Submit or Track your Manuscript LOG-IN

Comparative Foraging Behavior of Honey Bee Species A. cerana (F) and A. mellifera (L)

SJA_41_1_304-314

Research Article

Comparative Foraging Behavior of Honey Bee Species A. cerana (F) and A. mellifera (L)

Hamza Iftikhar1, Ranra Jalal2, Mansoor Ali Shah1, Syed Anas Shah Bacha1, Amjid Ali1 and Syed Majid Rasheed1*

1Department of Agriculture, Bacha Khan University, Charsadda, Khyber Pakhtunkhwa, Pakistan; 2Department of Weed Science, The University of Agriculture, Peshawar, Khyber Pakhtunkhwa, Pakistan.

Abstract | An experiment was conducted to compare the foraging behavior of two honey bee species i.e., A. mellifera and A. cerana in Langstroth hives and A. cerana in traditional mud hives across eight weeks and three-time durations (T1, T2 & T3) at the Directorate of Non-Timber Forest Products (NTFP), Forest Department Khyber Pakhtunkhwa, Peshawar during spring, 2020. The highest outgoing foraging was recorded for A. cerana in a traditional mud hive (46.54), followed by A. mellifera (44.84), and the minimum outgoing foraging was recorded from A. cerana in a Langstroth hive (44.76). Considering outgoing, incoming and foragers returning with pollen, T1 (0700-0800 hr) was best time, whereas the foragers returning with water or nectar the most active time was T3 (1100-1200 hr). Weeks were inversely proportional to foraging behavior due to increase in temperature as predicted by returning of foragers with water and nectar. The pollen collection sources for A. mellifera and A. cerana, were 4 and 6, respectively. There was no significant difference in the ash and moisture content of the pollen of honey bee species. In contrast, the sugar concentration of A. mellifera pollen was higher than that of A. cerana in the Langstroth hive and A. cerana in the traditional mud hive when the three glucose-D standards were used to compare them to each other. Thus, it can be concluded that A. cerana in traditional mud hive shows better foraging performance as compare to A. mellifera and A. cerana in Langstroth hive.


Received | October 29, 2024; Accepted | January 07, 2025; Published | February 14, 2025

*Correspondence | Syed Majid Rasheed, Department of Agriculture, Bacha Khan University, Charsadda, Khyber Pakhtunkhwa, Pakistan; Email: [email protected]

Citation | Iftikhar, H., R. Jalal, M.A. Shah, S.A.S. Bacha, A. Ali and S.M. Rasheed. 2025. Comparative foraging behavior of honey bee species A. cerana (F) and A. mellifera (L). Sarhad Journal of Agriculture, 41(1): 304-314.

DOI | https://dx.doi.org/10.17582/journal.sja/2025/41.1.304.314

Keywords | Foraging behavior, A. mellifera, A. cerana, Langstroth hive, Traditional mud hive

Copyright: 2025 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).



Introduction

Apiculture is the combination of two words Api means bees and culture means cultivation. Apiculture is the knowledge and ability of bees and beekeeping. A honey bee belongs to class insect order hymenoptera genus Apis. Bees are reared for the production of Honey (Cook et al., 2019). Honey is highly nutritive food consisting of a variety of proteins, sugars, minerals, free amino acids, enzymes, vitamins and trace elements. Human blood absorbs laevulose and dextrose directly from honey. Asian continent has a variety of diverse honey bee species. A number of species of genus Apis are found in Asian continent are: florae, dorsata, andreniformis, cerana, koschevnikovi, nuluensis, nigrocincta and laborios A. Taxonomists also introduced A. mellifera which are now days widely used for honey production. In Pakistan there are mainly four species present which are broadly spread in the country (Nabila et al., 2022).

Of the four species two species of honey bees that are Asian honey bees, the A. cerana, and European honey bees, the A. mellifera, can be domesticated in Pakistan for their by-products whereas the other two species A. florae and A. dorsata cannot be domesticated due to their wild behavior and habitation preference (Gratzer et al., 2019). A. cerana and A. mellifera species resembles each other in behavior and morphology to such extent that the scientists were confused that whether they both are same species (Oldroyd and Wongsiri, 2009). While some scientists believed that A. cerana and A. mellifera belongs to the same ancestral base from last two million years (Yang, 2009).

Lately the promotion of sustainable beekeeping and training in mite supervision is being initiated under Pakistan-USDA funded project. Due to queen rearing and colony multiplication, the number of A. mellifera colonies has increased significantly over the past 20 years. These colonies have subsequently been dispersed among beekeepers throughout Pakistan. By 1985 there were over 3000 colonies of A. mellifera honey bees species in Langstroth hives but in the mountainous regions of Pakistan, people use to keep A. cerana species for the production of honey. A. cerana has been raised in Asian countries for thousands of years and has brought considerable economic benefits to the apicultural industry (Natapot et al., 2023). Geographically Pakistan is blessed with diverse range of habitats from 8000 m snow-capped Himalayan peaks down to different forests and plains of the Indus and arid deserts regions found in the south of the country (Usman et al., 2022).

The western honey bee (A. mellifera L.) provides highly valued pollination services for a wide variety of agricultural crops and ranks as the most frequent single species of pollinator for crops worldwide. A long history of domestication and intentional transport of A. mellifera by humans has resulted in its current cosmopolitan distribution that includes all continents except Antarctica and many oceanic islands (Hung et al., 2018). As they fulfill the tasks, which are carried out of the bee hive during foraging for their colonies they bring water, pollens, nectars and resin. Many scientists have reported the significance of honey bee foraging in the pollination of plants. Russell et al. (2021) particularly in those plants in which honey bees primarily serves as pollinators.

The flowering plant species of a particular area can also be detected by the foraging of honey bees. Pest infestation of flowering crops or other plants from which the honey bees collect their requirements can be detected through foraging for example fruit flies (Chinkangsadarn and Kafle, 2024). All those people who are involved in Beekeeping can also take advantage of honey bee foraging by placing venom collection boards and pollen traps installed at the entrances of honey bee hives for collection purposes. Honey bees are blessed with such good qualities that they can choose better and best food source when many food sources are available in an area (El-Ghouizi et al., 2023)

Foraging honeybees bring pollens that could be analyzed, which is helpful in the classification of honey. Over 250 biological components are present in bee pollens that include antioxidants, vitamins, fats, carbs, minerals and enzymes. Plant source and collection season plays important role in the composition of exact nutrients (Kieliszek et al., 2018).

This experiment was conducted to identify the more effective pollinators of honey bee species and to categorize the bee flora in a certain location. Furthermore, the researcher learned about the differences in foraging among the species of honey bees.

Materials and Methods

Study area

The research was conducted at the Directorate of Non-Timber Forest Products, Khyber Pakhtunkhwa Forest Department, Peshawar during year 2020.

Honeybees (A. mellifera) and (A. cerana) colonies

Three honey bees colonies of (A. mellifera) Langstroth hive, (A. cerana) Langstroth hive and A. cerana in natural traditional mud hive with same number of worker bees, food and the brood comb were separated from their apiaries for the experiment. Three factor factorial experiments in randomized complete block design were conducted.

Treatment (Honey bee species) was taken as first factor having three levels i.e., H1 = A. mellifera in Langstroth hive. H2 = A. cerana in Langstroth hive. H3 = A. cerana in traditional mud hive.

Time duration was considered as second factor having three levels i.e.,

T1 = 0700-0800 hours. T2 = 0900-1000 hours. T3 = 1100-1200 hours. Weeks were taken as third factor having eight levels i.e., W1, W2, W3, W4, W5, W6, W7 and W8.

Foraging behavior data collection

Foraging data was recorded as per (Cartin et al., 2008) method.

Pollen classification

Pollens were collected from the surrounding area in such manner that pollens from newly emerged flowers of the surrounding area of each plant was collected in a white cloth and was brought to the laboratory, reference slides from the pollens were made. Hive entrances were equipped with pollen traps of their respective sizes to study the efficiency of pollen and foraging pattern of H1, H2 and H3. After collecting pollens from the hives through traps it was compared with the reference slides (Ramalho et al., 1991).

The experiment was repeated 04 times after every 15 days. The collected pollens of H1, H2 and H3 were weighed and compared at the end.

Chemical analysis of pollen

Moisture content: The pollen samples were dried to constant weight at 70oC in an air oven and then the moisture content was estimated (Bell et al., 1983). After estimating moisture content of dried samples of the pollen of each species, the comparison of moisture contents of each species was carried out.

Ash content

The ash content pollen samples of both species was estimated by heating the sample of pollen in the muffle furnace at 600 oC till it turns to grey white ash. The samples were weighed to measure the average percent of ash substance (Bell et al., 1983). Results of both pollen samples were compared.

Sugar concentration

Quantification of sugar was carried out as per Brummer and Cui (2005) method. The samples were prepared in two separate mediums i.e., aqueous and acidic medium.

Aqueous medium preparation

0.2 g of pollen sample of A. cerana in mud and Langstroth hive and A. mellifera was collected in beaker. It was mixed with 50 ml distilled water. All the samples were homogenized by mixing them thoroughly in the aqueous solution.

Acidic digested medium preparation

0.1 g of each treatment pollen samples was added with 20 ml HNO3. The samples were kept on a heating bath for 02 hours at 95oC for digestion. After the digestion, the samples were homogenized and filtered.

Standard procedure for determination of sugar content

In order to determine the total sugar content in the samples, the standard procedure was followed. The pollens were first dried and stored in a zip-lock bag. 0.2 g of each pollen sample was weighted and poured into a test-tube followed by the addition of 0.5 ml phenol. After the addition of phenol, 2.5ml concentrated H2SO4 was added to each of the test-tube containing samples of Honey bee species. The mixture was thoroughly combined using the vortex mixture. The color development was observed and was absorbed at 450 nm using a UV-spectrophotometer against Glucose D as standard. This procedure was followed for both the mediums and the results were then compared.

Results and Discussion

Foraging behavior of honey bee species

Out-going foragers: Honey bee species x Time intervals interaction: Honey bee species and time intervals data were recorded and depicted in Table 1. Honey bee species and time intervals were significantly different. The interaction of honey bee species and time interval revealed significant differences at 5% level of significance. Abou-Shaara et al. (2017) stated that A. cerana as compare to A. mellifera initiates foraging earlier and requires low thoracic temperature. Similarly, A. cerana foraging (departures per minute) also peaked earlier and at lower temperature than did A. mellifera foraging. Similar research results were also reported by Verma and Dulta (2015).

 

Table 1: Out-going foragers Honey bee species x Time intervals mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Time intervals

Mean

T1

T2

T3

H1

51.75 b

42.70 d

40.08 e

44.84 b

H2

51.20 b

44.25 c

38.83 f

44.76 b

H3

54.37 a

45.12 c

40.12 e

46.54 a

Mean

52.44 a

44.02 b

39.67 c

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Time intervals 0.8753. Critical Value for Honey bee species 0.5054. Critical Value for Time intervals 0.5054.

 

Honey bee species x weeks interaction

Honey bee species and weeks data were recorded and given in Table 2. Honey bee species, weeks and their interaction revealed significant differences. Maximum outgoing foraging was recorded by A. cerana in traditional mud hive in the first week while minimum foraging was revealed by A. cerana in langstroth in week seven. Blazyte-Cereskiene et al. (2010) recorded that a strong increase in ambient temperature (43+ ) had a negative impact on the foraging of honey bees on flowering plants. The temperature among different weeks fluctuated between 23 - 41 .

Time intervals x weeks interaction

It is revealed from the analysis of data that time intervals, weeks and their interaction among the out-going foragers were significant (Table 3). The maximum outgoing foraging was recorded at T1 during the W1 (58.33), while minimum value was recorded for T3 at W7 (37.77) Verma and Dulta (2015) argued that Peak foraging activity for A. cerana. Indica took place at 09.00–11.30 hrs when the temperature ranged between 15·5 and 21°C while 11.00–13.30 hrs for A. mellifera at temperature of 21 to 25°C. Contrary to their finding, peak time of out-going foraging activity was recorded at T1 (07.00-08.00 am). Furthermore, the difference in the foraging peak time can be due to the differences in altitude.

In-coming foragers

Honey bee species x Time intervals interaction: Significant difference among the Honey bee species, time intervals and their interaction was recorded for in-coming foragers of honey bee species (Table 4). The maximum and minimum in-coming foraging was recorded by A. cerana in traditional mud hive at time interval (T1) (51.79) and T3 (38.37), respectively. Our results are in similarity with Zhang et al. (2019), who argued that A. cerana has more foraging trips, higher forager proportion, less sugar consumption, and longer survival than those of A. mellifera.

 

Table 2: Out-going foragers Honey bee species x Weeks mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

H1

46.77 cdef

44.33 ijkl

43.33 lm

44.22 jkl

43.55 klm

45.44 fghij

45.33 ghij

45.77 defgh

44.84 b

H2

47.11 bcd

43.66 klm

43.77 klm

44.66 hijkl

44.77 hijk

45.66 efghi

42.44 m

46.00 cdefgh

44.76 b

H3

49.44 a

48.33 ab

44.33 ijkl

46.55 cdefg

43.77 klm

47.33 bc

45.55 fghij

47.00 bcde

46.54 a

Mean

47.77 a

45.44 bc

43.81 e

45.14 cd

44.03 e

46.14 b

44.44 de

46.25 b

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Weeks interaction 1.4294, Critical Value for Honey bee species 0.5054, Critical Value for weeks 0.8253

 

Table 3: Out-going foragers Time intervals x Weeks mean interaction of Honey bee species in Spring, 2020.

Time intervals

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

T1

58.33 a

53.88 b

50.77 d

52.33 c

50.66 d

52.22 c

50.22 d

51.11 cd

52.44 a

T2

44.55 ef

42.88 gh

42.11 h

44.11 fg

42.66 h

45.66 e

45.33 ef

44.88 ef

44.02 b

T3

40.44 i

39.55 ij

38.55 jk

39.00 jk

38.77 jk

40.55 i

37.77 k

42.77 gh

39.68 c

Mean

47.77 a

45.44 bc

43.81 e

45.14 cd

44.03 e

46.14 b

44.44 de

46.25 b

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Time intervals x weeks interaction 1.4294; Critical Value for time intervals 0.5054; Critical Value for weeks 0.8253.

 

Table 4: In-coming foragers Honey bee species x Time intervals mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Time intervals

Mean

T1

T2

T3

H1

48.37 c

42.25 e

38.79 f

43.13 b

H2

49.41 b

42.04 e

38.70 f

43.38 b

H3

51.79 a

43.83 d

38.37 f

44.66 a

Mean

49.86 a

42.70 b

38.62 c

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Time intervals interaction 0.7622; Critical Value for Honey bee species 0.4400; Critical Value for time intervals 0.4400.

 

Honey bee species x weeks interaction

The data for incoming foragers of honey bee species revealed significant differences among Honey bee species, weeks and interaction of honey bee species by weeks (Table 5). The maximum in-coming foraging was recorded by A. cerana in langstroth at W1 (46.55), whereas A. mellifera in langstroth hive revealed minimum in-coming foraging at W2 (40.66). Li et al. (2019) stated that high temperatures can adversely affect bees. They not only affect the survival and water loss, but also stimulate oxidative stress in bees. Also, A. cerana was more tolerant than A. mellifera. These finding were in coincidence to our research work.

Time intervals x weeks interaction

The analyzed data of in-coming foragers against time intervals and weeks data were given in Table 6. Time intervals, weeks and their interaction was significantly different at 5% level of significance. The maximum in-coming foraging of bee species was recorded at time T1 and week W1 (54.00) whereas minimum in-coming foraging was recorded at time T3 and week W5 (37.44). Week and peak hour for foraging was recorded for W1 (45.63) and T1 (49.86), contrary to our findings Verma and Dulta (2015) concluded that 1100-1330 hrs is best time for foraging. The difference in the results can be due to the altitude and environmental difference.

Foragers returned with pollens

Honey bee species x time intervals interaction

The data for honey bee species and time intervals were given in Table 7. Significant differences were recorded for honey bee species, time interval and the interaction of both. The maximum foragers returned with pollens are A. cerana in traditional mud hive at time T1 (33.50), whereas minimum foragers returned with pollens are A. mellifera in Langstroth hive at time T3 (16.62). Similar to our results, Zhang et al. (2019) stated that A. cerana do more foraging trips as compare to A. mellifera.

 

Table 5: In-coming foragers Honey bee species x Weeks mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

H1

44.11 cde

40.66 j

41.77 ij

43.11 efgh

42.77 fghi

43.66 def

44.55 bcd

44.44 bcd

43.13 b

H2

46.55 a

42.55 fghi

42.66 fghi

43.77 def

43.44 defg

44.33 bcde

41.55 ij

42.22 ghi

43.38 b

H3

46.22 a

44.44 bcd

43.11 efgh

46.00 a

42.11 hi

45.33 abc

44.66 bcd

45.44 ab

44.66 a

Mean

45.63 a

42.55 d

42.51 d

44.29 bc

42.77 d

44.44 b

43.59 c

44.03 bc

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Weeks interaction 1.2446; Critical value for Honey bee species 0.4400; Critical Value for weeks 0.7186

 

Table 6: In-coming foragers Time intervals x Weeks mean interaction of Honey bee species in Spring, 2020.

Time intervals

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

T1

54.00 a

46.88 e

49.44 cd

50.88 b

49.44 cd

50.55 bc

48.55 d

49.11 d

49.86 a

T2

42.00 hi

42.11 hi

40.44 jk

43.22 gh

41.44 ij

43.55 g

44.00 fg

44.88 f

42.70 b

T3

40.88 ij

38.66 lmn

37.66 mn

38.77 lm

37.44 n

39.22 kl

38.22 lmn

38.11 lmn

38.62 c

Mean

45.63 a

42.55 d

42.51 d

44.29 bc

42.77 d

44.44 b

43.59 c

44.03 bc

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Time intervals x Weeks interaction 1.2446; Critical value for time intervals 0.4400; Critical value for weeks 0.7186

 

Table 7: Foragers returned with pollens Honey bee species x Time intervals mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Time intervals

Mean

T1

T2

T3

H1

29.50 c

20.37 e

16.62 g

22.16 c

H2

31.70 b

20.83 e

16.83 g

23.12 b

H3

33.50 a

22.91 d

18.29 f

24.90 a

Mean

31.56 a

21.37 b

17.25 c

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Time intervals interaction 0.8463; Critical Value for Honey bee species 0.488; Critical value for time intervals 0.4886

 

Honey bee species x weeks interaction

The recorded data of honey bee species and weeks were given in Table 8. Honey bee species, weeks means and their interaction revealed significant differences. The maximum and minimum foragers returned with pollens were A. cerana in Langstroth hive in W1 (33.55) and A. mellifera in Langstroth hive at W7 (14.88). Raj et al. (1993) stated that the pollen load availability varies from day to day and both the species could have minor difference in their pollen trips. Same results have been recorded in our study. Zhang et al. (2019) also confirmed the results that A. cerana being higher forager species than A. mellifera.

Time intervals x weeks interaction

Significant differences were recorded for time intervals, weeks and interaction of time interval by weeks among the foragers returned with pollens (Table 9). The maximum foragers returned with pollens were at time T1 (0700-0800 hrs) during week W1 (40.66), whereas minimum value of 9.55 foragers were recorded at time T3 (1100-1200 hrs) and week W6. Similar to our finding, Joshi and Joshi (2010) stated that pollen availability decreases from morning to evening. Raj et al. (1993) also revealed that A. mellifera bees carried maximum average pollen loads at 1200 hrs, whereas A. cerana bees carried maximum average pollen load at 0900 hrs.

Foragers returned with water/nectar

Honey bee species x Time intervals interaction: The analyzed data of foragers returned with water revealed significant differences among honey bee species, time intervals and interaction of honey bee species and time interval (Table 10). The maximum foragers returned with water/nectar are A. mellifera in Langstroth hive at time T3 (22.16) and the minimum foragers returned with water/nectar are A. cerana in Langstroth hive at time T1 (17.75). Li et al. (2019) revealed that A. mellifera lost more water as compare to A. cerana and his finding were similar to our study. He also stated that higher temperature can adversely affect the foraging of honey bees.

 

Table 8: Foragers returned with pollens Honey bee species x Weeks mean interaction Honey bee species in Spring, 2020.

Honey bee species

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

H1

30.33 b

27.11 cd

25.11 ef

26.00 de

23.55 g

15.11 i

14.88 i

15.22 i

22.16 c

H2

33.55 a

27.66 c

25.88 de

26.55 cd

24.22 fg

16.22 i

15.11 i

15.77 i

23.12 b

H3

32.77 a

29.88 b

26.88 cd

29.11 b

24.66 efg

18.44 h

18.33 h

19.11 h

24.90 a

Mean

32.22 a

28.22 b

25.96 d

27.22 c

24.14 e

16.59 f

16.11 f

16.70 f

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Weeks interaction 1.3820; Critical Value for Honey bee species 0.4886; Critical Value for weeks 0.7979.

 

Table 9: Foragers returned with pollens Time intervals x Weeks mean interaction of Honey bee species in Spring, 2020.

Time intervals

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

T1

40.66 a

33.00 cd

34.33 bc

32.11 d

34.66 b

27.44 ef

25.44 h

24.88 h

31.56 a

T2

28.44 e

27.11 efg

25.88 gh

27.00 fg

24.66 h

12.77 k

12.66 k

12.44 k

21.37 b

T3

27.55 ef

24.55 h

17.66 j

22.55 i

13.11 k

9.55 l

10.22 l

12.77 k

17.25 c

Mean

32.22 a

28.22 b

25.96 d

27.22 c

24.14 e

16.59 f

16.11 f

16.70 f

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Time intervals x Weeks interaction 1.3820; Critical Value for Time intervals 0.4886; Critical Value for weeks 0.7979.

 

Table 10: Foragers returned with water/nectar Honey bee species x Time intervals mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Time intervals

Mean

T1

T2

T3

H1

18.87 d

21.87 ab

22.16 a

20.97 a

H2

17.75 e

21.20 b

21.87 ab

20.27 b

H3

18.25 de

21.50 ab

20.12 c

19.95 b

Mean

18.29 b

21.52 a

21.38 a

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Time intervals interaction 0.8742; Critical Value for Honey bee species 0.5047; Critical Value for time intervals 0.5047.

 

Honey bee species x weeks interaction

The analyzed data of honey bee species and weeks were given in Table 11. Significant differences among the foragers were recorded for honey bee species, weeks interval and interaction of both. The maximum and minimum foragers returned with water/nectar were A. mellifera in week W7 (29.66) and A. cerana in Langstroth hive in week W1 (13.11), respectively. Zhang et al. (2019) stated that A. cerana are less consumer of sugar as compare to A. mellifera similarly Li et al. (2019) stated that water loss occurs much higher in A. mellifera as compare to A. cerana.

Time intervals x weeks interaction

It is revealed from Table 12 that foragers returned with water/ nectar showed significant differences for time intervals, weeks and their interaction. The maximum foragers returned with water/nectar at time T2 during week W8 (32.44) whereas minimum foragers returned with water/nectar were at time T3 and week W1 (13.33). Our findings are in coincidence with Li et al. (2019) who stated that higher ambient temperature can adversely affect the foraging behavior of honey bee species. In each time interval and week, the temperature was increasing which increased the number of foragers to bring water along with them to compete environmental stress (Li et al., 2018).

 

Table 11: Foragers returned with water/nectar Honey bee species x Weeks mean interaction of Honey bee species in Spring, 2020.

Honey bee species

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

H1

13.77 fgh

13.55 fgh

16.66 e

17.11 e

19.22 d

28.55 ab

29.66 a

29.22 ab

20.97 a

H2

13.11 h

14.88 f

16.77 e

17.22 e

19.22 d

28.11 b

26.44 c

26.44 c

20.27 b

H3

13.44 gh

14.55 fg

16.66 e

16.88 e

17.44 e

28.00 b

26.33 c

26.33 c

19.95 b

Mean

13.44 f

14.33 e

16.70 d

17.07 d

18.63 c

28.22 a

27.48 ab

27.33 b

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Honey bee species x Weeks interaction 1.4276; Critical Value for Honey bee species 0.5047; Critical Value for weeks 0.8242.

 

Table 12: Foragers returned with water/nectar Time intervals x Weeks mean interaction of Honey bee species in Spring, 2020.

Time intervals

Weeks

Mean

W1

W2

W3

W4

W5

W6

W7

W8

T1

13.44 jk

13.88 ijk

15.11 hi

18.66 f

14.77 ij

23.11 e

23.11 e

24.22 de

18.29 b

T2

13.55 jk

15.00 hi

15.00 hi

16.22 gh

16.77 g

31.88 a

31.33 a

32.44 a

21.52 a

T3

13.33 k

14.11 ijk

20.00 f

16.33 gh

24.33 de

29.66

28.00 c

25.33 d

21.38 a

Mean

13.44 f

14.33 e

16.70 d

17.07 d

18.63 c

28.22 a

27.48 ab

27.33 b

Mean followed by same letters are not significantly different at 5% level of significance (LSD test). Critical Value for Time intervals x Weeks interaction 1.4276; Critical value for time intervals 0.5047; Critical Value for weeks 0.8242.

 

Table 13: Pollen source preferences of Honey bee species in Spring, 2020.

S. No.

A. mellifera (H1)

A. cerana (Langstroth hive) (H2)

A. cerana (Traditional mud hive) (H3)

1

Eucalyptus camaldulensis

Eucalyptus camaldulensis

Eucalyptus camaldulensis

2

Amaryllis belladonna

Amaryllis belladonna

Amaryllis belladonna

3

Brassica napus

Brassica napus

Brassica napus

4

Taraxacum japonicum

Taraxacum japonicum

Taraxacum japonicum

5

--

Rumex dentatus

Rumex dentatus

6

--

Althaea officinalis

Althaea officinalis

 

Pollen source preference of honey bee species

Different honey bee species have different pollen prefernces. Reddy et al. (2015) stated that A. cerana and A. mellifera may have slight difference in their pollen sources due to their own preference. A. cerana prefer tall trees while A. mellifera prefer short herbs in Japan. Hu and Wu (2019) argued that the pollen composition in between A. cerana and A. mellifera may differ. Yang et al. (2020) stated that A. mellifera are more likely to bring pollens from the near sources as compare to A. cerana. Current study shows resemblance with the previous studies (Table 13).

Ahmad et al. (2017) stated that A. mellifera carries much heavy pollen loads having more pollen grains and uni-floral pollen loads as compare to A. cerana. Hu and Wu (2019) stated that A. mellifera carries much pollens per individual than A. cerana. Similar results were also recorded in current study, where A. mellifera (H1) brought more pollens by weight than A. cerana in Langstroth hive (H2) and A. cerana in traditional mud hive (H3) (Table 14).

 

Table 14: Pollen difference by weight of Honey bee species.

Honey bee spp

A. mellifera

(H1)

A. cerana (Langstroth hive) (H2)

A. cerana (Traditional mud hive) (H3)

R1

12.004 g

07.065 g

07.923 g

R2

11.028 g

06.569 g

07.004 g

R3

10.438 g

04.313 g

04.812 g

R4

06.383 g

03.002 g

03.991 g

Total

39.853 g

20.949 g

23.730 g

 

Chemical analysis of honey

Ash content: Margaoan et al. (2012) stated that ash content of honey bee pollens may vary from 1.75-3.25% whose results are in accordance with the current study (Figure 1).

 

Moisture content: Margaoan et al. (2012) stated that the moisture content of honey bee pollens may vary from 17.59-29.55%. Thakur and Nanda (2020) stated that fresh bee pollens moisture content may vary from 7-30%. These results show similarity with the current results (Figure 2).

 

Total sugar content: Aqueous medium: The sugar analysis was carried out in aqueous medium through spectrophotometer by passing each sample from 450 nm light. It was concluded that the pollens brought by the honey bee species A. mellifera (H1), A. cerana in Langstroth hive (H2) and A. cerana in traditional mud hive (H3) were having 2.07%, 1.30% and 1.31% absorbance of 450 nm light, respectively. While the standard glucose 1%, 3% and 5% was having total sugar absorbance of 0.85%, 1.75% and 2.08% respectively. H1 was having significant sugar content results to 5% glucose standard while H2 and H3 were lying below 3% glucose results (Figures 3, 4, 5).

 

Acidic medium: In acidic medium the same method was applied apart from medium, the pollens of H1, H2 and H3 absorbed 450 nm light at 2.863%, 1.953% and 1.958%, respectively. In acidic medium H1 was having higher (2.867%) absorbance at 450 nm light than 5% glucose standard (2.08 %) whereas H2 and H3 were having 1.953% and 1.958% absorbance, respectively. This value was lower as compare to 5% glucose D % absorbance but higher than 3% glucose D % absorbance (1.75%) (Figures 6, 7, 8).

 

 

 

 

 

Conclusions and Recommendations

It has been concluded that A. cerana in traditional mud hive (H3) shows better foraging performance as compare to A. mellifera (H1) and A. cerana in Langstroth hive (H2). T1 (07:00-08:00 am) was recorded as peak foraging performance time. The ratio of foragers returning with pollens and water is affected by high temperature as foragers returning with water increases with increase in temperature. A. cerana brought pollens from six sources while A. mellifera brought pollens from four sources, this revealed that A. cerena is more diverse than A. mellifera. The ash and moisture content of all the three Honey bee species was 3% and 16%, respectively, whereas the total sugar content results obtained through spectrophotometer in aqueous medium were 2.07% for A. mellifera, 1.30% for A. cerana in Langstroth hive and 1.31% for A. cerana in traditional mud hive.

Acknowledgements

Authors are grateful to The Directorate of Non-Timber Forest Products (NTFP), Forest Department, Khyber Pakhtunkhwa, Peshawar for collaboration on this study.

Novelty Statement

This study is helpful in understanding the foraging behavior and peak foraging performance of honey bees as it is reported for the first time in Peshawar. This will also help the farmers to move their colony as per preference of the honey bees.

Author’s Contribution

Hamza Iftikhar: Carried out research, data collection, analysis and write-up

Ranra Jalal: Helped in data analysis

Mansoor Ali Shah: Helped in data collection

Syed Anas Shah Bacha: Helped in write-up

Amjid Ali: Helped in editing and graphs designing

Syed Majid Rasheed: Helped in proofreading and editing

Conflict of interest

The authors have declared no conflict of interest.

References

Abou-Shaara, H.F., A.A. Owayss, Y.Y. Ibrahim and N.K. Basuny. 2017. A review of impacts of temperature and relative humidity on various activities of honey bees. Insect. Soc., 64: 455-463. https://doi.org/10.1007/s00040-017-0573-8

Ahmad, S.B., S.A. Dar and B.A. Pandith. 2017. Comparative foraging behaviour of honey bees, Apis cerana F. and Apis mellifera L. (Hym: Apidae) on apple bloom. J. Ent. Zool. Stud., 5(1): 474-482.

Bell, R.R., E.J. Thornber, J.L.L. Seet, M.T. Groves, N.P. Ho and D.T. Bell. 1983. Composition and protein quality of honey bee-collected pollen of Euclyotus marginata and Euclyptus calophylla. J. Nutr., 113: 2479-2484. https://doi.org/10.1093/jn/113.12.2479

Blazyte-Cereskiene, L., G. Vaitkeviciene, S. Venskutonyte and V. Buda. 2010. Honey bee foraging in spring oilseed rape crops under high ambient temperature conditions. Zemdirbyste, 97(1): 61-70.

Brummer, Y. and S.W. Cui. 2005. Understanding carbohydrates analysis. Food carbohydrates: Chemistry, physical properties and applications. Chapter 02.

Cartin, W., R. Bommarco, G. Carre, E. Lamborn, N. Morison, T. Petanidou, S.G. Potts, S.P.M. Roberts, H. Szentgyorgyi, T. Tscheulin, B.E. Vaissiere, M. Woyciechowski, J.C. Biesmeijer, W.E. Kunin, J. Settele and I.S. Dewenter. 2008. Measuring bee diversity in different European habitats and bio geographical regions. Ecol. Monogr., 78(4): 653-671. https://doi.org/10.1890/07-1292.1

Chinkangsadarn, S. and L. Kafle. 2024. Invasive ant detection: Evaluating honeybee learning and discrimination abilities for detecting Solenopsis invicta Odor. Insects, 15(10): 808. https://doi.org/10.3390/insects15100808

Cook, C.N., T. Mosqueiro, C.S. Brent, C. Ozturk, J. Gadau, N. Pinter-Wollman and B.H. Smith. 2019. Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honey bee scouts and recruits. J. Anim. Ecol., 88: 236–246. https://doi.org/10.1111/1365-2656.12911

El-Ghouizi, A., M. Bakour, H. Laaroussi, D. Ousaaid, N. El-Menyiy, C. Hano and B. Lyoussi. 2023. Bee pollen as functional food: Insights into its composition and therapeutic properties. Antioxidants, 12(3): 557. https://doi.org/10.3390/antiox12030557

Gratzer, K., F. Susilo, D. Purnomo, S. Fiedler and R. Brodschneider. 2019. Challenges for beekeeping in indonesia with autochthonous and introduced bees. Bee World, 96(2): 40–44. https://doi.org/10.1080/0005772X.2019.1571211

Hu, L. and X. Wu. 2019. The difference in pollen harvest between Apis mellifera and Apis cerana in a Tibetan alpine meadow. J. Mt. Sci., 16: 1598-1605. https://doi.org/10.1007/s11629-018-5245-2

Hung, K.L.J., J.M. Kingston, M. Albrecht, D.A. Holway and J.R. Kohn. 2018. The worldwide importance of honey bees as pollinators in natural habitats. Proc. R. Soc. B Biol. Sci., 285(1870): 20172140. https://doi.org/10.1098/rspb.2017.2140

Joshi, N.C. and P.C. Joshi. 2010. Foraging behaviour of Apis spp. on apple flowers in a subtropical environment. N. Y. Sci. J., 3(3): 71-76.

Kieliszek, M., K. Piwowarek, A.M. Kot, S. Blazejak, A. Chlebowske-Smigiel and I. Wolska. 2018. Pollen and bee bread as new health-oriented products: A review. Trends Food Sci. Tech., 71: 170-180. https://doi.org/10.1016/j.tifs.2017.10.021

Li, G., H. Zhao, Z. Liu, H. Wang, B. Xu and X. Guo. 2018. The wisdom of honey bee defenses against environmental stresses. Front. Microbiol., 9: 722. https://doi.org/10.3389/fmicb.2018.00722

Li, X., W. Ma, J. Shen, D. Long, Y. Feng, W. Su, K. Xu, Y. Du and Y. Jiang. 2019. Tolerance and response of two honey bee species Apis cerana and Apis mellifera to high temperature and relative humidity. PLoS One, 14(6): e0217921. https://doi.org/10.1371/journal.pone.0217921

Margaoan, R., L.A. Marghitas, D.S. Dezmirean, O. Bobis and C.M. Mihai. 2012. Physical-chemical composition of fresh bee pollen from Transylvania. Bul. UASVM Anim. Sci. Biotechnol., 69: 351-355.

Nabila, M.A., M. Ali, M. Zafar, S. Sultana, S. Majeed, G. Yaseen and S. Ahmad. 2022. Palynological diversity of Melliferous flora around Apiaries from District Mardan Khyber Pakhtunkhwa-Pakistan. Bot. Rev., 88: 299–332. https://doi.org/10.1007/s12229-021-09268-w

Natapot, W., J. Ascher, P. Basu, V. Belavadi, A. Brockmann and D. Buchori, J. Dorey, H. Alice, K. Smitha, H. Ngo, P. Williams, C.D. Zhu, A. Dharam, B. Kamal, C. Bhatta, B. Renee, B. Silas, C. Cervancia, C. Nontawat and O. Michael. 2023. Opportunities and challenges in Asian bee research and conservation. Biol. Cons., 285: 110173. https://doi.org/10.1016/j.biocon.2023.110173

Oldroyd, B.P. and S. Wongsiri. 2009. Asian honey bees: Biology, conservation, and human interactions. Harvard University Press. https://doi.org/10.2307/j.ctv2drhcfb

Raj, D., V.K. Rana and N. Devi. 1993. Comparative studies on pollen loads and pollen constancy of A. mellifera L. and A. cerana indica F. on rapeseed. J. Entomol. Res., 17(1): 43-48.

Ramalho, M., L.S. Guibu, T.C. Giannini, A. Kleinert-Giovannini and V.L. Imperatriz-Fonseca. 1991. Characterization of some southern Brazilian honey and bee plants through pollen analysis. J. Apic. Res., 30(2): 81-86. https://doi.org/10.1080/00218839.1991.11101238

Reddy, P.V.R., T. Rashmi and A. Verghese. 2015. Foraging activity of Indian honey bee, Apis cerana in relation to ambient climate variables under tropical conditions. J. Environ. Biol., 36(3): 577-581.

Russell, A.L., A.M. Fetters, E.I. James and T. Ashman. 2021. Pollinator effectiveness is affected by intra-individual behavioral variation. Oecologia, 197: 189–200. https://doi.org/10.1007/s00442-021-05016-4

Thakur, M. and V. Nanda. 2020. Composition and functionality of bee pollen: A review. Trends Food Sci. Technol., 98: 82-106. https://doi.org/10.1016/j.tifs.2020.02.001

Usman, M., M. Hasnain, S. Banaras, M. Akram, Q. Abbas, J.A. Shah, S. Tabasum, S.A. Shah, A. Raza. M.N. Khan and M. Jamil. 2022. Potential emerging constraints and management strategies of different honeybee species in Pakistan: A review. CABI Reviews. https://doi.org/10.1079/cabireviews202217058

Verma, L.R. and P.C. Dulta. 2015. Foraging behavior of A. cerana indica and A. mellifera in pollination Apple flowers. J. Apic. Res., 25(4): 197-201. https://doi.org/10.1080/00218839.1986.11100717

Yang, H., J. Sun, P. Tang, C. Ma, S. Luo and J. Wu. 2020. The ratio of sunflower pollens foraged by Apis mellifera is more than that of Apis cerana does during sunflower blooming. Sociobiology, 67(2): 256-260. https://doi.org/10.13102/sociobiology.v67i2.4408

Yang, M., 2009. Studies on mixed-species colonies of Honey bees A. cerana and A. mellifera. Rhodes University. Chapter, 1: 19-25.

Zhang, C., S. Pokhrel, Z. Wu, X. Miao, Z.Y. Haung and W. Yang. 2019. Longevity, food consumption, and foraging performance of A. cerana and A. mellifera in mixed colonies. Apidologie, 50: 153-162. https://doi.org/10.1007/s13592-018-0626-7

To share on other social networks, click on any share button. What are these?

Pakistan Journal of Zoology

November

Pakistan J. Zool., Vol. 56

Featuring

Click here for more

Subscribe Today

Receive free updates on new articles, opportunities and benefits


Subscribe Unsubscribe