect pollinator species and other natural enemies.Authors' contributionsConceived and designed the experiments: F Said, Performed the experiments: F Said, Analyzed the data: F Jalal, Contributed materials/ analysis/ tools: M Imtiaz, MA Khan & S Hussain, Wrote the paper: F Said.Manager, New Developmental Farm (NDF) for providing experimental plot.The financial assistance provided by the Higher Education Commission (HEC) Islamabad, Government of Pakistan is also highly acknowledged.