Next Article in Journal
Primate Conservation Efforts and Sustainable Development Goals in Ecuador, Combining Research, Education and Capacity Building
Next Article in Special Issue
Insights into the Role of Natural Products in the Control of the Honey Bee Gut Parasite (Nosema spp.)
Previous Article in Journal
Luteolin and Chrysin Could Prevent E. coli Lipopolysaccharide-Ochratoxin A Combination-Caused Inflammation and Oxidative Stress in In Vitro Porcine Intestinal Model
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

A Spotlight on the Egyptian Honeybee (Apis mellifera lamarckii)

1
International Research Center for Food Nutrition and Safety, Jiangsu University, Zhenjiang 212013, China
2
Pharmacognosy Group, Department of Pharmaceutical Biosciences, Biomedical Centre, Uppsala University, P.O. Box 591, SE-751 24 Uppsala, Sweden
3
Department of Chemistry, Faculty of Science, Menoufia University, Shebin El-Koom 32512, Egypt
4
International Joint Research Laboratory of Intelligent Agriculture and Agri-Products Processing, Jiangsu Education Department, Nanjing 210024, China
5
Department of Bee Research, Plant Protection Research Institute, Agricultural Research Centre, Giza 12627, Egypt
6
College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China
7
Department of Chemistry, Quaid-i-Azam University, Islamabad 45320, Pakistan
8
School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, China
9
Zoonotic Diseases Department, National Research Centre, Giza 12622, Egypt
10
Avian and Rabbit Diseases Department, Faculty of Veterinary Medicine, University of Sadat City, Menoufia 22857, Egypt
11
PerNaturam GmbH, An der Trift 8, 56290 Gödenroth, Germany
12
Prophy-Institute for Applied Prophylaxis, 59159 Bönen, Germany
13
Faculty of Medicine, Riga Stradins University (RSU), LV-1007 Riga, Latvia
14
Alnahal Aljwal Foundation Saudi Arabia, P.O. Box 617, Makkah 24211, Saudi Arabia
15
Zoology Department, Faculty of Science, Tanta University, Tanta 31527, Egypt
16
Nutrition Department, Food Analysis Division, High Institute of Public Health, Alexandria University, Alexandria 21561, Egypt
17
School of Computing, Engineering and Physical Sciences, University of the West of Scotland, Paisley PA1 2BE, UK
18
Central Agriculture Pesticides Laboratory, Pesticide Analysis Research Department, Agriculture Research Center, Giza 24221, Egypt
19
Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, SE-106 91 Stockholm, Sweden
20
Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
*
Authors to whom correspondence should be addressed.
Animals 2022, 12(20), 2749; https://doi.org/10.3390/ani12202749
Submission received: 30 July 2022 / Revised: 15 September 2022 / Accepted: 27 September 2022 / Published: 13 October 2022
(This article belongs to the Special Issue Apiculture and Challenges for Future)

Abstract

:

Simple Summary

The Egyptian honeybee (Apis mellifera lamarckii) is one of the honeybee subspecies known for centuries since the ancient Egypt civilization. The subspecies of the Egyptian honeybee is distinguished by certain traits of appearance and behavior that were well-adapted to the environment and unique in a way that it is resistant to bee diseases, such as the Varroa disease. The subspecies is different than those found in Europe and is native to southern Egypt. Therefore, a special care should be paid to the vulnerable A. m. lamarckii subspecies and greater knowledge about the risk factors as well as conservation techniques will protect these bees. Additionally, more qualitative and quantitative measures will be taken to obtain deep insights into the A. m. lamarckii products’ chemical profile and biological characters.

Abstract

Egypt has an ongoing long history with beekeeping, which started with the ancient Egyptians making various reliefs and inscriptions of beekeeping on their tombs and temples. The Egyptian honeybee (Apis mellifera lamarckii) is an authentic Egyptian honeybee subspecies utilized in apiculture. A. m. lamarckii is a distinct honeybee subspecies that has a particular body color, size, and high levels of hygienic behavior. Additionally, it has distinctive characteristics; including the presence of the half-queens, an excessive number of swarm cells, high adaptability to climatic conditions, good resistance to specific bee diseases, including the Varro disorder, and continuous breeding during the whole year despite low productivity, using very little propolis, and tending to abscond readily. This review discusses the history of beekeeping in Egypt and its current situation in addition to its morphology, genetic analysis, and distinctive characters, and the defensive behaviors of native A. m. lamarckii subspecies.

1. Introduction

Beekeeping has been conducted for thousands of years; hence, the honeybee and their products have been known in ancient Egypt. Egyptians used bee products in daily life, including honey and wax, as food and in ceremonies. They also recorded their knowledge and practices on templates and tombs [1,2].
The honeybee subspecies Apis mellifera lamarckii is assumed to be the same species as the one discovered during the Pharaohs’ period [3,4]. A. m. lamarckii Cockerell, 1906 is geographically distributed in the Egyptian desert, delta region, Nile valley, and Sudan [5,6,7]. Lamarck’s honeybee was previously known as Apis fasciata Latreille and is considered an offshoot of adansonii. It resembles the lighter, yellow-banded varieties with very dark drones, and the width of the worker cells is identical to that of adansonii from center to center [7]. Lamarck’s bee is described as a good housekeeper but a poor honey producer. Thus, the Carniolan honeybee, which gained popularity because it is peaceful and easy to manage in modern Langstroth hives, thus effectively replaced the A. m. lamarckii in commercial beekeeping in Egypt.
As a result, the native honeybee population in Egypt was suppressed and predominantly centered in the Manfalut area of the Assiut governorate, which was surrounded by hybrids from Europe. A. m. lamarckii was introduced to the Dakhla oasis in 1928, and was utilized there until 1960, when the New Valley Government decided to breed less aggressive bees than A. m. lamarckii [8,9]. A large number of A. m. lamarckii colonies (about 400,000) were found in traditional mud-tube hives in the Assiut Governorate and small populations in isolated oases of Egypt [10]. The A. m. Lamarckii is noticeably smaller and has legs and wings that are shorter. Compared to the European subspecies, its colonies have fewer bees. It does not store food for the winter or form winter clusters, and it does not stop reproducing for practically the entire year. It is viewed as a representative model of the tropical African bees in general [11].
The phylogenetic analyses of A. m. lamarckii and other subspecies demonstrated a close relationship between A. m. lamarckii and A. m. syriaca (Syrian honeybee) [12]. A. m. lamarckii has various distinctive characteristics, including a higher quality of reared queens [10], A. m. lamarckii exerts high levels of defensive behavior [13]. The Egyptian honeybee exhibits a more combative defensive response when compared to European bees, and the A. m. lamarckii larva develops more quickly; hence, they tolerate Varroa destructor mites, the serious and dangerous pest to Apis mellifera species [9]. Additionally, the biochemical and molecular characterization for three subspecies of honey bee workers explained the high genetic gap of 0.25 separating the Egyptian A. m. lamarckii subspecies from the other two subspecies, A. m. ligustica (Italian), and A. m. carnica (Carniolan) [14]. Here, we aimed to shed the light on the history of beekeeping in Egypt and the Egyptian honeybee subspecies A. m. lamarckii, reviewing their morphology, genetic analysis, distinctive characters, and defensive behaviors as part of our efforts to study honeybee and its bee products [15,16,17,18,19,20,21,22,23,24].

2. The History of Beekeeping in Egypt and Its Current Situation

Honey is a natural product produced by bees and used in Egypt not only as a sweetener but also associated with medical practices, and was deemed a poison for ghosts, demons, evil spirits, and the dead, representing a symbol of resurrection [25]. The first crude examples of the honeybee hieroglyphs were carved by the Egyptians of the first dynasty, in approximately 3000 B.C.E [2,3,4,26]. In the Nile Valley region, the bees were used as a source of honey from the earliest years; thus, bees were highly appreciated insects by the ancient Egyptians. In the old kingdom, the earliest inscription exemplifying beekeeping came from the sun temple of pharaoh Newossere in the fifth dynasty and back to 2450 B.C.E. [27]. In the sun temple, a room adjacent to the central obelisk was discovered by Ludwig Borchardt in 1898 and called “The Chamber of the Seasons” as it contains reliefs of activities that happened at particular times of the year, and one of them was found to be the oldest evidence of beekeeping [1,27]. The bas-relief from left to right shows four scenes: (I) a beekeeper working with the beehives; (II) three men pouring honey into containers; (III) two men processing honey (this scene is mostly missing); (IV) a beekeeper sealing honey in a vessel for storage [1]. By the end of the old kingdom and during the sixth dynasty, honey production increased to the level of trading [26]. During the time of the new kingdom, there were many tombs with images illustrating the practices involved in the treatment using bees and their products [28]. In the tomb of the 18th Dynasty vizier Rekhmire, there were inscriptions demonstrating honeycombs gathering from large horizontal hives, as shown in Figure 1, pouring the honey into large vessels, the successive honey sealing in diamond-shaped containers, and comb pulverizing [1]. During the 26th dynasty, the tomb of Pabasa demonstrated one of the most famous beekeeping reliefs in Egypt, where a beekeeper is facing a group of honeybee and a series of horizontal hives with his hands held up in praise. These horizontal hives were similar to the carved hives of the old kingdom from Newossere Any’s sun temple, as shown in Figure 2. They also authenticated the continued value of the honey and the honeybee in the ancient Egyptian times and the progress of hives types throughout the time [1,29,30].
In the Ptolemaic Period (304–30 B.C.E.), the state taxed bee keeping and the bee derived products. In the Nile Valley, beekeeping processes and breeding programs were established, as honey was fundamental to the people’s food [25]. The Egyptian mud hives (traditional bee hives) were placed in piles that could reach hundreds and were combined by pouring mortar in-between [31,32]. In 1918, modern beekeeping started in Egypt using wooden Langstroth frames. In 1920, the first association of beekeepers was established to improve beekeeping process and develop its marketing. Since, then traditional beekeeping methods were used in parallel with modern ones.
The modern beekeeping represents 99% of the used practices in Egypt [9]. Figure 3 illustrates the difference between the Egyptian mud traditional hives (A1-3) and the modern wooden ones (B). According to the Food and Agriculture Organization (FAO), statistics on the number of beehives in Egypt between 1961–2020 have been fluctuating, as represented in Figure 4. The number of beehives demonstrated noticeable increases between 1964–1972, 1980–1990, and 1999–2001, reaching 937,000, 1,651,000, and 1,485,000 hives, respectively, at the end of each period. In contrast, they demonstrated noticeable decreases in 1980, 1994, and 2017, reaching 858,000, 1,225,000, and 820,516 hives, respectively [9].
Honey bees are given special attention in Egypt because of their importance in pollination and their impact on the economy [33]. The pollination is mainly conducted using the Egyptian clover blooming during June, cotton flowering during August–September, and a minor contribution of citrus in April [31,32]. In the future, thermal stress on the Egyptian honey bee colonies will be a significant problem for beekeepers, especially during summer [24,34].

3. Apis mellifera lamarckii Morphology

The Egyptian A. m. lamarckii is considered an offshoot of adansonii. [7]. Some morphometric characteristics of Egyptian A. m. lamarckii, African Apis mellifera scutellata, and Apis mellifera jemenitica were reported where these subspecies were very close to A. m. lamarckii, as mentioned in Table 1, using different techniques such as an electron microscope [7,11,35,36,37,38,39]. Otherwise, the average length of the honeybee forewing in difference races was reported. The highest average was 10.700 mm in A. m. florea, while the lowest average was 8.275 mm in A. m. lamarckii. The average head length on different races in adult gave the highest average of 5.575 mm in A. m. lamarckii, while the lowest average was 3.750 mm in A. mellifera ligustica [38]. The mean body mass of the European (Apis mellifera Carnica) bee amounted to 120 mg, while the Egyptian bee to 78 mg. This shows that the Egyptian bee is much smaller than the European one, with only 65% of its mass. Similar results related to the thorax masses of both subspecies differ significantly (33 mg vs. 24 mg) for the European and Egyptian bee, respectively. The Egyptian bee is characterized with shorter wing size (45 mm) compared to the European bee (55 mm). The Egyptian honeybee A. m. lamarckii is significantly smaller, slimmer, and has shorter wings and legs. Moreover, the wing load was 17 and 21 Nm−2 for the Egyptian and European bee, respectively [11].
The Egyptian honeybee A. m. lamarckii neither forms winter clusters nor stores food for overwintering and breed nearly throughout the year. A. m. lamarckii is forced to form winter clusters and to store food for unfavorable periods [11].

4. Distinctive Characters of Apis mellifera lamarckii

The Egyptian A. m. lamarckii is known for its excessive large number of swarm cells, continuous breeding during throughout the whole year, low productivity using very little propolis, and proclivity to migrate, tending to migrate readily [7,11]. Its colonies include fewer bees (8000–10,000) compared to the European subspecies, which have more than 40,000 bees. A. m. lamarckii was found to exhibit a higher mass specific metabolism than the European A. m. carnica, and A. m. lamarckii, being more aggressive, active, and well adapted to its environment [11,47]. Another characteristic of A. m. lamarckii is the presence of half-queens, which are intermediate in morphology between queens and workers. They have a number of ovarioles that range between workers and queens, are possibly egg-laying workers, and help the queen’s colony by contributing to egg laying. A. m. lamarckii flagella of workers were longer than those of queens and half-queens; however, they did not differ in the length of flagellum. [38,48]. A study has been conducted to evaluate the quality of reared queens produced from A. m. carnica (Carniolian honey bee), A. m. ligustica (Italian honey bee), and A. m. lamarckii colonies. The highest accepted percentage of A. m. lamarckii-grafted larvae was significantly higher than A. m. ligustica, where the acceptance % was (93.75, 87.2, and 62.5) in A. m. carnica, A. m. lamarckii and A. m. ligustica, respectively. The Egyptian and the Carniolian colonies have a higher quality of reared queens represented in the long queen cell size, heaviest virgin queen, large number of ovarioles, and large volume of spermatheca of the produced queens than that of the Italian honey bees [10]. On the other hand, A. m. lamarckii was more resistance to chalkbrood diseases, with an infestation average of 0.218 % after the three inoculations. In contrast, the Carniolan race (A. m. carnica) demonstrated a lower tolerance, with an infestation average of 0.844% [49].

5. Genetic Analysis of Apis mellifera lamarckii

Using various analytical tools and different approaches, A. m. lamarckii mtDNA sequences were analyzed for a better understanding of its phylogenetic relationships with other different subspecies as well as to detect the genetic characteristics of these bees. The phylogenetic analyses of A. m. lamarckii and other different subspecies demonstrated a close relationship between A. m. lamarckii and A. m. capensis, A. m. intermissa, A. m. ligustica, and A. m. scutellata. The highest identity percentage (95.78%) was between A. m. lamarckii and A. m. syriaca, whereas A. m. lamarckii were far from A. florea, A. koschevnikovi, A. cerana japonica, A. laboriosa, A. nuluensis, and A. m. sahariensis [12]. Another study confirmed the close phylogenetic relationship between A. m. lamarckii and A. m. syriaca using the complete mtDNA sequences [50]. The honeybee in the dry regions of Sudan (desert, semi desert, and dry savannah) were genetically similar to A. m. lamarckii and A. m. syriaca, as both of them possess the O-lineage [51]. Abou-Shaara et. al. [52] confirmed a close genetic relationship between A. m. lamarckii, A. m. jemenitica (Arabian or Nubian honeybee), and A. m. syriaca. A. m. lamarckii was distinguished by the restriction of the Hinf-I enzyme from other honeybee subspecies using a PCR assay [53]. CO I/Hinf I was used not only to discriminate the mitochondrial “O” lineage but also as a diagnostic site for A. m. lamarckii [54]. The whole mitochondrial genome of the Egyptian A. m. lamarckii was examined and a 16,589 bp mitochondrial genome of A. m. lamarckii including 37 classical eukaryotic mitochondrial genes and an A + T-rich region were revealed. The arrangements and directions of the genes were identical to those of other Apis mitogenomes. All genes terminated with TAA, seven genes started with ATT, four with ATG, and two with ATA. Nine genes were encoded on the light strand and four on the heavy strand. The whole 22 tRNA genes had a cloverleaf structure that ranged from 66 to 80 bp. A. m. lamarckii is clustered with other A. mellifera subspecies in the phylogenetic tree [55]. A study has been conducted on two Apis mellifera (A. m. lamarckii and A. m. carnica) races as well as the hybrid and demonstrated the presence of clear genetic variations between A. m. lamarckii and A. m. carnica; the hybrid was closely related to the Carniolan (A. m. carnica) rather than to the A. m. lamarckii race. The higher resemblance between the Carniolan race and the hybrid suggested that the hybrid originated from Egyptian drones and Carniolan queens [56]. The genetic relationships and identical genetic characteristics between different African bee subspecies were investigated and demonstrated that A. m. lamarckii has the least genetic relationships with all other studied African bee subspecies (A. m. scutellata, A. m. capensis, A. m. intermissa, and A. m. monticola). While those of north and east Africa, namely, A. m. intermissa and A. m. monticola, exhibited less genetic similarity, the African subspecies A. m. scutellata demonstrated considerable genetic similarity and a tight evolutionary link to A. m. capensis. There were very few similarities and no close links among the bees from North Africa, A. m. Intermissa, and A. m. Lamarckii [57].

6. Apis mellifera lamarckii Hygienic Behaviors

The hygienic behavior of different honeybee species plays a critical role in the colony’s health of diverse honeybee races [58,59]. The hygienic behavior represents a behavioral defensive response of honeybee workers to uncap the wax covering of the brood cells, detect diseased brood, get rid of infected larvae or pupae, and inhibit the spreading of infective diseases [60,61]. Hygienic behaviors enable bees to resist parasitic mites (Varroa destructor) [60,62], American foulbrood (Paenibacillus larvae), and chalkbrood (Ascosphaera apis) among other infestations [63,64]. Hygienic behavior helps maintain the health of densely populated insect societies by limiting the horizontal transmission of pathogens and population growth of parasites [65]. Hygienic behavior relies on a limited set of genes linked to different regulation patterns associated with an over-expression of cytochrome P450 genes [66].
Native honeybee races (for example, A. m. jemenitica and A. m. syriaca) exhibited a certain degree of hygienic behavior compared to the exotic one, owing to its different genetic structure as well as its compatibility with local environmental conditions [67,68]. The A. m. jemenitica native race was significantly higher than that of the exotic one, A. m. carnica. The deformed mites, as a result of the grooming behavior, were also significantly higher in the colonies of the native race than those of exotic one [68]. Allam and Zakaria reported two defensive behavior mechanisms against the Varroa mite, namely the hygienic and grooming behaviors to minimize the parasitic threat. Moreover, the hygienic behavior of the Egyptian hybrid honeybee represented in cutting up Varroa mite bodies was related to treating the diseased colonies with black cumin oil or an oils mixture [69,70]. A. m. lamarckii are characterized by their high levels of defensive behaviors [13]. A. m. lamarckii colonies were found to exhibit higher levels of hygienic behavior compared to the Egyptian A. m. carnica colonies, according to a study conducted by Kamel and other collaborators [13]. The study demonstrated that, after 24 h, the dead broods were totally removed from 42.9% of A. m. lamarckii colonies, while 0% of the Egyptian A. m. carnica colonies were free from the dead broods. After 48 h, 71.4% of A. m. lamarckii colonies were completely free from the killed broods, whereas 8.3% of the Carniolan hybrid A. m. carnica colonies cleaned all of the killed broods [13].
In a different study, the percentages of cleaned cells were determined at different times for the local A. m. lamarckii and the Carniolan hybrid colonies and demonstrated 32.2% and 15.5% after 6 h, 70.6% and 38.4% after 24 h, 83.8% and 46.7% after 30 h, and 93.4% and 64.4% after 48 h, for the local A. m. lamarckii and the Carniolan hybrid colonies, respectively [35]. Clearly, the results revealed that A. m. lamarckii has significantly higher levels of hygienic behaviors, which could be affecting the survival and efficiency of the whole honeybee colonies against the Varroa mite infestation [13,35,60,65].

7. Biological Properties of Bee Venom from A. m. lamarckii

The venom produced by the Egyptian honeybee has a biological activity and potential pharmacological effects owned to the peptides, enzymes, amino acids, and minerals contents. Bee venom possesses biological properties that are anticancer, anti-inflammatory, and antibacterial [71].
Global threats to human health and the environment are posed by methylmercury pollution. The etiology of Minamata sickness was determined to be caused by methylmercury, which is a particularly neurotoxic pollutant. The intake of seafood exposes people to methylmercury. Because methylmercury rapidly crosses the blood–brain barrier, it can have an impact on the neurological system [72]. A. m. lamarckii venom has an in vivo protective influence (apitherapy) against methyl mercury chloride-induced blood–brain barrier dysfunction and neurobehavioral toxicity [73].
As one of the most serious infectious illnesses affecting cattle, buffalo, swine, goats, and sheep, foot-and-mouth disease (FMD) is a major problem worldwide, as per its high transmissibility and related monetary and productive losses [74]. FMDV was treated with Egyptian bee venom. Bee venom injections administered daily for seven days to sick goats and guinea pigs resulted in a significant reduction in the viral load and a shorter treatment period [72].
The comparison between bee venom composition obtained from A. m. lamarckii, A. m. carnica, and the hybrid has been established, and demonstrated that the hybrid venom was more similar to A. m. lamarckii than A. m. carnica, reflecting the domination of lamarkii subspecies’ genetic characters over those of carnica [75].
Hyaluronidase, the main allergen in bee venom, contains four different N-linked carbohydrate sites, and consists of 373 amino acid residues. The enzyme acts as an anti-inflammatory by causing hyaluronic acid break down in various tissues, allowing it to enter the tissue. Treatment with hyaluronidase was reported to prevent tumor cells from reaching lymph nodes in T cell lymphoma, and it may have important anticancer effects to stifle tumor growth [76,77]. Recently, Abdel-Monsef and colleagues purified and characterized hyaluronidase enzyme for the first time from Egyptian bee venom homogeneously using DEAE-cellulose and Sephacryl S-300 columns [78,79].
Phospholipase A2 (PLA2), the second-largest component of bee venom after mellitin, is one of the most significant bee venom enzymes and might be regarded as one of its primary constituents. It is a lipolytic enzyme that hydrolyzes phospholipids at the sn-2-acyl linkage to release free fatty acids and lysophospholipids. PLA2 has a wide range of pharmacological properties, such as the ability to inhibit the growth of cancer cells and to have anti-inflammatory, hepatotoxic, and neuroprotective effects [80,81,82]. PLA2 enzyme was purified from A. m. lamarckii venom and displayed anti-coagulant and anti-platelet aggregation activities, making it a promising agent against clot formation [83].
Additionally, the bee venom of A. m. lamarckii can treat respiratory illnesses by improving the haematological and respiration parameters in the animal model [84].

8. Conclusions and Future Perspective

A. m. lamarckii honeybee subspecies is thought to be the same subspecies as the one that could be found during the Pharaohs’ time, and it is still managed in mud-tube hives beside modern hives. The Egyptian A. m. lamarckii spreads in the Egyptian desert, delta region, Nile valley, and Sudan and resembles the lighter yellow-banded varieties with very dark drones. A. m. lamarckii is known for its excessive number of swarm cells, continuous breeding during the whole year, and low productivity, using very little propolis, and tends to migrate readily. A. m. lamarckii is characterized by higher mass-specific metabolism, presence of the half-queens, and high levels of defensive behaviors. The indigenous A. m. lamarckii subspecies have been hybridized with other introduced varieties, especially A. m. carnica; hence, pure subspecies have become very rare.
Due to the limited location and quantity of colonies in the small districts of Upper Egypt (Assiut), where it is kept in modern and mud tube hives, the populations of A. m. lamarckii have unfortunately suffered a significant decline. The owners of these Egyptian hives consider them a family heritage and refuse to accept governmental calls to rescue and enlarge them.
In order to maintain their colony stocks, beekeepers were compelled to purchase colonies of different subspecies, such as Italian and Carniolan honeybee. To date, the current status and the geographic variation of the A. m. amarckii populations in Egypt have not been studied in-depth and thus the data available is limited.
Futureward, efforts are highly recommended by the government, public, and researchers to preserve A. m. lamarckii, requiring more knowledge on the harmful effects threatening this bee subspecies as well as its conservation strategies, such as phylogenetic studies as well as the genetic network analysis. Moreover, beekeeping developmental projects can contribute to the conservation of honeybee and their environment. Qualitative and quantitative comparative studies could be conducted on A. m. lamarckii and the other Egyptian bee subspecies regarding their different products and how to be improved. One possibility that could be applied to improve the genetic conservation of local breeds in Egypt is the creation of isolated mating sites for the reproduction of A. m. lamarckii in the future breeding program. Although the Wadi Al-Assiut Protectorate uses the preserve for a range of flora and animals, including the native honeybees subspecies A. m. lamarckii, the protectorate should continue to focus on increasing bee populations with the help of the governmental scientific and financial support.
Further studies should focus on studying the A. m. lamarckii behavior that could positively affect the survival, efficiency, and decrease the infestation.

Author Contributions

Conceptualization, H.R.E.-S. and S.A.M.K.; Writing of the original draft, H.R.E.-S., A.A.A.E.-W., H.H.R.E.-S. and S.A.M.K.; Revision and editing of the final version, C.Z., A.S., X.Z., Z.G., A.G.H., A.A.S., A.F.A., Y.A.N., N.F.A., M.E.R., M.F.A.R. and K.W.; Supervision, H.R.E.-S. and K.W. All authors have read and agreed to the published version of the manuscript.

Funding

El-Seedi, H.R thanks Jiangsu University for the Adjunct Professor fellowship. Al Naggar, Y. is grateful to Alexander von Humboldt (AvH) foundation for a return fellowship (Ref 3.4-1196574-EGY-GF-P).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Dedicated with great pleasure and honor to Rob Verpoorte (Leiden University, the Netherlands) and Lars Bohlin (Uppsala University, Sweden) on the occasion of their 75th birthday.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kritsky, G. The quest for the perfect hive: Ancient Mediterranean origins. In Beekeeping in the Mediterranean from Antiquity to the Resent; Agricultural Organization “Demeter” Athens: Athens, Greece, 2017; pp. 50–56. [Google Scholar]
  2. Kuropatnicki, A.K.; Kłósek, M.; Kucharzewski, M. Honey as medicine: Historical perspectives. J. Apic. Res. 2018, 57, 113–118. [Google Scholar] [CrossRef]
  3. Sheppard, W.S.; Shoukry, A.K.S. The Nile honey bee—The bee of ancient Egypt in modern times. Am. Bee J. 2001, 14, 260–263. [Google Scholar]
  4. Abushady, A.Z. Races of bees. In The Hive and the Honey Bee; Dadant & Sons: Hamilton, NY, USA, 1949; pp. 11–20. [Google Scholar]
  5. Abdullah, I.; Gary, S.R.; Marla, S. Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie 2007, 38, 67–76. [Google Scholar] [CrossRef]
  6. Fasasi, K.A.; Malaka, S.L.O.; Amund, O.O. Studies on the life cycle and morphometrics of honeybees, Apis mellifera adansonii (Hymenoptera: Apidae) in a Mangrove area of Lagos, Nigeria. Ife J. Sci. 2011, 13, 103–109. [Google Scholar]
  7. Smith, F.G. The races of honeybees in Africa. Bee World 1961, 42, 255–260. [Google Scholar] [CrossRef]
  8. Simonthomas, R.T.; Simonthomas, A.M.J. Philanthus triangulum and its recent eruption as a predator of honeybees in an Egyptian oasis. Bee World 1980, 61, 97–107. [Google Scholar] [CrossRef]
  9. Al Naggar, Y.; Codling, G.; Giesy, J.P.; Safer, A. Beekeeping and the need for pollination from an agricultural perspective in Egypt. Bee World 2018, 95, 107–112. [Google Scholar] [CrossRef] [Green Version]
  10. Masry, S.H.D.; Ebadah, I.M.A.; Abd El-Wahab, T.E. Impact of honey bee colonies of different races on rearing Apis mellifera lamarckii queen larvae. Egypt. J. plant Prot. 2013, 8, 28–35. [Google Scholar]
  11. Schmolz, E.; Dewitz, R.; Schricker, B.; Lamprecht, I. Energy metabolism of European (Apis mellifera Carnica) and Egyptian (A. m. lamarckii) honeybees. J. Therm. Anal. Calorim. 2001, 65, 131–140. [Google Scholar] [CrossRef]
  12. Abou-Shaara, H.F.; Eid, K.S.A.; Bayoumi, S.R. Insights into the mtDNA of the Egyptian honey bees, Apis mellifera lamarckii using different analytical tools. J. Entomol. Res. 2020, 44, 575–580. [Google Scholar] [CrossRef]
  13. Kamel, S.M.; Strange, J.P.; Sheppard, W.S. A scientific note on hygienic behavior in Apis mellifera lamarckii and A. m. carnica in Egypt. Apidologie 2003, 34, 189–190. [Google Scholar] [CrossRef] [Green Version]
  14. El-Bermawy, S.M.; Ahmed, K.S.; Al-Gohary, H.Z.; Bayomy, A.M. Biochemical and molecular characterization for three subspecies of honey bee worker, Apis mellifera L. (Hymenoptera: Apidae) in Egypt. Egypt. Acad. J. Biol. Sci. A Entomol. 2012, 5, 103–115. [Google Scholar] [CrossRef]
  15. El-Seedi, H.R.; Eid, N.; El-Wahed, A.A.A.; Rateb, M.E. Honey bee products: Preclinical and clinical studies of their anti-inflammatory and immunomodulatory properties. Front. Nutr. 2022, 8, 761267–761285. [Google Scholar] [CrossRef] [PubMed]
  16. Yosri, N.; El-Wahed, A.A.A.; Ghonaim, R.; Khattab, O.M.; Sabry, A.; Ibrahim, M.A.A.; Moustafa, M.F.; Guo, Z.; Zou, X.; Algethami, A.F.M.; et al. Anti-viral and immunomodulatory properties of propolis: Chemical diversity, pharmacological properties, preclinical and clinical applications, and in silico potential against SARS-CoV-2. Foods 2021, 10, 1776. [Google Scholar] [CrossRef] [PubMed]
  17. El-Wahed, A.A.A.; Farag, M.A.; Eraqi, W.A.; Mersal, G.A.M.; Zhao, C.; Khalifa, S.A.M.; El-Seedi, H.R. Unravelling the beehive air volatiles profile as analysed via solid-phase microextraction (SPME) and chemometrics. J. King Saud Univ. Sci. 2021, 33, 101449–101456. [Google Scholar] [CrossRef]
  18. Khalifa, S.A.M.; Elashal, M.H.; Yosri, N.; Du, M.; Musharraf, S.G.; Nahar, L.; Sarker, S.D.; Guo, Z.; Cao, W.; Zou, X.; et al. Bee pollen: Current status and therapeutic potential. Nutrients 2021, 13, 1876. [Google Scholar] [CrossRef] [PubMed]
  19. El-Wahed, A.A.A.; Khalifa, S.A.M.; Elashal, M.H.; Musharraf, S.G.; Saeed, A.; Khatib, A.; Tahir, H.E.; Zou, X.; Naggar, Y.A.; Mehmood, A.; et al. Cosmetic applications of bee venom. Toxins 2021, 13, 810. [Google Scholar] [CrossRef] [PubMed]
  20. El-Seedi, H.R.; Khalifa, S.A.M.; El-Wahed, A.A.; Gao, R.; Guo, Z.; Tahir, H.E.; Zhao, C.; Du, M.; Farag, M.A.; Musharraf, S.G.; et al. Honeybee products: An updated review of neurological actions. Trends Food Sci. Technol. 2020, 101, 17–27. [Google Scholar] [CrossRef]
  21. Aufschnaiter, A.; Kohler, V.; Khalifa, S.; El-Wahed, A.; Du, M.; El-Seedi, H.; Büttner, S. Apitoxin and its components against cancer, neurodegeneration and rheumatoid arthritis: Limitations and possibilities. Toxins 2020, 12, 66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Khalifa, S.A.M.; Elashal, M.; Kieliszek, M.; Ghazala, N.E.; Farag, M.A.; Saeed, A.; Xiao, J.; Zou, X.; Khatib, A.; Göransson, U.; et al. Recent insights into chemical and pharmacological studies of bee bread. Trends Food Sci. Technol. 2020, 97, 300–316. [Google Scholar] [CrossRef]
  23. El-Seedi, H.R.; Ahmed, H.R.; El-Wahed, A.A.A.; Saeed, A.; Algethami, A.F.; Attia, N.F.; Guo, Z.; Musharraf, S.G.; Khatib, A. Bee stressors from an immunological perspective and strategies to improve bee health. Vet. Sci. 2022, 9, 199. [Google Scholar] [CrossRef] [PubMed]
  24. Khalifa, S.A.M.; Elshafiey, E.H.; Shetaia, A.A.; El-Wahed, A.A.A.; Algethami, A.F.; Musharraf, S.G.; Alajmi, M.F.; Zhao, C.; Masry, S.H.D.; Abdel-Daim, M.M.; et al. Overview of bee pollination and its economic value for crop production. Insects 2021, 12, 688. [Google Scholar] [CrossRef] [PubMed]
  25. Bunson, M. Encyclopedia of Ancient Egypt; Infobase Publishing: New York, NY, USA, 2014; ISBN 1438109970. [Google Scholar]
  26. Kritsky, G. The Tears of Re: Beekeeping in Ancient Egypt; Oxford University Press: Oxford, UK, 2015; ISBN 0199361398. [Google Scholar]
  27. Kritsky, G. Beekeeping from antiquity through the middle ages. Annu. Rev. Entomol. 2017, 62, 249–264. [Google Scholar] [CrossRef] [PubMed]
  28. Allon, N. The Tears of Re: Beekeeping in Ancient Egypt. J. Am. Orient. Soc. 2019, 139, 775–777. [Google Scholar]
  29. Hammad, M. Bees and beekeeping in ancient Egypt (a historical study) ancient Egyptian bee and its nature. J. Assoc. Arab Univ. Tour. Hosp. 2018, 15, 1–16. [Google Scholar] [CrossRef]
  30. Leek, F.F. Some evidence of bees and honey in ancient Egypt. Bee World 1975, 56, 141–163. [Google Scholar] [CrossRef]
  31. Gupta, R.K.; Khan, M.S.; Srivastava, R.M.; Goswami, V. History of beekeeping in developing world. In Beekeeping for Poverty Alleviation and Livelihood Security; Springer: Dordrecht, The Netherlands, 2014; pp. 3–62. [Google Scholar]
  32. Hussein, M.H. A review of beekeeping in Arab countries. Bee World 2000, 81, 56–71. [Google Scholar] [CrossRef]
  33. Amro, A.M. Pollinators and pollination effects on three canola (Brassica napus L.) cultivars: A case study in Upper Egypt. J. King Saud Univ. Sci. 2021, 33, 101240. [Google Scholar] [CrossRef]
  34. Abou-Shaara, H.F. Expectations about the potential impacts of climate change on honey bee colonies in Egypt. J. Apic. 2016, 31, 157–164. [Google Scholar] [CrossRef]
  35. Abou-Shaara, H.F.I. Morphometrical, Biological and Behavioral Studies on Some Honey Bee Races at El-Beheira Governorate. Doctoral Dissertation, Alexandria University, Alexandria, Egypt, 2009. [Google Scholar]
  36. Shaibi, T.; Fuchs, S.; Moritz, R.F.A. Morphological study of honeybees (Apis mellifera) from Libya. Apidologie 2009, 40, 97–105. [Google Scholar] [CrossRef] [Green Version]
  37. Rukhosh, J.R. The morphometrical study of some honeybee (Apis mellifera L.)(Hymenoptera: Apidae) races in Sulaimani-Iraqi Kurdistan Region. Euphrates J. Agric. Sci. 2021, 13, 23–41. [Google Scholar]
  38. Zeid, A.S.A.; Schricker, B. Antennal sensilla of the queen, half-queen and worker of the Egyptian honey bee, Apis mellifera lamarckii. J. Apic. Res. 2001, 40, 53–58. [Google Scholar] [CrossRef]
  39. Ahmed, K.-A.; El-Bermawy, S.; El-Gohary, H.; Bayomy, A. Electron microscope study on workers antennae and sting lancets of three subspecies of honey bee Apis mellifera L. (Hymenoptera: Apidae) and its bearing on their phylogeny. Egypt. Acad. J. Biol. Sci. A Entomol. 2015, 8, 105–124. [Google Scholar] [CrossRef]
  40. Al-Kahtani, S.N.; Taha, E.K.A. Morphometric study of Yemeni (Apis mellifera jemenitica) and Carniolan (A. m. carnica) honeybee workers in Saudi Arabia. PLoS ONE 2021, 16, e0247262. [Google Scholar] [CrossRef]
  41. Meixner, M.D.; Leta, M.A.; Koeniger, N.; Fuchs, S. The honey bees of Ethiopia represent a new subspecies of Apis melliferaApis mellifera simensis n. ssp. Apidologie 2011, 42, 425–437. [Google Scholar] [CrossRef]
  42. Buco, S.M.; Collins, A.M.; Rinderer, T.E.; Lancaster, V.A.; Sylvester, H.A.; Crewe, R.M.; Davis, G.L. Morphometric differences between south American Africanized and South African Scutellata ) honey bees. Apidologie 1987, 18, 217–222. [Google Scholar] [CrossRef] [Green Version]
  43. Alabdali, E.A.; Ghramh, H.A.; Ibrahim, E.H.; Ahmad, Z.; Asiri, A.N. Characterization of the native honey bee (Apis mellifera jemenitica) in the south western region of Saudi Arabia using morphometric and genetic (mtDNA COI) characteristics. Saudi J. Biol. Sci. 2021, 28, 2278–2284. [Google Scholar] [CrossRef]
  44. Alqarni, A.S.; Hannan, M.A.; Owayss, A.A.; Engel, M.S. The indigenous honey bees of Saudi Arabia (Hymenoptera, Apidae, Apis mellifera jemenitica Ruttner): Their natural history and role in beekeeping. Zookeys 2011, 134, 83–98. [Google Scholar]
  45. Elfeel, M.A.M. Studies on the Egyptian Honeybee Race Apis mellifera lamarckii Cockerel in Siwa Oasis as a New Isolated Region; Cairo University: Cairo, Egypt, 2008. [Google Scholar]
  46. Alburaki, A. Morphometrical study on Syrian honeybee (Apis mellifera syriaca) introduction important social insects known in the honeybee evolutionary lineages (Ruttner, 1978). Biometrical studies were also done on other honeybee species Abd. Emir. J. Food Agric. 2008, 20, 89–93. [Google Scholar] [CrossRef] [Green Version]
  47. Abdelkader, F. Situation of beekeeping in North Africa. J. Apitherapy Nat. 2020, 3, 1–9. [Google Scholar] [CrossRef]
  48. Zeid, A.S.A. Comparison of eggs produced by queens, halfqueens and worker bees and weight of emerging workers in Apis mellifera lamarckii. J. Apic. Res. 2020, 59, 685–690. [Google Scholar] [CrossRef]
  49. Abdel-Rahman, M.F. Chalkbrood tolerance in Apis mellifera lamarckii and A. m. carnica in Egypt. J. Agric. Sci. Assiut Univ. 2009, 40, 125–132. [Google Scholar]
  50. Abou-Shaara, H.F.; Abbas, A.S.; Al-Kahtani, S.N.; Taha, E.-K.A.; Khan, K.A.; Jamal, Z.A.; Alotaibi, M.A.; Ahmad, B.; Khan, N.A.; Qamer, S. Exploring the non-coding regions in the mtDNA of some honey bee species and subspecies. Saudi J. Biol. Sci. 2021, 28, 204–209. [Google Scholar] [CrossRef]
  51. El-Niweiri, M.A.A.; Moritz, R.F.A. Mitochondrial discrimination of honeybees (Apis mellifera) of Sudan. Apidologie 2008, 39, 566–573. [Google Scholar] [CrossRef] [Green Version]
  52. Abou-Shaara, H.F.; Al-Ghamdi, A.A.; Khan, K.A.; Al-Kahtani, S.N. Genetic network analysis between Apis mellifera subspecies based on mtDNA argues the purity of specimens from North Africa, the Levant and Saudi Arabia. Saudi J. Biol. Sci. 2021, 28, 2718–2725. [Google Scholar] [CrossRef]
  53. Nielsen, D.I.; Ebert, P.R.; Page, R.E.; Hunt, G.J.; Guzmán-Novoa, E. Improved polymerase chain reaction-based mitochondrial genotype assay for identification of the Africanized honey bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 2000, 93, 1–6. [Google Scholar] [CrossRef]
  54. Kandemir, I.; Pinto, M.A.; Meixner, M.D.; Sheppard, W.S. Hinf-I digestion of cytochrome oxidase I region is not a diagnostic test for A. m. lamarckii. Genet. Mol. Biol. 2006, 749, 747–749. [Google Scholar] [CrossRef]
  55. Eimanifar, A.; Kimball, R.T.; Braun, E.L.; Moustafa, D.M.; Haddad, N.; Fuchs, S.; Grünewald, B.; Ellis, J.D. The complete mitochondrial genome of the Egyptian honey bee, Apis mellifera lamarckii (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part B 2017, 2, 270–272. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. El-Barbary, N.S.; Youssef, M.K. Biochemical genetic studies in honeybees Apis mellifera L. J. Plant Prot. Pathol. 2006, 31, 1107–1121. [Google Scholar] [CrossRef]
  57. Abou-shaara, H.F. Utilizing bioinformatics to detect genetic similarities between African honey bee subspecies. J. Genet. 2019, 98, 96–102. [Google Scholar] [CrossRef]
  58. Pernal, S.F.; Sewalem, A.; Melathopoulos, A.P. Breeding for hygienic behaviour in honeybees (Apis mellifera) using free-mated nucleus colonies. Apidologie 2012, 43, 403–416. [Google Scholar] [CrossRef] [Green Version]
  59. Alacioa, M.A.P.; Iginib, E.E.F.; Uffinengoa, S.R.R.; Odriguezb, E.M.R.; Oyob, M.L.D.E.L.H.; Edascarrasbureb, E.L.B. Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie 2000, 31, 471–478. [Google Scholar]
  60. Khan, K.A.; Ghramh, H.A. An investigation of the efficacy of hygienic behavior of various honey bee (Apis mellifera) races toward Varroa destructor (Acari: Varroidae) mite infestation. J. King Saud Univ. Sci. 2021, 33, 101393. [Google Scholar] [CrossRef]
  61. Boecking, O.; Spivak, M. Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 1999, 30, 141–158. [Google Scholar] [CrossRef] [Green Version]
  62. Parker, R.; Guarna, M.M.; Melathopoulos, A.P.; Moon, K.-M.; White, R.; Huxter, E.; Pernal, S.F.; Foster, L.J. Correlation of proteome-wide changes with social immunity behaviors provides insight into resistance to the parasitic mite, Varroa destructor, in the honey bee (Apis mellifera). Genome Biol. 2012, 13, R81. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Spivak, M.; Gilliam, M. Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa: Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World 1998, 79, 169–186. [Google Scholar] [CrossRef]
  64. Pivak, M.S.; Euter, G.S.R. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apiacta 2001, 32, 555–565. [Google Scholar]
  65. Spivak, M.; Danka, R.G. Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie 2021, 52, 1–16. [Google Scholar] [CrossRef]
  66. Hamiduzzaman, M.; Emsen, B.; Hunt, G.J.; Subramanyam, S.; Williams, C.E.; Tsuruda, J.M.; Novoa, E.G. Differential gene expression associated with honey bee grooming behavior in response to Varroa mites. Behav. Genet. 2017, 47, 335–344. [Google Scholar] [CrossRef] [PubMed]
  67. Zaitoun, S.T.; Al-Ghzawi, A.M.; Shannag, H.K. Grooming behaviour of Apis mellifera syriaca towards Varroa jacobsoni in Jordan. J. Appl. Entomol. 2001, 125, 85–87. [Google Scholar] [CrossRef]
  68. Balhareth, H.M.; Alqarni, A.S.; Owayss, A.A. Comparison of hygienic and grooming behaviors of indigenous and exotic honeybee (Apis mellifera) races in central Saudi Arabia. Int. J. Agric. Biol. 2012, 14, 1005–1008. [Google Scholar]
  69. Russo, R.M.; Liendo, M.C.; Landi, L.; Pietronave, H.; Merke, J.; Fain, H.; Muntaabski, I.; Palacio, M.A.; Rodríguez, G.A.; Lanzavecchia, S.B.; et al. Grooming behavior in naturally varroa-resistant Apis mellifera colonies from North-central Argentina. Front. Ecol. Evol. 2020, 8, 590281–590293. [Google Scholar] [CrossRef]
  70. Allam, S.; Zakaria, M. Stimulation effects of the essential oils on the sensory and defensive behaviors of Egyptian honey bees towards Varroa invasion. Acarines J. Egypt. Soc. Acarol. 2009, 3, 29–36. [Google Scholar] [CrossRef] [Green Version]
  71. Wehbe, R.; Frangieh, J.; Rima, M.; El Obeid, D.; Sabatier, J.M.; Fajloun, Z. Bee venom: Overview of main compounds and bioactivities for therapeutic interests. Molecules 2019, 24, 2997. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. M Mansour, A.; Elfiky, A.A.; Fahmy, A.; Diab, A.A. Therapeutic effect of bee venom formulation in the treatment of FMD viral infection: Preclinical and clinical evaluation. Int. J. Sci. Res. Publ. 2016, 6, 711–728. [Google Scholar]
  73. Abu-Zeid, E.H.; Khalifa, B.A.; Elewa, Y.H.A.; Arisha, A.H.; Ismail, T.A.; Hendam, B.M.; El Abdel-Hamid, S. Bee venom Apis mellifera lamarckii rescues blood brain barrier damage and neurobehavioral changes induced by methyl mercury via regulating tight junction proteins expression in rat cerebellum. Food Chem. Toxicol. 2021, 154, 112309. [Google Scholar] [CrossRef] [PubMed]
  74. Singh, R.K.; Sharma, G.K.; Mahajan, S.; Dhama, K.; Basagoudanavar, S.H.; Hosamani, M.; Sreenivasa, B.P.; Chaicumpa, W.; Gupta, V.K.; Sanyal, A. Foot-and-mouth disease virus: Immunobiology advances in vaccines and vaccination strategies addressing vaccine failures—An Indian perspective. Vaccines 2019, 7, 90. [Google Scholar] [CrossRef] [Green Version]
  75. Zalat, S.; Abouzeid, A.; Ibrahim, A.; Abd El-Aal, A. Protein pattern of the honeybee venoms of Egypt. Egypt. J. Biol. 2002, 4, 42–46. [Google Scholar]
  76. El-Wahed, A.A.A.; Khalifa, S.A.; Sheikh, B.Y.; Farag, M.A.; Saeed, A.; Larik, F.A.; Koca-Caliskan, U.; AlAjmi, M.F.; Hassan, M.; Wahabi, H.A.; et al. Bee venom composition: From chemistry to biological activity. In Studies in Natural Products Chemistry; Elsevier: Amsterdam, The Netherlands, 2018; Volume 60, pp. 459–484. ISBN 9780444641816. [Google Scholar]
  77. García, M.L.G.; Plischuk, S.; Bravi, C.M.; Reynaldi, F.J. An overview on honeybee colony losses in Buenos Aires province, Argentina. Sociobiology 2019, 66, 75–80. [Google Scholar] [CrossRef] [Green Version]
  78. Kim, Y.-W.; Chaturvedi, P.; Chun, S.; Lee, Y.; Ahn, W. Honeybee venom possesses anticancer and antiviral effects by differential inhibition of HPV E6 and E7 expression on cervical cancer cell line. Oncol. Rep. 2015, 33, 1675–1682. [Google Scholar] [CrossRef] [Green Version]
  79. Abdel-Monsef, M.M.; Zidan, H.A.; Darwish, D.A.; Masoud, H.M.; Helmy, M.S.; Ibrahim, M.A. Biochemical isolation and characterization of hyaluronidase enzyme from venom of egyptian honey bee Apis mellifera lamarcki. J. Apic. Sci. 2020, 64, 153–164. [Google Scholar] [CrossRef]
  80. Putz, T.; Ramoner, R.; Gander, H.; Rahm, A.; Bartsch, G.; Bernardo, K.; Ramsay, S.; Thurnher, M. Bee venom secretory phospholipase A2 and phosphatidylinositol-homologues cooperatively disrupt membrane integrity, abrogate signal transduction and inhibit proliferation of renal cancer cells. Cancer Immunol. Immunother. 2007, 56, 627–640. [Google Scholar] [CrossRef] [PubMed]
  81. Kang, G.H.; Lee, S.; Choi, D.B.; Shin, D.; Kim, J.; Yang, H.; Bae, H. Bee venom phospholipase A2 ameliorates atherosclerosis by modulating regulatory T cells. Toxins 2020, 12, 609. [Google Scholar] [CrossRef] [PubMed]
  82. Kim, H.; Keum, D.J.; Kwak, J.W.; Chung, H.S.; Bae, H. Bee venom phospholipase A2 protects against acetaminophen-induced acute liver injury by modulating regulatory T cells and IL-10 in mice. PLoS ONE 2014, 9, e114726. [Google Scholar] [CrossRef] [PubMed]
  83. Darwish, D.A.; Masoud, H.M.M.; Abdel-Monsef, M.M.; Helmy, M.S.; Zidan, H.A.; Ibrahim, M.A. Phospholipase A2 enzyme from the venom of Egyptian honey bee Apis mellifera lamarckii with anti-platelet aggregation and anti-coagulation activities. J. Genet. Eng. Biotechnol. 2021, 19, 10. [Google Scholar] [CrossRef] [PubMed]
  84. Patel, A. Effect of honeybee venom (Apis mellifera) on respiratory functions of hypercholesterolemic male albino rats. Assiut Vet. Med. J. 2019, 67, 9–25. [Google Scholar]
Figure 1. Honey combs gathering from large horizontal hives in Rekhmira tomb.
Figure 1. Honey combs gathering from large horizontal hives in Rekhmira tomb.
Animals 12 02749 g001
Figure 2. Beekeeping reliefs from the tomb of Pabasa and Karnak Temple (Photography by Aida Abd El-Wahed).
Figure 2. Beekeeping reliefs from the tomb of Pabasa and Karnak Temple (Photography by Aida Abd El-Wahed).
Animals 12 02749 g002
Figure 3. The Egyptian mud traditional hives (A1A3) and modern ones (B). (Photo A1A3: Dahy M. Mostafa and used with permission).
Figure 3. The Egyptian mud traditional hives (A1A3) and modern ones (B). (Photo A1A3: Dahy M. Mostafa and used with permission).
Animals 12 02749 g003
Figure 4. Beehives stocks in Egypt within the period (1961–2020) according to FAO (Data source: www.fao.org/faostat/en/#data/QCL, accessed on 29 July 2022).
Figure 4. Beehives stocks in Egypt within the period (1961–2020) according to FAO (Data source: www.fao.org/faostat/en/#data/QCL, accessed on 29 July 2022).
Animals 12 02749 g004
Table 1. Morphological characters of Apis mellifera lamarckii compared to African Apis mellifera scutellata and Apis mellifera jemenitica.
Table 1. Morphological characters of Apis mellifera lamarckii compared to African Apis mellifera scutellata and Apis mellifera jemenitica.
Morphology Characteristics Apis mellifera lamarckiiAfrican Apis mellifera scutellataApis mellifera jemeniticaReference
ColorLighter yellow-banded varieties with very dark drones--[7]
Width of worker cells4.8 mm--[7]
Average head width4.550 mm--[37]
Bodyweight 78 mg-87.65 mg[11,40]
Body size56.82 mm55.04 mm54.07 mm[41]
Thorax mass24 mg--[11]
Wing load17 Nm−2--[11]
Wing size45 mm2--[11]
Average length of forewing5.575 mm--[37]
Forewing width2.78–2.96 mm2.71–3.03 mm2.44, 3.20–3.03 and 2.77–3.23 mm[35,36,42,43,44]
Leg size7.39 mm--[36]
Forewing length8.23 and 8.74 mm8.48–9.01 mm7.94, 7.53–9.01, 7.94, and 7.55–9.39 mm[35,36,40,42,43,44,45,46]
Tongue length5.75 mm--[35]
Hindwing length6.11 mm4.02–4.24 mm5.85 mm[35,40,41,42,45]
Hindwing width1.76 mm1.52–168 mm1.67 mm[35,42]
Femur length2.24 mm2.44–1.63 mm2.44, 2.39–1.63 mm[35,42,43]
Tibia length2.82 mm3.05–3.23 mm2.55, 2.69–3.23 mm[35,40,42,43]
Tibia width--1.12 mm[40]
Basitarsus length2.13 mm1.81–2.02 mm-[35,42]
Basitarsus width1.10 mm1.05–1.15 mm-[35,42]
Cubital index2.33 and 2.94 mm1.77–2.86 & 2.33 mm2.10–2.86 and 2.36 mm[35,41,42,43,46]
Number of hooks20.34--[35]
Lengths of the workers flagella2.60–2.80 mm-2.29–2.80 mm[38,43]
Lengths of the queens flagella2.60 mm--[38]
Lengths of the half-queen flagella2.48–2.60 mm--[38]
Length waxmirror 1.11 mm1.16–1.32 mm-[36,42]
Waxmirror index0.55 mm--[36]
Hair length21.49 mm20.88 mm22.55 mm[41]
Length of hind leg738.09 mm741.10 mm717.71 mm [41,43]
Wing angle J1698.42--[41]
Proboscis length5.65–570 mm-5.28, 5.30 and 4.84–5.74 mm[40,43,45]
Metatarsus length1.88–1.91 mm-2.03, 2.22 and 1.94–2.26 mm[40,43,45]
Metatarsus width1.05–1.08 mm-1.10, 1.01 and 0,97–1.16 mm[40,43,45]
Wax mirror width--2.00 mm[43]
Total length of antenna3.92 mm-3.64 mm[40,45]
(-): No reported.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

El-Seedi, H.R.; El-Wahed, A.A.A.; Zhao, C.; Saeed, A.; Zou, X.; Guo, Z.; Hegazi, A.G.; Shehata, A.A.; El-Seedi, H.H.R.; Algethami, A.F.; et al. A Spotlight on the Egyptian Honeybee (Apis mellifera lamarckii). Animals 2022, 12, 2749. https://doi.org/10.3390/ani12202749

AMA Style

El-Seedi HR, El-Wahed AAA, Zhao C, Saeed A, Zou X, Guo Z, Hegazi AG, Shehata AA, El-Seedi HHR, Algethami AF, et al. A Spotlight on the Egyptian Honeybee (Apis mellifera lamarckii). Animals. 2022; 12(20):2749. https://doi.org/10.3390/ani12202749

Chicago/Turabian Style

El-Seedi, Hesham R., Aida A. Abd El-Wahed, Chao Zhao, Aamer Saeed, Xiaobo Zou, Zhiming Guo, Ahmed G. Hegazi, Awad A. Shehata, Haged H. R. El-Seedi, Ahmed F. Algethami, and et al. 2022. "A Spotlight on the Egyptian Honeybee (Apis mellifera lamarckii)" Animals 12, no. 20: 2749. https://doi.org/10.3390/ani12202749

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop