IN VITRO SPERMATOLOGICAL PARAMETERS IN DRONES

Year 2023, , 268 - 279, 19.11.2023

Abdulkadir Kaya , Ongun Uysal

https://doi.org/10.31467/uluaricilik.1279779

Abstract

Honey bees are an indispensable element of the ecosystem, as they provide an important part of plant pollination beyond food production. The queen bee, which forms the core of the bee colony, is at the center of bee production in the beekeeping sector. Undoubtedly, the production of high-quality queen bees primarily depends on suitable drones and therefore, quality sperm. In addition, artificial insemination of queen bees is a successful production method, as in other species, due to its superior characteristics compared to natural mating. In many apiaries and research centers, artificial insemination is used routinely for queen production. One of the advantages of this method is that the sperm can be preserved for the short or long term. In this respect, it is very effective in protecting genetic resources, preventing bee diseases and facilitating bee transportation. Today, spermatological studies and parameters used in drones are very few compared to other species. With the increasing importance given to the subject in recent years, many spermatological parameters have started to be used in honey bees. However, the morphological and physiological differences of drone semen require the development and standardization of these parameters with further studies. In this review, the spermatological parameters used in drone semen, together with the working principles and materials used, were examined in general terms and presented to the readers.

Keywords

Beekeeping, Artificial insemination, Drone, Honey bee, Sperm

Bal Arılarında İn Vitro Spermatolojik Parametreler

Abstract

Bal arıları, gıda üretiminin ötesinde bitki tozlaşmasının önemli bir bölümünü sağladıkları için ekosistemin vazgeçilmez bir unsurudur. Arı kolonisinin çekirdeğini oluşturan ana arı, arıcılık sektöründe arı üretiminin merkezinde yer almaktadır. Kuşkusuz kaliteli ana arı üretimi öncelikle uygun erkek arılara ve dolayısıyla kaliteli spermaya bağlıdır. Ayrıca suni tohumlama doğal çiftleşmeye göre üstün özellikleri nedeniyle diğer türlerde olduğu gibi başarılı bir üretim yöntemidir. Birçok arıcılık işletmesinde ve araştırma merkezinde ana arı üretimi için suni tohumlama rutin olarak kullanılmaktadır. Bu yöntemin avantajlarından biri de spermanın kısa ya da uzun süreli saklanabilmesidir. Bu yönüyle genetik kaynakların korunmasında, arı hastalıklarının önlenmesinde ve arı taşımacılığının kolaylaştırılmasında oldukça etkilidir. Günümüzde erkek arılarda kullanılan spermatolojik çalışmalar ve uygulanan parametreler diğer türlere göre çok azdır. Son yıllarda konuya verilen önemin artmasıyla bal arılarında birçok spermatolojik parametre kullanılmaya başlanmıştır. Ancak erkek arı spermasının morfolojik ve fizyolojik farklılıkları, bu parametrelerin ileri çalışmalarla geliştirilmesini ve standardize edilmesini gerektirmektedir. Bu derlemede erkek arı spermasında kullanılan spermatolojik parametreler, çalışma prensipleri ve kullanılan materyaller genel hatlarıyla incelenmiş ve okuyucuların beğenisine sunulmuştur.

Keywords

Arıcılık, Bal Arısı, Erkek Arı, Suni Tohumlama, Sperma

References

• Abdelkader F, Kairo G, Bonnet M, Barbouche N, Belzunces LP et al. Effects of Clothianidin on Antioxidant Enzyme Activities and Malondialdehyde Level in Honey Bee Drone Semen. J. Apic. Res. 2019;58 (5):740-745. http://dx.doi.org/10.1080/00218839.2019.1655182
• Abdelkader F, Kairo G, Tchamitchian S, Cousin M, Senechal J et al. Semen Quality of Honey Bee Drones Maintained from Emergence to Sexual Maturity Under Laboratory, Semi-Field and Field Conditions. Apidologie, 2014;45(2):215-223. http://dx.doi.org/10.1007/s13592-013-0240-7.
• Alcay S, Cakmak S, Cakmak I, Aktar A, Yilmaz M et al. L-Carnitine Supplemented Extenders Improve Post-Thawing Quality of Honey Bee Drone (Apis mellifera) Spermatozoa. Kafkas Univ. Vet. Fak. Derg. 2021;27(4):489-493. http://10.9775/kvfd.2021.25756
• Alçay S, Çakmak S, Cakmak I, Aktar A, Yılmaz M et al. Honey Bee Drone (Apis mellifera) Sperm Cryopreservation with Rainbow Trout Seminal Plasma Supplemented Extenders. J. Hell. Vet. Medical Soc. 2022;1(73):3745-3750. http://dx.doi.org/10.12681/jhvms.25651
• Alcay S, Cakmak S, Cakmak I, Mulkpinar E, Gokce E et al. Cryobiology Successful Cryopreservation of Honey Bee Drone Spermatozoa with Royal Jelly Supplemented Extenders. Cryobiology, 2019;87(October 2018):28-31. https://doi.org/10.1016/j.cryobiol.2019.03.005.
• Alçay S, Çakmak S, Çakmak İ, Mülkpinar E, Toker MB et al. Drone Semen Cryopreservation with Protein Supplemented TL-Hepes Based Extender. Kafkas Univ. Vet. Fak. Derg. 2019;25(4):553-557. htttp://10.9775/kvfd.2018.2131.
• Andere CI, Monteavaro C, Palacio MA, Catena M, Rodríguez EM et al. Apis mellifera Semen: Bacterial Contamination and Susceptibility to Antibiotics. Apidologie 2011;42(5):551-559. http://dx.doi.org/10.1007/s13592-011-0051-7
• Auth CA, Hopkins BK. Nitrogen Vapor Immersion : An Accessible Alternative for Honey Bee (Apis mellifera L .) Semen Cryopreservation. Cryobiology, 2021;100(April):12-18. https://doi.org/10.1016/j.cryobiol.2021.04.006
• Banaszewska D, Andraszek K. Identification of Honey Bee Sperm Structures Following The Use of Various Staining Techniques. J. Vet. Res. 2023. http://dx.doi.org/10.2478/jvetres-2023-0001
• Ben Abdelkader F, Çakmak İ, Çakmak SS, Nur Z, İncebıyık E et al. Toxicity Assessment of Chronic Exposure to Common Insecticides and Bee Medications on Colony Development and Drones Sperm Parameters. Ecotoxicology, 2021;30(5):806-817. http://dx.doi.org/10.1007/s10646-021-02416-3
• Berg S, Koeniger N. Larger Drones (Apis mellifera) Have More Offspring. Proc. German Zoological Society, 83rd Meeting, Frankfurt Am Main, Gustav Fischer Verlag, 1990;614
• Borsuk G, Kozłowska M, Anusiewicz M, Paleolog J. Nosema ceranae Changes Semen Characteristics and Damages Sperm DNA in Honeybee Drones. Invertebr. Surviv. J. 2018;15:197-202. https://doi.org/10.25431/1824-307X/isj.v15i1.197-202
• Bratu IC, Igna V, Simiz E, Dunea IB, Pătruică S. The Influence of Body Weight on Semen Parameters in Apis mellifera Drones. Insects 2022;13(12):1141. http://dx.doi.org/10.3390/insects13121141
• Ciereszko A, Wilde J, Dietrich GJ, Siuda M, Bąk B et al. Sperm Parameters of Honeybee Drones Exposed to Imidacloprid. Apidologie 2017;48 (2):211-222 http://dx.doi.org/10.1007/s13592-016-0466-2.
• Cobey SW, Tarpy DR, Woyke J. Standard Methods for Instrumental Insemination of Apis Mellifera Queens. J. Apic. Res., 2013;52(4):1-54. http://dx.doi.org/10.3896/IBRA.1.52.4.09
• Collins AM. Relationship Between Semen Quality and Performance of Instrumentally Inseminated Honey Bee Queens. Apidologie, 2000;31(3):421-429. http://dx.doi.org/10.1051/apido:2000132
• Collins AM. Sources of Variation in The Viability of Honey Bee, Apis mellifera L., Semen Collected for Artificial Insemination. Invertebr. Reprod. Dev. 2004;45(3):231-237. https://doi.org/10.1080/07924259.2004.9652594
• Collins AM, Donoghue AM. Viability Assessment of Honey Bee, Apis Mellifera, Sperm Using Dual Fluorescent Staining. Theriogenology 1999;51(8):1513-1523. http://dx.doi.org/10.1016/S0093-691X(99)00094-1
• Collins AM, Pettis JS. Effect of Varroa Infestation on Semen Quality. Am. Bee J. 2001;141(8): 590
• Czekońska K, Chuda-Mickiewicz B, Chorbiński P. The Effect of Brood Incubation Temperature on The Reproductive Value of Honey Bee (Apis Mellifera) Drones. J. Apic. Res, 2013a;52(2):96–105. http://dx.doi.org/10.3896/IBRA.1.52.2.19
• Czekońska K, Chuda-Mickiewicz B, Chorbiński P. The Influence of Honey Bee (Apis mellifera) Drone Age on Volume of Semen and Viability of Spermatozoa. J. Apic. Sci, 2013b;57:61–66. http://dx.doi.org/10.2478/jas-2013-0007
• Czekońska K, Chuda-Mickiewicz B, Samborski J. Quality of Honeybee Drones Reared in Colonies with Limited and Unlimited Access to Pollen. Apidologie, 2015;46(1):1-9. http://dx.doi.org/10.1007/s13592-014-0296-z
• Den Boer SPA, Baer B, Boomsma JJ. Seminal Fluid Mediates Ejaculate Competition in Social Insects. Science 2010;327(5972):1506-1509. https://doi.org/10.1126/science.1184709
• Duay P, De Jong D, Engels W. Decreased Flight Performance and Sperm Production in Drones of The Honey Bee (Apis mellifera) Slightly İnfested By Varroa Destructor Mites During Pupal Development. Genet. Mol. Res, 2002;1(3):227-232
• Falencka-Jabłońska M. Bees in The City. Studia Ecologiae et Bioethicae, 2022;20(3):25–31. http://dx.doi.org/10.21697/seb.2022.20
• Gençer HV, Kahya Y. Are sperm traits of drones (Apis mellifera L.) from laying worker colonies noteworthy? J. Apic. Sci, 2011;50(2):130-137. http://dx.doi.org/10.3896/IBRA.1.50.2.04
• Ghramh HA, Iqbal A, Rafique MK, Mahmood R, Ahmed AM et al. Instrumental Insemination: A Nontraditional Technique to Produce Superior Quality Honey Bee (Apis mellifera) Queens. J. King Saud Univ. Sci. 2022;34(5):102077. https://doi.org/10.1016/j.jksus.2022.102077
• Glander H-J, Schaller J. Binding of Annexin V to Plasma Membranes of Human Spermatozoa: A Rapid Assay for Detection of Membrane Changes After Cryostorage. MHR Basic Science of Reproductive Medicine 1999;5(2):109-115. http://dx.doi.org/10.1093/molehr/5.2.109
• Gulov AN, Bragina YE. Morphofunctional Changes in Frozen-Thawed Sperm of Apis mellifera Linnaeus Drones. Russ. Agric. Sci. 2022;48(6):512-520. http://dx.doi.org/10.3103/S1068367422060040
• Hayashi S, Satoh T. Sperm Maturation Process Occurs in The Seminal Vesicle Following Sperm Transition From Testis in Honey Bee Males. Apidologie, 2019;50(3):369-378. http://dx.doi.org/10.1007/s13592-019-00652-5
• Hopkins BK, Cobey SW, Herr C, Sheppard WS. Gel-Coated Tubes Extend Above-Freezing Storage of Honey Bee (Apis mellifera) Semen to 439 Days with Production of Fertilised Offspring. Reprod. Fertil. Dev. 2017;29(10):1944-1949. https://doi.org/10.1071/RD16087
• Johnson RM, Dahlgren L, Siegfried BD, Ellis MD. Effect of In-Hive Miticides on Drone Honey Bee Survival and Sperm Viability. J. Apic. Res. 2013;52(2):88-95. http://dx.doi.org/10.3896/IBRA.1.52.2.18
• Kaftanoglu O, Peng Y-S. Preservation of Honeybee Spermatozoa in Liquid Nitrogen. J. Apic. Res. 1984;23(3):157-163. http://dx.doi.org/10.1080/00218839.1984.11100625
• Kahya Y, Gençer HV. Reproductive Quality in Drones Bred From Caucasian (A. m. caucasica) and Italian (A. m. ligustica) Honey Bee Colonies. Apidologie, 2023;54(1):1. http://dx.doi.org/10.1007/s13592-022-00973-y
• Kairo G, Provost B, Tchamitchian S, Ben Abdelkader F, Bonnet M et al. Drone Exposure to The Systemic Insecticide Fipronil Indirectly Impairs Queen Reproductive Potential. Sci. Rep. 2016;6(1):1-12. http://dx.doi.org/10.1038/srep31904
• Kaya A, Akyol N. Comparative Analysis of Spermatological and Morphometric Parameters in Honey Bee Samples Collected From Some Beekeeping Located in Kırıkkale Region. MSc Thesis. Kırıkkale University, Institute of Health Science, 2021
• Lensky Y, Ben-David E, Schindler H. Ultrastructure of The Spermatozoon of The Mature Drone Honeybee. J. Apic. Res. 1979;18(4):264-271. http://dx.doi.org/10.1080/00218839.1979.11099981
• Lino-Neto J, Báo SN, Dolder H. Sperm Ultrastructure of The Honey Bee (Apis mellifera) (L)(Hymenoptera, Apidae) with Emphasis on The Nucleus-Flagellum Transition Region. Tissue Cell, 2000;32(4):322-327. http://dx.doi.org/10.1054/tice.2000.0119
• Locke SJ, Peng Y. The Effects of Drone Age, Semen Storage and Contamination on Semen Quality in The Honey Bee (Apis mellifera). Physiol. Entomol. 1993;18(2):144-148. http://dx.doi.org/10.1111/j.1365-3032.1993.tb00461.x
• Locke SJ, Peng Y, Cross NL. A Supravital Staining Technique for Honey Bee Spermatozoa. Physiol. Entomol. 1990;15(2):187-192. http://dx.doi.org/10.1111/j.1365-3032.1990.tb00506.x
• Lodesani M, Balduzzi D, Galli A. Functional Characterisation of Semen in Honeybee Queen (A m ligustica) Spermatheca and Efficiency of The Diluted Semen Technique in Instrumental Insemination. Ital. J. Anim. Sci. 2004;3(4):385-392. https://doi.org/10.4081/ijas.2004.385
• Mackensen O. Viability and Sex Determination in The Honey Bee (Apis mellifera L.). Genetics 1951;36(5):500. http://dx.doi.org/10.1093/genetics/36.5.500
• Morais LS, Araujo Neto ER, Silva AM, Marinho DEL, Bezerra LGP et al. Sperm Characteristics of Africanized Honey Bee (Apis mellifera L.) Drones During Dry and Wet Seasons in The Caatinga Biome. J. Apic. Res. 2022;1-8. http://dx.doi.org/10.1080/00218839.2022.2113328
• Moreira DR, de Souza THS, Galhardo D, Puentes SMD, Figueira CL et al. Imidacloprid Induces Histopathological Damage in The Midgut, Ovary, and Spermathecal Stored Spermatozoa of Queens After Chronic Colony Exposure. Environ. Toxicol. Chem. 2022;41 (7):1637-1648. http://dx.doi.org/10.1002/etc.5332
• Moritz RFA. Der Einfluss der Inzucht auf die Fitness der Drohnen von Apis mellifera carnica. Apidologie, 1981;12(1):41-55. http://dx.doi.org/10.1051/apido:19810104
• Moritz RFA. The Effect of Different Diluents on Insemination Success in The Honeybee Using Mixed Semen. J. Apic. Res. 1984;23(3):164-167. http://dx.doi.org/10.1080/00218839.1984.11100626
• Muller K, Pomorski T, Muller P, Herrmann A. Stability of Transbilayer Phospholipid Asymmetry in Viable Ram Sperm Cells After Cryotreatment. J. Cell. Sci.1999;112(1):11-20. http://dx.doi.org/10.1242/jcs.112.1.11
• Murray JF, van der Horst G, Allsopp M, Kotzé RCM. A New Fluorescent Method to Determine Honey Bee Sperm Motility Parameters with Computer-Aided Sperm Analysis. J. Apic. Res. 2022;62(4):944-952. http://dx.doi.org/10.1080/00218839.2022.2090729
• Papa G, Maier R, Durazzo A, Lucarini M, Karabagias IK et al. The Honey Bee Apis mellifera: An Insect at The Interface Between Human and Ecosystem Health. Biology (Basel), 2022;11 (2):233. http://dx.doi.org/10.3390/biology11020233
• Peña FJ, Johannisson A, Wallgren M, Rodrı́guez-Martı́nez H. Assessment of Fresh and Frozen–Thawed Boar Semen Using An Annexin-V Assay: A New Method of Evaluating Sperm Membrane Integrity. Theriogenology, 2003;60(4):677-689. https://doi.org/10.1016/S0093-691X(03)00081-5
• Peng Y, Locke SJ, Nasr ME, Liu TP, Montague MA. Differential Staining for Live and Dead Sperm of Honey Bees. Physiol. Entomol. 1990;15 (2):211-217. http://dx.doi.org/10.1111/j.1365-3032.1990.tb00509.x
• Power K, D’Anza E, Martano M, Albarella S, Ciotola F et al. Morphological and Morphometric Analysis of The Italian Honeybee (Apis mellifera ligustica) Spermatozoa: A Preliminary Study in Campania Region. Vet. Med. Sci. 2019;6(2):0-61. http://dx.doi.org/10.7243/2054-3425-6-2
• Rajamohan A, Danka RG, Hopkins BK, Rinehart JP. A Non-Activating Diluent to Prolong in Vitro Viability of Apis mellifera Spermatozoa: Effects on Cryopreservation and on Egg Fertilization. Cryobiology 2020;92(September 2019):124–129. http://dx.doi.org/10.1016/j.cryobiol.2019.11.045
• Rhodes JW, Harden S, Spooner-Hart R, Anderson DL, Wheen G. Effects of Age, Season and Genetics on Semen and Sperm Production in Apis mellifera Drones. Apidologie, 2011;42 (1):29-38. http://dx.doi.org/10.1051/apido/2010026
• Rinderer TE, Collins AM, Pesante D, Daniel R, Lancaster V et al. Comparison of Africanized and European Drones: Weights, Mucus Gland and Seminal Vesicle Weights, and Counts of Spermatozoa. Apidologie, 1985;16(4):407-412. http://dx.doi.org/10.1051/apido:19850405
• Rinderer TE, De Guzman LI, Lancaster VA, Delatte GT, Stelzer JA. Varroa in The Mating Yard: I. The Effects of Varroa Jacobsoni and Apistan on Drone Honey Bees. Am. Bee J. 1999;139:134-139. 134–139
• Rousseau A, Fournier V, Giovenazzo P. Apis mellifera (Hymenoptera: Apidae) Drone Sperm Quality in Relation to Age, Genetic Line, and Time of Breeding. Can. Entomol. 2015;147(6):702-711. http://dx.doi.org/10.4039/tce.2015.12
• Rousseau A, Giovenazzo P. Optimizing Drone Fertility with Spring Nutritional Supplements to Honey Bee (Hymenoptera: Apidae) Colonies. J. Econ. Entomol. 2016;109(3):1009-1014. http://dx.doi.org/10.1093/jee/tow056
• Rowland SC, Jacobson JD, Patton WC, King A, Chan PJ. Dual Fluorescence Analysis of DNA Apoptosis in Sperm. Am. J. Obstet. Gynecol. 2003;188(5):1156-1157. http://dx.doi.org/10.1067/mob.[phone]
• Schlüns H, Schlüns EA, Van Praagh J, Moritz RFA. Sperm Numbers in Drone Honeybees (Apis mellifera) Depend on Body Size. Apidologie, 2003;34(6):577-584. http://dx.doi.org/10.1051/apido:2003051
• Sharma GP, Gupta BL, Kumbkarni CG. Cytology of Spermatogenesis in The Honey Bee, Apis indica (F.). J. R. Microsc. Soc. 1961;79(4):337-351. http://dx.doi.org/10.1111/j.1365-2818.1961.tb05227.x
• Snodgrass RE. Anatomy of The Honey Bee. Cornell University Press. 1956, p.130-134
• Stürup M, Baer-Imhoof B, Nash DR, Boomsma JJ, Baer B. When Every Sperm Counts: Factors Affecting Male Fertility in The Honeybee Apis mellifera. Behav. Ecol. 2013;24(5):1192-1198. http://dx.doi.org/10.1093/beheco/art049
• Taylor MA, Guzmán-Novoa E, Morfin N, Buhr MM. Improving Viability of Cryopreserved Honey Bee (Apis mellifera L.) Sperm with Selected Diluents, Cryoprotectants and Semen Dilution Ratios. Theriogenology, 2009;72(2):149-159. https://doi.org/10.1016/j.theriogenology.2009.02.012
• Tofilski A. A Scientific Note on Amoeboid Movement of Honey Bee Semen. Apidologie, 2014;45:637–640. http://dx.doi.org/10.1007/s13592-014-0269-2
• Uysal O, Bucak MN. The Role of Different Trehalose Concentrations and Cooling Rates in Freezing of Ram Semen. Ankara Univ. Vet. Fak. Derg. 2009;56(2):99-103. https://doi.org/10.1501/Vetfak_0000002176
• Wegener J, Bienefeld K. Toxicity of Cryoprotectants to Honey Bee Semen and Queens. Theriogenology, 2012;77(3):600-607. http://dx.doi.org/10.1016/j.theriogenology.2011.08.036
• Wegener J, May T, Bienefeld K, Kamp N. New Methods and Media for The Centrifugation of Honey Bee (Hymenoptera: Apidae) Drone Semen. J. Econ. Entomol. 2014;107(1):47-53. http://dx.doi.org/10.1603/EC13159
• Wegener J, May T, Kamp G, Bienefeld K. A Successful New Approach to Honeybee Semen Cryopreservation. Cryobiology 2014;69(2):236-242. http://dx.doi.org/10.1016/j.cryobiol.2014.07.011
• Wegener J, May T, Knollmann U, Kamp G, Müller K, Bienefeld K. In Vivo Validation of In Vitro Quality Tests for Cryopreserved Honey Bee Semen. Cryobiology, 2012;65(2):126-131. http://dx.doi.org/10.1016/j.cryobiol.2012.04.010
• Woyke J. Naturalne I Sztuczne Unasienianie Matek Pszczelich. Pszczelnicze Zeszyty Naukowe, 1960;4(3/4):183-275
• Woyke J. Natural and Artificial Insemination of Queen Honeybees. Bee World, 1962;43(1):21-25. http://dx.doi.org/10.1080/0005772X.1962.11096922
• Woyke J. Correlations Between The Age at Which Honeybee Brood was Grafted, Characteristics of The Resultant Queens, and Results of Insemination. J. Apic. Res. 1971;10(1):45-55. http://dx.doi.org/10.1080/00218839.1971.11099669
• Woyke J. Ultrastructure of Single and Multiple Diploid Honeybee Spermatozoa. J. Apic. Res. 1984;23(3):123-135. http://dx.doi.org/10.1080/00218839.1984.11100621
• Yániz JL, Silvestre MA, Santolaria P. Sperm Quality Assessment in Honey Bee Drones. Biology (Basel), 2020;9(7):1-16. http://dx.doi.org/10.3390/biology9070174
• Yániz J, Palacín I, Santolaria P. Effect of Chamber Characteristics, Incubation, and Diluent on Motility of Honey Bee (Apis mellifera) Drone Sperm. Apidologie, 2019;50(4):472-481. http://dx.doi.org/10.1007/s13592-019-00659-y
• Yu W-H, Li Z-H, Yang W-M, Li G-Z, Zhou X-M et al. Comparison Between Two Methods for Staining DNA of Apoptotic Spermatozoa. Zhonghua nan ke xue = National Journal of Andrology, 2005;11 (2):101-103
• Yue C, Schröder M, Bienefeld K, Genersch E. Detection of Viral Sequences in Semen of Honeybees (Apis mellifera): Evidence for Vertical Transmission of Viruses Through Drones. J. Invertebr. Pathol. 2006;92 (2):105-108. http://dx.doi.org/10.1016/j.jip.2006.03.001