Table of Contents
BENTHAM SCIENCE PUBLISHERS LTD.
End User License Agreement (for non-institutional, personal use)
Usage Rules:
Disclaimer:
Limitation of Liability:
General:
PREFACE
CONSENT FOR PUBLICATION
CONFLICT OF INTEREST
ACKNOWLEDGEMENTS
The Queen Honey Bee: Introduction, Development, Pheromones, Mating, and Role in the Colony
Abstract
1.1. INTRODUCTION
1.1.1. General Information about Colonial Organizations
1.1.2. Different Castes and Respective Duties
1.1.3. General Differences in the Three Castes
1.1.4. Ovarian State of Active Queen and Sterile Workers
1.1.5. Queen Quality Influencing Factors
1.1.6. Queen Failure
1.2. DEVELOPMENT OF QUEEN
1.2.1. Queen Development: General Information
1.2.2. Development Post-Queen Egg Hatching
1.2.3. Queen Larval Development
1.2.4. Role of Royal Jelly
1.2.5. Plasticity of the Queen Development Phase
1.3. QUEEN PHEROMONES
1.3.1: Queen Pheromones Composition
1.3.2. Queen Mating Status Correlation with QMPs
1.3.3. Functions of Pheromones
1.4. MATING
1.4.1. Nuptial Flight
1.4.2. DCA
1.4.3. Process of Mating and Post Mating
1.5. Role of Queen honey Bee
REFERENCES
The Queen Honey Bee Duties in the Composite Colonies
Abstract
2.1. REPRODUCIBILITY OF QUEEN HONEY BEE
2.1.1. General Information on Queen Reproduction
2.1.2. Factors Influencing Queen Reproductive Characteristics
2.1.3. Queen Making Decision in the Colony
2.1.4. The Queen Elimination Procedure
2.2. QUEEN PHEROMONES
2.2.1. General Information about Queen Pheromones
2.2.2. Queen Mandibular Gland Pheromones
2.2.3. Dufour’s Gland
2.3. Conclusion
REFERENCES
The Queen Honey Bee Morphology, Development, and Reproductive System
Abstract
3.1. INTRODUCTION
3.2. MORPHOLOGY OF THE QUEEN
3.3. DEVELOPMENT OF THE QUEEN HONEY BEE
3.4. OVARIAN STRUCTURAL INTEGRITY (3a-b)
REFERENCES
Royal Jelly as Larval Food for Honey Bees
Abstract
4.1. INTRODUCTION
4.1.1. Information That Is General Regarding Royal Jelly
4.2. COMPOSITION
4.2.1. Sugar
4.2.2. Lipid
4.2.3. Protein
4.2.4. Phenols, Flavonoids And Free Amino Acids
4.2.5. Vitamins, Minerals And Other Bioactive Sustances
4.2.6. The Importance of Royal Jelly to the Developmental Process
4.3. SECRETION OF ROYAL JELLY
4.4. DIET OF OTHER CASTES
Conclusion
REFERENCES
Quality Influencing Factors and Disease Resistance in Queen of Apis mellifera (Hymenoptera: Apidae)
Abstract
5.1. INTRODUCTION
5.2. STRONG QUEEN AND COLONY
5.3. QUEEN QUALITY AND ASSOCIATED FACTORS
5.3.1. Larval Selection Influence
5.3.2. Other Factors
5.4. OVARIAN WEIGHT AND FUNCTIONALITY AS QUEEN QUALITY INDEXES
5.5. QUALITY OF QUEEN ON THE BASICS OF SPERMATHECAE
5.6. DISEASES AND REPRODUCTIVITY OF QUEEN HONEY BEE
Conclusion
REFERENCES
Differential Pheromone Secretion By Female Castes In Apis mellifera (Hymenoptera: Apidae)
Abstract
6.1. INTRODUCTION
6.2. QUEEN PHEROMONES
6.2.1. Queen Mandibular Gland
6.2.1.1. Composition of QMPs and Variation in Accordance of Mating Status
6.2.1.2. Secretion of QMP
6.2.1.3. Colonial Regulation Imposed by QMP
6.2.1.4. On Retinue
6.2.1.5. On Wax Secretion
6.2.1.6. On Ovarian Development
6.2.2. Dufour's Gland
6.2.3. Koschevnikov Gland
6.2.4. Tarsal Gland
6.3. WORKERS' PHEROMONES
Alarm pheromone
6.3.1. Koschevnikov Gland
6.3.2. Mandibular Gland
6.3.3. Brood Recognition Pheromones
6.3.4. Nasonov Gland
6.3.5. Dufour's Gland Pheromone
6.3.6. Footprint Pheromones
6.3.7. Forager Pheromone
6.3.8. Other Pheromones
Conclusion
REFERENCES
Mandibular Pheromone Types, Functions, Synthesis, And Associated Genetic Elements In The Queen Honey Bee, Apis mellifera
Abstract
7.1. INTRODUCTION
7.2. COMPOSITION OF QMP
7.3. DIFFERENTIAL MANDIBULAR PHEROMONAL COMPOSITION IN QUEEN AND WORKER HONEY BEE
7.4. SYNTHESIS OF QMPs
7.5. EFFECT OF QMP
7.5.1. On Mating and Swarm
7.5.2. On Retinue
7.6. Workers' Mandibular Gland Pheromones
7.7. Gene Associated with Mandibular Gland
Conclusion
REFERENCES
Retinue Behaviour of Worker Honey Bees
Abstract
8.1. INTRODUCTION
8.2. PHEROMONES FOR ATTRACTION OF NEST MATES
8.2.1. Factors For Inducing Variation in Retinue Behaviour
8.2.2. Various Components of QMP and Retinue in Workers
8.2.3. QMP Influence on Drone and Swarming
8.2.4. Colonial Transfer of Queen Pheromones
Conclusion
REFERENCES
Influence of Queen Pheromones on Worker Ovarian PCD in Apis mellifera (Hymenoptera: Apidae)
Abstract
9.1. INTRODUCTION
9.2. QUEEN PHEROMONES RELATED TO PCD IN WORKERS' OVARIES
9.2.1. General Information
9.2.1.1. General Ovarian Structure
9.2.1.2. Larval Gonadial Development
9.2.2. Main Pheromones Which Influence PCD
9.2.3. Differential Pheromonal Synthesis in Queen and Workers
9.3. Queen's Influence on Programmed Cell Death
9.3.1. General Information
9.3.2. Mechanism of PCD
9.3.3. Detection of PCD in Workers' Ovaries
Conclusion
REFERENCES
Genetic Influence on Ovarian Development Plasticity In Apis mellifera (Hymenoptera: Apidae)
Abstract
10.1. INTRODUCTION
10.2. Differential Gene Expression in Queen and Workers
10.3. Brief Description of Various Genetic Regulators of PCD
10.3.1. Anarchy Gene
10.3.2. Ark Gene
10.3.3. Miscellaneous Description of Various Genes Involved in Development
10.3.4. Hormonal Effect on Gene Expression
Conclusion
REFERENCES
Drone Development, Biology, and And Interaction With The Queen in Apis mellifera
Abstract
11.1. INTRODUCTION
11.2. GENERAL DEVELOPMENT
11.3. DIPLOID DRONES
11.4. LIFE SPAN
11.5. DRONE NUMBER
11.6. FLIGHT ACTIVITY
11.7. DRIFT AND ORIENTATION OF DRONES' FLIGHT TO THE HIVE
11.8. ATTRACTION OF DRONES TO VIRGIN QUEEN
11.9. DRONE DEVELOPMENT
11.10. REPRODUCTIVE SYSTEM OF DRONES
11.11:MATING
11.12. INFLUENTIAL FACTORS FOR DRONE QUALITY
11.13. DRONE AGING
Conclusion
REFERENCES
Mating and Reproduction in Queen Honey Bee
Abstract
12.1. INTRODUCTION
12.2. MATING AND FREQUENCY OF OCCURRENCE
12.3. FACTORS AFFECTING MATING
12.4. Pheromones
12.5. DRONES CONGREGATION AREAS
12.6. DRONE ATTRACTION
Conclusion
REFERENCES
Swarming and Queen Honey Bee
Abstract
13.1. INTRODUCTION
13.2. FACTORS AFFECTING SWARMING
13.2.1. Queen Age As Promoting Factor for Swarming
13.2.2. Reduced Queen Pheromones
13.2.3. Infection as Cause of Swarming
13.3. ROLE OF QUEEN MANDIBULAR PHEROMONES IN SWARMING
13.4. OTHER QUEEN GLANDS PHEROMONES IN SWARMING
13.5. MAJOR EVENTS IN SWARMING
13.5.1. Pre-Swarming Phase
13.5.2. Exodus of Swarm
13.5.3.Swarming
13.5.4. Migration During Swarming
13.6.TYPES OF SWARMING WORKERS
13.7.AGE AND PHYSIOLOGY OF SWARMING WORKERS
13.8. NATAL COLONY AFTER SWARMING
Conclusion
REFERENCES
Requeen Process and Importance
Abstract
14.1. INTRODUCTION
14.2. QUEEN'S ROLE AND GENERAL DEVELOPMENT
14.3. METHOD OF QUEEN PRODUCTION
Conclusion
The Polyandrous Queen Honey Bee: Biology and Apiculture
Authored by
Lovleen Marwaha
Department of Zoology, School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India
BENTHAM SCIENCE PUBLISHERS LTD.
End User License Agreement (for non-institutional, personal use)
This is an agreement between you and Bentham Science Publishers Ltd. Please read this License Agreement carefully before using the ebook/echapter/ejournal (“Work”). Your use of the Work constitutes your agreement to the terms and conditions set forth in this License Agreement. If you do not agree to these terms and conditions then you should not use the Work.
Bentham Science Publishers agrees to grant you a non-exclusive, non-transferable limited license to use the Work subject to and in accordance with the following terms and conditions. This License Agreement is for non-library, personal use only. For a library / institutional / multi user license in respect of the Work, please contact: [email protected].
Usage Rules:
All rights reserved: The Work is the subject of copyright and Bentham Science Publishers either owns the Work (and the copyright in it) or is licensed to distribute the Work. You shall not copy, reproduce, modify, remove, delete, augment, add to, publish, transmit, sell, resell, create derivative works from, or in any way exploit the Work or make the Work available for others to do any of the same, in any form or by any means, in whole or in part, in each case without the prior written permission of Bentham Science Publishers, unless stated otherwise in this License Agreement.You may download a copy of the Work on one occasion to one personal computer (including tablet, laptop, desktop, or other such devices). You may make one back-up copy of the Work to avoid losing it.The unauthorised use or distribution of copyrighted or other proprietary content is illegal and could subject you to liability for substantial money damages. You will be liable for any damage resulting from your misuse of the Work or any violation of this License Agreement, including any infringement by you of copyrights or proprietary rights.
Disclaimer:
Bentham Science Publishers does not guarantee that the information in the Work is error-free, or warrant that it will meet your requirements or that access to the Work will be uninterrupted or error-free. The Work is provided "as is" without warranty of any kind, either express or implied or statutory, including, without limitation, implied warranties of merchantability and fitness for a particular purpose. The entire risk as to the results and performance of the Work is assumed by you. No responsibility is assumed by Bentham Science Publishers, its staff, editors and/or authors for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products instruction, advertisements or ideas contained in the Work.
Limitation of Liability:
In no event will Bentham Science Publishers, its staff, editors and/or authors, be liable for any damages, including, without limitation, special, incidental and/or consequential damages and/or damages for lost data and/or profits arising out of (whether directly or indirectly) the use or inability to use the Work. The entire liability of Bentham Science Publishers shall be limited to the amount actually paid by you for the Work.
General:
Any dispute or claim arising out of or in connection with this License Agreement or the Work (including non-contractual disputes or claims) will be governed by and construed in accordance with the laws of Singapore. Each party agrees that the courts of the state of Singapore shall have exclusive jurisdiction to settle any dispute or claim arising out of or in connection with this License Agreement or the Work (including non-contractual disputes or claims).Your rights under this License Agreement will automatically terminate without notice and without the need for a court order if at any point you breach any terms of this License Agreement. In no event will any delay or failure by Bentham Science Publishers in enforcing your compliance with this License Agreement constitute a waiver of any of its rights.You acknowledge that you have read this License Agreement, and agree to be bound by its terms and conditions. To the extent that any other terms and conditions presented on any website of Bentham Science Publishers conflict with, or are inconsistent with, the terms and conditions set out in this License Agreement, you acknowledge that the terms and conditions set out in this License Agreement shall prevail.
Bentham Science Publishers Pte. Ltd.
80 Robinson Road #02-00
Singapore 068898
Singapore
Email: [email protected]
PREFACE
Dear Readers,
The book Polyandrous Queen Honey Bee is attributed to the predominant caste of honey bee colony. This specific book provides information about the development of a queen honey bee, associated genetic elements, her pheromone profile, life span, immunity, mating, reproduction, artificial method of bee rearing, swarming and the role of a queen in the colony.
While working on apiculture, I was encouraged to share my experience and observations on bee farming. Further, the desire to compile the scattered information on a specific topic furthered the book writing process. Additionally, while visiting various apiaries and observing honey bee cultural practices including traditional and scientific practices, both served as great factors for compiling information in the form of a book. I am further planning to publish two more books dedicated to worker honey bees and drones.
I would like to thank my parents, sister, friends, and my students, who have shown the required support and encouragement for the completion of this work. I personally thank the management of Lovely Professional University, Punjab, India for providing the required facilities for Apiculture.
Regards,
CONSENT FOR PUBLICATION
Not applicable.
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or otherwise.
ACKNOWLEDGEMENTS
Declared none.
Lovleen Marwaha
Associate Professor
Department of Zoology
School of Bioengineering and Biosciences
Lovely Professional University
Punjab, India
The Queen Honey Bee: Introduction, Development, Pheromones, Mating, and Role in the Colony
Lovleen Marwaha
1 Lovely Professional University , Punjab, India Department of Zoology India
Abstract
Apis mellifera (2n=32), commonly known as the European honey bee or the Western honey bee, is a eusocial insect. Each honey bee colony is a composite unit of thousands of bees, with three different castes: a polyandrous reproductively active queen; thousands of workers; and a few hundred drones. The queen and the workers represent the female caste that develops from fertilized eggs, whereas the drones are male bees formed from unfertilized or fertilized eggs. In the case of the female honey bees, the phenomenon of polyphenism can be easily highlighted, which is the developmental plasticity of the same genomic contents to express differently as per environmental cues. During the queen larval developmental phase, the exclusive diet is royal jelly, which induces hyper-secretion of juvenile and ecdysone hormones that ultimately cause sequential activation of certain genetic elements, specifically after 3rd instar onward. For the worker honey bee larvae, initially, the diet includes royal jelly exclusively, followed by honey, pollen grains, and worker jelly, which collectively direct development toward the worker caste. Furthermore, for harmonious social interaction, the queen secretes certain volatile chemical bouquets including 9-ODA(2E)-9-oxodecenoic acid), 9-HDA (9-hydroxy-(E)-2-decenoic acid), 10-HDA (10-hrdroxy-2-decenoic acid), HVA (4-hydroxy-3-methoxyphenylethanol), HOB (Methyl-p-hydroxybenzoate), 10-HDAA (10-hydroxydecanoic acid), OLA (oligolactide), methyl oleate, decyl decanoate, linolenic acid, coniferyl alcohol, cetyl alcohol, etc. The concerned pheromones facilitate the regulation of workers' behavior; workers' ovarian suppression; retinue control; overall worker’s development modulation; colonial product production; swarming tendency; pseudo-queen formation suppression; mating, etc. The queen honey bee is polyandrous, as she mates with many drones during the nuptial flight in 'Drone Congregation Areas (DCA)’, within about 2 weeks of her post-emergence. This chapter provides a comprehensive review of the polyandrous queen honey bee; her synchronous developmental phases; her pheromone dominance; her regulation and coordination of colonies; her mating preference and habits; and her role in a composite hive. Subsequent chapters provide an elaborative view of different aspects of the queen honey bees' life cycle.
Keywords: Developmental Plasticity, Polyphenism and DCA, Queen Honey Bee.
REFERENCES
Akyol E., Yeninar H., Kaftanoglu O.. Live weight of queen honey bees (Apis mellifera L.) predicts reproductive characteristics., J. Kans. Entomol. Soc..2008; 81(2): 92-100.
[CrossRef]Alber M.. Von der paarung der honigbiene., Z Bienenforsch.1955; 3: 1-28.Al-Lawati H., Kamp G., Bienefeld K.. Characteristics of the spermathecal contents of old and young honeybee queens., J. Insect Physiol..2009; 55(2): 117-122.
[CrossRef] [PubMed]Alaux C., Dantec C., Parrinello H., Le Conte Y.. Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and varroa-parasitized bees., BMC Genomics.2011; 12(1): 496.
[CrossRef] [PubMed]Amiri E., Strand M., Rueppell O., Tarpy D.. Queen quality and the impact of honey bee diseases on queen health: potential for interactions between two major threats to colony health., Insects.2017; 8(2): 48.
[CrossRef] [PubMed]Apðegaitë V., Skirkevièius A.. Quantitative and qualitative composition of extracts from virgin and mated honeybee queens (Apis mellifera L.)., Pheromones.1995; 5(1-2): 23-36.Asencot M., Lensky Y.. The effect of sugars and Juvenile Hormone on the differentiation of the female honeybee larvae ( L.) to queens., Life Sci..1976; 18(7): 693-699.
[CrossRef] [PubMed]Baer B., Collins J., Maalaps K., Boer S.P.A.. Sperm use economy of honeybee ( Apis mellifera ) queens., Ecol. Evol..2016; 6(9): 2877-2885.
[CrossRef] [PubMed]Barchuk A.R., Cristino A.S., Kucharski R., Costa L.F., Simões Z.L.P., Maleszka R.. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera., BMC Dev. Biol..2007; 7(1): 70.
[CrossRef] [PubMed]Beetsma J.. The process of queen-worker differentiation in the honeybee., Bee World.1979; 60(1): 24-39.
[CrossRef]Beggs K.T., Glendining K.A., Marechal N.M., Vergoz V., Nakamura I., Slessor K.N., Mercer A.R.. Queen pheromone modulates brain dopamine function in worker honey bees., Proc. Natl. Acad. Sci. USA.2007; 104(7): 2460-2464.
[CrossRef] [PubMed]Blum M.S.. Honey bee pheromones in the hive and the honey bee.. Dadant and Sons; 1992: 385-389.Böttcher F.K.. Beiträge zur Kenntnis des Paarungsfluges der Honigbiene., Apidologie (Celle).1975; 6(3): 233-281.
[CrossRef]Brodschneider R., Crailsheim K.. Nutrition and health in honey bees., Apidologie (Celle).2010; 41(3): 278-294.
[CrossRef]Burley L.M., Fell R.D., Saacke R.G.. Survival of honey bee (Hymenoptera: Apidae) spermatozoa incubated at room temperature from drones exposed to miticides., J. Econ. Entomol..2008; 101(4): 1081-1087.
[CrossRef] [PubMed]Butler C.G., Fairey E.M.. The role of the queen in preventing oogenesis in worker honeybees., J. Apic. Res..1963; 2(1): 14-18.
[CrossRef]Butler C.G., Simpson J.. Pheromones of the queen honeybee (Apis mellifera L.) which enable her workers to follow her when swarming., Proc. R. Entomol. Soc. Lond., Ser. A Gen. Entomol..1967; 42(10-12): 149-154.
[CrossRef] [). Oxford, UK: Blackwell Publishing Ltd.].Carreck N.L., Andree M., Brent C.S., Cox-Foster D., Dade H.A., Ellis J.D., Hatjina F., van Englesdorp D.. Standard methods for Apis mellifera anatomy and dissection., J. Apic. Res..2013; 52(4): 1-40.
[CrossRef]Chaimanee V., Evans J.D., Chen Y., Jackson C., Pettis J.S.. Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos., J. Insect Physiol..2016; 89: 1-8.
[CrossRef] [PubMed]Collins A.M.. Relationship between semen quality and performance of instrumentally inseminated honey bee queens., Apidologie (Celle).2000; 31(3): 421-429.
[CrossRef]Collins A.M.. Variation in time of egg hatch by the honey bee, Apis mellifera (Hymenoptera: Apidae)., Ann. Entomol. Soc. Am..2004; 97(1): 140-146.
[CrossRef]Collins A.M., Williams V., Evans J.D.. Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera., Insect Mol. Biol..2004; 13(2): 141-146.
[CrossRef] [PubMed]Crewe R.M.. Compositional variability: the key to the social signals produced by honeybee mandibular glands., The biology of social insects.. Breed M.D., Mitchener E.D., Evans H.E.Boulder: Westview; 1982: 318-322.Crewe R.M., Velthuis H.H.W.. False queens: A consequence of mandibular gland signals in worker honeybees., Naturwissenschaften.1980; 67(9): 467-469.
[CrossRef]Cruz-Landim C.. Aparelho reprodutor feminino e ovogênese. Abelhas: Morfologia e função de sistemas.. São Paulo: Editora UNESP; 2009: 15-55.
[CrossRef]de Azevedo S.V., Hartfelder K.. The insulin signaling pathway in honey bee (Apis mellifera) caste development — differential expression of insulin-like peptides and insulin receptors in queen and worker larvae., J. Insect Physiol..2008; 54(6): 1064-1071.
[CrossRef] [PubMed]Dedej S., Hartfelder K., Aumeier P., Rosenkranz P., Engels W.. Caste determination is a sequential process: effect of larval age at grafting on ovariole number, hind leg size and cephalic volatiles in the honey bee ( Apis mellifera carnica )., J. Apic. Res..1998; 37(3): 183-190.
[CrossRef]Delaney D.A., Keller J.J., Caren J.R., Tarpy D.R.. The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera L.)., Apidologie (Celle).2011; 42(1): 1-13.
[CrossRef]Dombroski T.C.D., Simões Z.L.P., Bitondi M.M.G.. Dietary dopamine causes ovary activation in queenless Apis mellifera workers., Apidologie (Celle).2003; 34(3): 281-289.
[CrossRef]Eckert J.E.. Studies in the number of ovarioles in queen honeybees in relation to body size., J. Econ. Entomol..1934; 27(3): 629-635.
[CrossRef]Engels W., Rosenkranz P., Adler A., Taghizadeh T., Lübke G., Francke W.. Mandibular gland volatiles and their ontogenetic patterns in queen honey bees, Apis mellifera carnica., J. Insect Physiol..1997; 43(4): 307-313.
[CrossRef] [PubMed]Estoup A., Solignac M., Cornuet J.M.. Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies., Proc. Biol. Sci..1994; 258(1351): 1-7.
[CrossRef]Evans J.D., Wheeler D.E.. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera., Proc. Natl. Acad. Sci. USA.1999; 96(10): 5575-5580.
[CrossRef] [PubMed]Fletcher D.J.C., Tribe G.D.. 1977b.—Natural emergency queen rearing by the African bee Apis mellifera adansonii and its relevance for successful queen production by beekeepers, II., Proc. Apimondia Inter. Symp.. Pretoria, South Africa: 161-168.Fleig R.. Role of the follicle cells for yolk uptake in ovarian follicles of the honey bee Apis mellifera L. (Hymenoptera : Apidae)., Int. J. Insect Morphol. Embryol..1995; 24(4): 427-433.
[CrossRef]Frazier M., Mullin C., Frazier J., Ashcraft S.. What have pesticides got to do with it?, Am. Bee J..2008; 148(6): 521-524.Franck P., Solignac M., Vautrin D., Cornuet J.M., Koeniger G., Koeniger N.. Sperm competition and last-male precedence in the honeybee., Anim. Behav..2002; 64(3): 503-509.
[CrossRef]Gauthier L., Ravallec M., Tournaire M., Cousserans F., Bergoin M., Dainat B., de Miranda J.R.. Viruses associated with ovarian degeneration in Apis mellifera L. queens., PLoS One.2011; 6(1)e16217[CrossRef] [PubMed]Gary N.E.. Chemical mating attractants in the queen honey bee., Science.1962; 136(3518): 773-774.
[CrossRef] [PubMed]Gilley D.C., Tarpy D.R., Land B.B.. Effect of queen quality on interactions between workers and dueling queens in honeybee ( Apis mellifera L.) colonies., Behav. Ecol. Sociobiol..2003; 55(2): 190-196.
[CrossRef]Gutzeit H.O., Zissler D., Fleig R.. Oogenesis in the honeybee Apis mellifera: cytological observations on the formation and differentiation of previtellogenic ovarian follicles., Rouxs Arch. Dev. Biol..1993; 202(3): 181-191.
[CrossRef] [PubMed]Haarmann T., Spivak M., Weaver D., Weaver B., Glenn T.. Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations., J. Econ. Entomol..2002; 95(1): 28-35.
[CrossRef] [PubMed]DeGrandi-Hoffman G., Chambers M., Hooper J.E., Schneider S.S.. Description of an intermorph between a worker and queen in African honey bees Apis mellifera scutellata (Hymenoptera: Apidae)., Ann. Entomol. Soc. Am..2004; 97(6): 1299-1305.
[CrossRef]Harbo J.R., Harris J.W.. Responses to Varroa by honey bees with different levels of Varroa Sensitive Hygiene., J. Apic. Res..2009; 48(3): 156-161.
[