Relationship Between Honeybee Workers and Plum Orchards I. Their Activity in Gathering Nectar and Pollen from Flowers

12 Arab Congress of Plant Protection ,ACPP ,4 -10 November, 2017 Hurghada Egypt Egyptian Academic Journal of Biological Sciences is the official English language journal of the Egyptian Society for Biological Sciences, Department of Entomology, Faculty of Sciences Ain Shams University. Entomology Journal publishes original research papers and reviews from any entomological discipline or from directly allied fields in ecology, behavioral biology, physiology, biochemistry, development, genetics, systematics, morphology, evolution, control of insects, arachnids, and general entomology. www.eajbs.eg.net Provided for non-commercial research and education use. Not for reproduction, distribution or commercial use.


INTRODUCTION
Pollination is one of the most important factors for the production of many fruits and vegetables (Free, 1993).Honeybees (Apis mellifera L.) play an important role in the pollination of flowers.Most surveys have shown that honeybees form a high percentage of the insects visiting fruit tree flowers (Thorp, 1979;Klungness et al., 1983;Verma andDulta, 1986 andFree, 1993).Bees gather nectar and pollen from flowers for food for their own use.Major role of honeybees in pollinating tree fruits has long been recognized.Stephen (1958) obtained a positive correlation between the number of bees and amount of fruit set in five pear orchards.Free (1962) found that plum trees near to honeybee colonies were visited by more bees and had a greater set than trees further away.Bees gathering pollen are considered the main pollinators of the plum species because of their activity early in flowering (Langridge and Goodman, 1985).Calzoni and Speranza (1998) indicated that foraging activity from 7 to 8 a.m. was generally very rare.The visits were more numerous from 12 to 1 p.m. and from 4 to 5 p.m.It is a well-known fact that foraging activity increases with increasing temperature, sunlight, and with decreasing relative humidity.Foraging activity of honey bees was highest during the second sampling hour of the day.
Also, in the recent study, El-Dereny (2010) found a positive correlation between the numbers of workers visited flower and fruit set in apple (1.92 bees/ flower) and almond (2.0 bees/ flower) orchards.In the same trend, she found a negative correlation with increasing honey bee visits/ flower and fruit firmness in apple or the percentages of empty nuts and the malformed kernels in almond.The behavior of bees during visiting flowers determines their efficiency as pollinators (Free, 1993).Bees collecting pollen, deliberately scrabble over the anthers pulling them towards its body and frequently biting them.Thus, touch the stamens and stigmas and so may pollinate the flowers (Parker, 1926).Whether or not nectargatherers pollinate depends upon where they stand on the flowers.Thus when a nectar-gatherer stands on the anthers and pushes its tongue as well as the front part of its body toward the nectaries it touches the stigmas and stamens and so could pollinate, but when it stands on the petals and pushes itself through the stamens and pistil to reach the nectaries, it does not touch the stigmas and so do not pollinate (Vansell, 1942 andStephen, 1958).
Therefore, the main objective of the current study is to determine and classify the honeybee foragers that visited flowers of certain plum cvs.commonly grown in Egypt, (Golden Japanese, Hollywood and Santarosa) at different periods of the day throughout the blossoming season of two successive years, (2012 & 2013).

MATERIALS AND METHODS
The current investigations were carried out in plum orchards (2000 m 2 ) at El-Qalubia Governorate, during the two successive seasons (2012,2013) on mature trees (20 years old) of Golden Japanese, Hollywood and Santarosa cvs.Trees were planted in a clay loamy soil and were of uniform growth, irrigated by furrow irrigation system and maintained according to the program applied.Trees were spaced at 4X5 m. and planted in rows where the cvs.alternated with each other.The experimental field was well provided with strong beehives as pollination requirements (2-3 hives/ ha) which recommended by Delaplane and Mayer (2000).
The study focused on the behavior of honeybee workers on the flowers of the three cvs.

Foraging activity of honeybee workers
Observations were made by randomly selecting five trees from each cv.and randomly choosing ten flowers (Fig. 1) at full pink stage from each tree as a replicate (a total 50 flowers/ cultivar) for each cv during the two successive seasons.As flowers reached full open stage, observations and counts were taken from 8 a.m. to 5 p.m. at 3 hour intervals for all of the trees under investigation throughout the whole blooming period (which extended from 3/3 to 21/4 during 2012 and from 7/3 to 18/4 during 2013).The following activities of honeybee foragers were recorded according to (Abd Al-Fattah, 1995 andEl-Dereny, 2010).a-No. of bees/ flower/ min., (mean of 10 flowers) b-No. of visited flowers/ bee/ min., (mean of 10 bees).c-Percentage of pollen, nectar or both honeybees collectors by classifying 20 foragers for each replicate.Experiments were designed in a randomized complete block design with five replicates; each tree was considered a replicate.Data were subjected to the analysis of variance (ANOVA) according to Freed et al. (1989) using MSTAT software and means of treatments were compared using Duncan multiple range test (Version 2.10) at a significance level of 0.05 (Duncan, 1955).

Foraging activities of honeybee workers: Number of bees/ flower/ minute:
The mean number of visited bees/ flower/ minute was significantly differed between the three studied cultivars (cvs.) during the day.The highest mean of bees was found on Hollywood (9.71 bees/ flower/ min.)followed by Santarosa (7.39 bees/ flower/ min.)then Golden Japanese flowers (5.10 bees/ flower/ min.).These means were 9.80 and 9.78; 7.48 and 7.40 and 5.07and 5.23 for the mentioned cvs., respectively, during the two successive seasons, 2012 & 2013 (Table 1 and Fig. 2).
For the three tested cvs.and during both years of investigation, the foraging activity of bees on plum flowers started in the early morning, and continued till the end of the day (Table 1).There were significant differences between the mean numbers of foraging bees on plum cvs.Throughout the day.Bees started to visit plum flowers from 8 a.m.(5.1 bees/ flower/ min.)and reached their maximum visits at 2 p.m.(10.8 bees/ flower/ min.)after that it declined to 6.7 bees/ flower/ min.at 5 p.m. (Fig. 3).
Results of the present study are in line with the findings of many investigations such as Noro and Yago (1934) and also with Mann and Singh (1983).They agreed that visiting bees to Rosaceae flowers mainly found between 8 a.m. and 5 p.m. also, these findings are in line with data observed by El-Dereny (2010).

Number of visited flowers/ bee/ minute
In both two flowering seasons, there were significant differences in foraging activity between the three studied cvs. in terms of the mean numbers of visited flowers/ bee/ minute during the different day time as shown in Table (2).In general, the flowers of Hollywood cv. were visited in pronounced multi-frequencies of bees (6.15 flowers/ bee/ min.),than other tested plum cvs., (4.72 flowers/ bee/ min.)for Santarosa and (3.3 flowers/ bee/ min.)for Golden Japanese.For Hollywood plum flowers, the number of visited flowers/ bee/ minute was 6.13 and 6.20 flowers/ bee/ minute in 2012 and 2013 seasons.The corresponding respective means for Santarosa cv. were 4.50 and 4.99, respectively.On the other hand, the lowest mean number of visited flowers was observed on Golden Japanese cv.(3.11 and 3.59 flowers/ bee/ minute) during the two seasons, respectively.(Table 2 and Fig. 4).As shown in Table (2) and Fig. ( 5), the number of visited flowers/ bee/ minute for the three tested plumcvs.during the different chronological periods of the dayhad the same trend.During both study seasons, the minimum significant number of flowers was visited at 8 a.m.(3.4 flowers/ bee/ min.).Foraging activity was significantly increased to reach its climax at 2 p.m. with mean value of (6.8), then it declined again by the end of the day (4.1 at 5 p.m.).The general mean number of flowers/ bee/ min.was 4.8 which was less than those recorded by Verma and Dulta (1986) where the average numbers of flowers that honeybees have been seen to visit per minute were 6.6 flowers.These results were also agreed with the earliest observation which recorded by Huston (1926) on apple flowers.Wilson (1926Wilson ( , 1929) ) and Free (1960) found that adverse weather conditions increased the time spent per flower and bee visitation was differed with different cultivars and from season to another.

Pollen and Nectar gathering activity
Data in Tables 3 and 4 clear the foraging activity of honeybee workers on plum flowers for collecting eitherpollen or nectar alone during day time of two successive seasons.But the collection of both pollen and nectar in the same trip by one forager bee was presented in Table (5).Regarding foraging activity during the different day time, the flowers of the three tested plum cvs.were preferred and attractive to the bee foragers for collecting pollen, nectar or both in the same trip.The early studies by Parker (1926) showed that the honeybees visiting apple, pear, plum and cherry flowers collected either pollen only, nectar only or both.
Results in Table (5) and Fig. (8) indicate that a portion of the honeybee workers collected both nectar and pollen together in the same trip from the three tested plum cvs.were nearly at similar rate in 2012 and 2013, (34.3% and37.0%,respectively for Hollywood, 39.1% and 39.5%, for Santarosa and 32.9% and35.4% for Golden Japanese, respectively).Table (3 and 4) and Figs.(9 and 10).clearlyemphasize that the collection of pollen from the three tested plum cvs.occurred before mid-day with a maximum peak at 11 a.m.By peak time, the percentages of pollen collectors were 51.1% and 48.4% for Hollywood, 32.7% and 37.3% for Santarosa and 36.8% and 39.1% for Golden Japanese trees in 2012 and 2013, respectively.These findings were coincided with those founded by Vansell (1942), Percival (1955) and Stephen (1958).They agreed that the honeybee foragers increased their activities in collecting pollen only from early morning, (8 a.m.) and reach the gathering peak before midday and then rapidly decreased towards the end of the day.
A reverse behavior was observed for collecting nectar which increased in the middle of day with a peak at 2 p.m.The percentages of nectar collectors were 36.8% and 36.8% for Hollywood, 44.8% and 42.0% for Santarosa and 47.7% and 49.7% for Golden Japanese trees during 2012 and 2013, respectively.
Many authors worked on the behavior of honeybees on stone fruits found that the collection of nectar occurred throughout the day time with a peak in the second half of the day time and correlated with the flower age, (Thorp, 1979 andKlungness et al., 1983), the flower type (Verma and Dulta, 1986) and prevailing conditions, (Williams andBrain, 1985 andEl-Dereny, 2010).
Both pollen and nectar were collected from the three tested plum cvs.during early morning (44.3%at8 a.m.) then this activity was declined gradually at mid-day, after that it rise again during the end of the day (41.8%at 5 p.m.), as shown in Table

Fig. 1 :
Fig. 1: Longitudinal section of a plum flowerStatistical Analyses:Experiments were designed in a randomized complete block design with five replicates; each tree was considered a replicate.Data were subjected to the analysis of variance (ANOVA) according toFreed et al. (1989) using MSTAT software and means of treatments were compared using Duncan multiple range test (Version 2.10) at a significance level of 0.05(Duncan, 1955).

Fig. 2 :
Fig. 2: Mean number of bee visits/ flower/ minute for three different plum varieties during day time for two successive seasons of flowering, (2012 & 2013).

Fig. 3 :
Fig. 3: Mean number of bee visits/ flower/ minute for three different plum varieties during day time for two successive seasons of flowering, (2012 & 2013).

Fig. 4 :
Fig. 4: Mean number of flowers/ bee/ minute for three different plum varieties during day time for two successive seasons of flowering, (2012 & 2013).

Fig. 5 :
Fig. 5: Mean number of flowers/ bee/ minute for three different plum varieties during day time for two successive seasons of flowering, (2012 & 2013).

Fig 11 .
Fig 11.Mean percentage of honeybee foragers collected both Pollen and Nectar from three Plum varieties through diurnal hours in two successive seasons, (2012 & 2013).

Table 1 : Mean number of visited bees/ flower/ minute for three different plum varieties during day time during two successive seasons of flowering, (2012 & 2013).
Mean in the same row or column with the same letter (s) are not differed significantly according to Duncan's Multiple Range Test at level 0.05%.

Table 2 : Mean number of flowers/ bee/ minute for three different plum varieties during day time during two successive seasons of flowering, (2012 & 2013).
Mean in the same row or column with the same letter (s) are not differed significantly according to Duncan's Multiple Range Test at level 0.05%.

Table 3 : Mean percentage of honeybee foragers collected Pollen from three Plum varieties through diurnal hours in two successive seasons, (2012 & 2013).
Mean in the same row or column with the same letter (s) are not differed significantly according to Duncan's Multiple Range Test at level 0.05%.

Table 4 : Mean percentage of honeybee foragers collected Nectar from three Plum varieties through diurnal hours in two successive seasons, (2012 & 2013).
Mean in the same row or column with the same letter (s) are not differed significantly according to Duncan's Multiple Range Test at level 0.05%.