Honey bee (Apis mellifera jemenitica) colony performance and queen fecundity in response to different nutritional practices.

Honey bee colony nutritional dynamics depend on the availability of floral resources throughout a countryside with varying forage circumstances. Few studies quantify the queen fecundity and colony performance about certain management approaches on a broad scale. The present study was conducted to investigate the queen bee fecundity and various colony performance parameters in response to different nutritional practices, i.e., Group-I, supplied with sucrose solution (1:1; w/v), Group-II, provided with locally available commercial pollen substitute, Group-III, supplied with both sucrose solution + locally available commercial pollen substitute, and Group-IV without any sugar solution and pollen substitute. Our results demonstrated that eggs laid by queen bees were significantly higher (1241.83 ± 46.24) in Group-III than in other groups over the time of observations. Similarly, a significant difference was noticed in the mean sealed worker brood area and honey store area between the different groups of management practices. Both, the max mean sealed worker brood area (2153.53 ± 29.18 cm2) and max mean honey store area (1713.33 ± 12.06 cm2) were observed in Group-III while, the mini mean sealed worker brood area (1066.53 ± 20.18 cm2) and mini mean honey store area (1058.86 ± 4.07 cm2) were observed in Group-IV. In contrast, a non-significant difference was observed in pollen stores between Group-II and Group-III (p > 0.005). Current findings add to our understanding of the mechanisms that underpin large-scale controlled colony performance when the natural pollens resources are insufficient.

Introduction

The world is majorly populated with pollinator-dependent plants. Around 200,000 distinct animal species serve as pollinators on a global scale (Ahmad et al., 2021a, Devi et al., 2021). Among these, 1000 are vertebrates such as birds, bats, and tiny mammals, while the remainder is invertebrates such as bees, beetles, butterflies, flies, and moths (Abrol, 2012). Pollinators pollinate approximately 180,000 different plant species worldwide (Council, 2007, Abrol, 2012). Notably, honey bees are among the most efficient pollinator species and pollinate 87.5% of angiosperms. A honey bee can visit around 2000 flowers daily during foraging of nectar and pollen (Ollerton et al., 2011, Abrol, 2012, Abbasi et al., 2021, Devi et al., 2021). In addition, honey bees produce various natural products such as honey, royal jelly, bee bread, and propolis (Ahmad et al., 2020, Jagdale et al., 2021). The Apis mellifera jemenitica governed the entire beekeeping industry of Saudi Arabia due to its good foraging ability to produce more honey than A. m. carnica and A. m. lamarki of Egypt (Al-Ghamdi et al., 2013, Al-Ghamdi et al., 2021). On the other hand, Saudi Arabian beekeepers are not fully exploiting beekeeping’s competitive advantages with A. m. jemenitica due to the low performances of bee colonies (Adgaba et al., 2014). Moreover, the decline of A. m. jemenitica colonies is attributed to three key factors that badly influence the colony health of honey bees; poor nutrition, pesticide exposure, and pathogens (Albarrak and Gray, 2017, Ansari et al., 2017, Iqbal et al., 2019). The honey bee queen is a central part of the colony and solely regulates the population of honey bees and the unity of the colony (Perumal et al., 2021).

The queen’s fecundity is a critical factor for the long-term survival of the honey bee colony, mainly depending upon younger queens (Winston, 1980, Winston, 1991, Amiri et al., 2017). A high-fecundity queen allows a colony to have a maximum bee population that is very productive. The queen bee relies on worker bees for constant care because sustained queen egg-laying does not occur without worker bees. The egg-laying by the queen bee is the result of the queen’s and workers’ synchronized efforts (Fine et al., 2018). Colony performance includes colony strength and productivity (Chemurot and de Graaf, 2019). The colony strength is determined by the number of adult worker bees in the hive, brood pattern, and the flight activity around the hive entrance (Pokhrel et al., 2006, Delaplane et al., 2013, Taha and AL-Kahtani, 2019, Grant et al., 2021) while colony productivity is measured in honey production and pollen collection (Hoover and Ovinge, 2018). The physical characters of the queen are associated with colony performance and were investigated using a different behavioral attribute by Akyol et al., 2008, Hatjina et al., 2014. The honey bee colony performance is crucial in beekeeping (Al-Ghamdi et al., 2021). The sharp decline of A. m. jemenitica is documented by Al-Ghamdi et al. (2017). It is associated with a mated queen’s low reproductive potential or fecundity (Al-Sarhan et al., 2019).

Queen-size is almost regulated by the larval rearing situation, mostly the royal jelly consumed by the larvae during their growth (Hartfelder et al., 2015). The queen’s fertility is determined by examining her ovaries and spermatheca. The size of these two organs is linked with more bodyweight when fed with sugar-based supplementary diets during beekeeping (Tarpy et al., 2011, De Souza et al., 2013, McAfee et al., 2020). Honey bee colonies are fed on commercially available pollen substitute diets when the natural pollen resources are scarce. Artificial pollen substitutes may affect bee physiology in addition to their primary nutritional role (Al-Ghamdi et al., 2011, Ahmad et al., 2021b). For instance, sugar syrup is the most often used artificial diet for honey bees. It is made by combining sugar and water in a 2:1 ratio (Genç and Aksoy, 1993). The different types of carbohydrates also significantly enhance the gut bacteria of the queen (Taylor et al., 2019). The sugar-based supplemental diet increased the honey bee’s reproductive development and fertility potential when mixed with juvenile hormones (Daiana et al., 2019, Frizzera et al., 2020).

The present study was conducted to demonstrate the effect of various nutritional management practices on the fecundity of honey bee queens. In addition to investigating the potential impacts of different nutritional practices on colony performance, including sealed brood area, pollen, and honey stored area. This study helps determine the optimal sucrose solution for maintaining the optimal population of the colony and its performance in the scarcity of natural pollen.

Materials and methods

Experimental honeybee colonies and treatments

The experiment was conducted at the Unit of Bee Research and Honey Production (UBRHP), King Khalid University, Abha, Saudi Arabia. This study used native honey bee (Apis mellifera jemenitica) colonies. All bee colonies were kept in standard Langstroth hives containing eight frames and aligned concerning equal colony strength, sealed brood area, and food stocks in June 2021. Every investigational group comprised five bee colonies and the mated queen age with one year. Group-I was supplied with sucrose solution (1:1; w/v) by using an internal sugar feeder, and Group-II was provided with a locally available commercial pollen substitute. At the same time, Group-III was given both sucrose solution (1:1) by using an internal sugar feeder and locally available commercial pollen substitute. Group-IV was controlled without any sugar solution and pollen substitute. All other management applications applied to each bee colony were the same throughout the experiments. In addition, allow the bees to forage around crops and urban residential neighborhoods freely.

Effect of various management practices on fecundity

Above mentioned four groups were selected for this experiment. An old frame was placed in the queen cage barrier with a healthy queen to count the egg numbers. The queen laid eggs on an old comb within one day in the queen cage barrier. The number of eggs laid by the queen per frame per day was recorded (Fig. 1). Eggs laid by the queen was tracked in each colony for 15 days.

Fig. 1

A frame inside the queen cage barrier (a); bees and queen working on the frames inside the queen cage barrier (b); a queen bee with some attendants prior to be caged (c); eggs laid by the queen bee (d).

Worker sealed brood area (cm2)

The worker sealed brood area was assessed with a modified grid system. Squares of the grid had a surface area of 25 cm2. The sealed brood frame area was marked and measured with a grid.

Food stores (pollen and honey)

Pollen stored in each colony was measured by placing a frame grid consisting of 25 cm2 over each side of every frame inside each bee colony and calculated the summing the number of grid cells occupied with pollen.

Similarly, honey stored in each colony was measured by placing a frame grid consisting of 25 cm2 and summing the number of grid cells with occupied honey.

Statistical analysis

Fecundity, sealed brood area, food stored were compared between the treatments. All statistical results were analyzed and calculated by SPSS software according to the analysis of variance (ANOVA). The figures were prepared by GraphPad Prism software (version 8). The Tukey posthoc test was conducted for multiple comparisons between treatment groups at a significance level (p = 0.05).

Results

Effect of different nutrition practices on fecundity

Overall, a statistically significant difference was detected between the effect of different nutritional practices and eggs laid by the queen bee over the time of observations (F (3, 296) = 37.971, p = 0.001). The queen laid max eggs (1241.83 ± 46.24) when fed on pollen substitute plus sucrose solution, and the lower number of eggs were observed in the control group (822.82 ± 31.62). The eggs laid by the queen were (1127.33 ± 10.56) and (908.01 ± 26.17) when either fed separately on commercially available pollen substitute and sucrose solution, respectively (Fig. 2).

Fig. 2

Honey bee (Apis mellifera jemenitica) queen fecundity in response to various nutrition practices, i.e., Group-I = bee colonies provided with sucrose solution (1:1; w/v), Group-II = bee colonies supplied with locally available commercial pollen substitute, Group-III = bee colonies given with both sucrose solution + locally available commercial pollen substitute, and Group-IV = bee colonies without any sugar solution and pollen substitute.

Effect of various nutritional management practices on brood area

A significant effect of various nutritional management was observed on sealed brood area of bee colonies (F (3, 176) = 257.93, p = 0.001). There was a fluctuating trend in the sealed brood area over the time of observations (Fig. 3). The mean highest sealed brood area (2153.53 ± 29.18 cm2) was recorded in Group-III, while less brood area (1066.53 ± 20.18 cm2) was noticed in the control group. The mean sealed worker brood area in Group-I was 1477.23 ± 15.58 cm2 and in Group-II was 1682.53 ± 40.81 cm2.

Fig. 3

Effect of different management practices on worker sealed brood area (cm2/ colony). Group-I = bee colonies provided with sucrose solution (1:1; w/v), Group-II = bee colonies supplied with locally available commercial pollen substitute, Group-III = bee colonies given with both sucrose solution + locally available commercial pollen substitute, and Group-IV = bee colonies without any sugar solution and pollen substitute.

Effect of various nutritional practices on food store (pollen and honey)

A significant difference was recorded in pollen store between the treatment’s groups over the time of observations (F (3, 176) = 44.83, p = 0.001). No significant difference was found in the pollen stored between Group-II and Group-III (p > 0.005) (Table 1).

Table 1

Effect of different management practices on queen fecundity and honey bee colony performance.

Treatment	Fecundity	Worker sealed brood area (cm2)	Pollen store area (cm2)	Honey store area (cm2)
	Mean ± S. Error	Mean ± S. Error	Mean ± S. Error	Mean ± S. Error
Group-I	908.01 ± 26.17b	1477.23 ± 15.58 a	646.76 ± 16.98b	1425.53 ± 19.31 a
Group-II	1127.33 ± 10.56 a	1682.53 ± 40.81b	756.22 ± 17.91 a	1527.03 ± 29.15b
Group-III	1241.83 ± 46.24 a	2153.53 ± 29.18c	780.62 ± 12.80 a	1713.33 ± 12.06c
Group-IV	822.82 ± 31.62b	1066.53 ± 20.18 d	571.29 ± 8.71c	1058.86 ± 4.07 d

Small letters within each column represent statistically significant differences (p < 0.05). Group-I = bee colonies provided with sucrose solution (1:1; w/v), Group-II = bee colonies supplied with locally available commercial pollen substitute, Group-III = bee colonies given with both sucrose solution + locally available commercial pollen substitute, and Group-IV = bee colonies without any sugar solution and pollen substitute.

The maximum mean pollen store was noticed in Group-III (780.62 ± 12.80 cm2) followed by Group-II (756.22 ± 17.91 cm2) and Group-I (646.76 ± 16.98 cm2). The least mean pollen stored was observed by the control group colonies (571.29 ± 8.71 cm2) (Fig. 4).

Fig. 4

Effect of nutritional management practices on pollen store area (cm2/colony). Group-I = bee colonies provided with sucrose solution (1:1; w/v), Group-II = bee colonies supplied with locally available commercial pollen substitute, Group-III = bee colonies given with both sucrose solution + locally available commercial pollen substitute, and Group-IV = bee colonies without any sugar solution and pollen substitute.

Similarly, a significant result was noticed on the honey store are between different treatment colony groups over the time of observations (F (3, 176) = 219.17, p = 0.001). A significant max mean honey store area was recorded in Group-III 1713.33 ± 12.06 cm2, and the least mean honey store area was observed in Group-IV (control), which was 1058.86 ± 4.07 cm2). The honey store area in Group-I and Group-II was (1425.53 ± 19.31 cm2) and (1527.03 ± 29.15 cm2), respectively (Fig. 5).

Fig. 5

Effect of various nutritional management practices on honey store area (cm2/colony). Group-I = bee colonies provided with sucrose solution (1:1; w/v), Group-II = bee colonies supplied with locally available commercial pollen substitute, Group-III = bee colonies given with both sucrose solution + locally available commercial pollen substitute, and Group-IV = bee colonies without any sugar solution and pollen substitute.

Discussion

Nutrition, particularly pollen, has a well-known impact on honey bee health and colony development (Stevanovic et al., 2010, Omar et al., 2017). In the present study, we compared the effect of various nutritional management practices on queen fecundity and colony performance of honey bees. Our results demonstrated different nutritional management practices significantly impacted queen fecundity and colony performance. The queen fecundity was significantly higher in Group-III (pollen substitute plus sucrose solution) than in other nutritional management practices. The commercially available pollen substitute has a lot of protein content and minerals and vitamins; thus, the availability of protein and sucrose solution to the bee colony resulted in the high fecundity of queen bees. Similarly, a statistically significant difference was found in the sealed worker brood area and honey store area (cm2) between the different groups of honey bees’ colonies over the time of observations. However, in the case of the pollen store area, a non-significant difference was recorded between Group-II and Group-III of honey bee colonies.

Remarkably, the honey bee queens are of great importance for bee colonies and beekeeping activities (Dolasevic et al., 2020). Previously, the impact of different diets on the quality of Apis mellifera queens has been studied (Dolasevic et al., 2020). In addition, the effect of food on the different traits of the queens of A. m. anatoliaca and A. m. meda subspecies was investigated (Gençer et al., 2000, Mahbobi et al., 2012). Our study investigated the impact of various nutritional practices on queen fecundity and colony performance. Our findings demonstrated that sucrose syrup solution with artificial pollen substitute enhanced the fecundity, sealed brood area and food storage area than sucrose syrup alone and pollen substitute alone. Ricigliano et al. (2018) suggested that the performance and health of honey bee colonies are heavily influenced by queen quality and availability of nutrition. Recently, Paray et al., (2021) reported that the number of eggs laid by the queen and worker sealed and unsealed brood reared is reduced, but the amount of stored food available determines the extent of the reduction. Many scientists have devised numerous commercially available artificial food recipes for honey bees. These diets contain a balanced nutritious composition for bees and are acceptable, digestible, and materially affordable. However, more research is required to determine which components of commercially available pollen substitute positively affect queen fecundity. In our findings, variation of egg-laying between groups suggested that external factors may impact fecundity.

Similar findings have been reported in the sealed brood area in previous literature (Sihag and Gupta, 2011, Lamontagne-Drolet et al., 2019, Ahmad et al., 2021b); various pollen substitutes increased the worker brood area. However, our results are inconsistent with the findings of Ali (2011), who reported that the worker brood area was 2813.13 cm2/colony, 1730.94, and 1867 cm2/colony in different groups. Our results revealed that less pollen store area was found between all treatments. Our findings are in line with (Ricigliano et al., 2018). A limited pollen store was recorded over the time of observations, suggesting that most bee colonies had at least intermittent access to natural forage, which could have reduced the impact of commercially available pollen substitutes with natural pollen.

Further investigation is required to determine optimal sucrose solution and commercially available pollen substitute ratios and demonstrate the optimal timing of artificial diets to colonies to enhance fecundity and colony performance.

Conclusions

The main purpose of the present study was to investigate whether commercially available pollen substitutes and sucrose to bee colonies affect queen fecundity and colony performance. Our findings revealed that the different nutritional management practices significantly impacted queen fecundity and colony performance. A significant difference was observed in fecundity, worker sealed brood area, and food storage area in sucrose solution plus commercially available pollen substitute than the other groups. However, further studies are needed to investigate the effect of nutritional management practices on honey bee physiology and colony-level molecular biomarkers.

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.