Geometric morphometric characteristics of Apis mellifera honeybee in Kazakhstan




Abstract. Nuralieva U, Tajiyev K, Sheralieva Z, Toishimanov M, Moldakhmetova G, Temirbayeva K, Tajieva A. 2023. Geometric morphometric characteristics of Apis mellifera honeybee in Kazakhstan. Biodiversitas 24: 4402-4409. This study was conducted in the whole beekeeping region of Kazakhstan. We researched morphological studies using (45 colony bees in 5 main regions in various geographical and climatic zone environmental conditions. The obtained data were compared with the Apis mellifera carnica reference samples, Apis mellifera caucasica, and Apis mellifera mellifera. Morphometric identification was carried out using 19 landmarks by IdentiFly software. Almost all colonies showed belonging to the lineage C (about 85%), by subspecies to A. m. carnica, A. m. caucasica showed 11%, A. m. mellifera belonged to only 4%. Furthermore, using multivariate principal component analysis compared honeybee lineages between reference samples. There were significant differences in wing landmarks between lineages and subspecies (Mahalanobis square distance). By Mahalanobis, distances between the evolutionary lineages M differ from line C by 15.93 and from line O by 19.03 units. In contrast, the distance between lines C and O is insignificant, with satisfactory reliability. The forewing wing size evaluated centroid size, which showed the highest degree of honeybees in the west and south Kazakhstan zones. The percentage of variation in wing centroids was relatively small between analyzed samples (less than 1%) but extremely changed for reference samples A. m. carnica, A. m. caucasica, A. m. mellifera, where log centroid sizes showed 1.33%, 4.18%, and 4.67%, respectively. The results showed significant differences between populations in different climatic zones.


Abed F, Bachir-Bouiadjra B, Dahloum L, Yakubu A, Haddad A, Homrani A. 2021. Procruste analysis of forewing shape in two endemic honeybee subspecies Apis mellifera intermissa and A. m.sahariensis from the Northwest of Algeria. Biodiversitas 22: 154-164. DOI: 10.13057/biodiv/d220121.
Abou-Shaara HF. 2013. Wing venation characters of honey bees. Journal of Apiculture 28(2):79-86.
Aglagane A, Tofilski A, Er-Rguibi O, Laghzaoui EM, Kimdil L, El Mouden EH, Fuchs S, Oleksa A, Aamiri A, Aourir M. 2022. Geographical Variation of Honey Bee (Apis mellifera L. 1758) Populations in South-Eastern Morocco: A Geometric Morphometric Analysis. Insects 15(3): 288. DOI: 10.3390/insects13030288.
Alpatov VV. 1948. Breeds of the honey bee. Publishing House of the Moscow Society of Naturalists. Moscow.
Barour C, Baylac M. 2016. Geometric morphometric discrimination of the three African honeybee subspecies Apis mellifera intermissa, A. m. sahariensis and A. m. capensis (Hymenoptera, Apidae): Fore wing and hind wing landmark configurations. Journal of Hymenoptera Research 28,52: 61-70.
Berezin A. 2019. Methods of morphometry in determining the breed of honey bees. Biomics 11: 167-189. DOI: 10.31301/2221-6197.bmcs.2019-16.
Bouga M, Alaux C, Bienkowska M, Büchler R, Carreck NL, et al. 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research 50: 51–84. DOI: 10.3896/IBRA.
Bykova TO, Triseleva TA, Ivashov AV. et al. 2016. Morphogenetic diversity of the honeybee Apis mellifera L. from the mountain-forest zone of Crimea. Biol Bull Russ Acad Sci 43: 541–546. DOI: 10.1134/S1062359016060054
Bureau of National statistics of the Agency for strategic planning and reforms of the Republic of Kazakhstan. Statistics of developed, forestry, hunting and fisheries Total number of bee colony. .
Bustamante T, Baiser B, Ellis JD. 2020. Comparing classical and geometric morphometric methods to discriminate between the South African honey bee subspecies Apis mellifera scutellata and Apis mellifera capensis (Hymenoptera: Apidae). Apidologie 51:123-36. DOI: 10.1007/s13592-019-00651-6.
Bustamante T, Fuchs S, Grünewald B, Ellis JD. 2021. A geometric morphometric method and web application for identifying honey bee species (Apis spp.) using only forewings. Apidologie 52(3):697-706. DOI: 10.1007/s13592-021-00857-7.
?ápek J, Chlebo R. 2016. Wing morphometry of Slovak lines of Apis mellifera carnica workers and drones population. Acta fytotechn zootechn.19(2):41-4. DOI: 10.15414/afz.2016.19.02.41–44.
Chen C, Liu Z, Pan Q, Chen X, Wang H, Guo H, Liu S, Lu H, Tian S, Li R, Shi W. 2016. Genomic analyses reveal cemographic history and temperate adaptation of the newly discovered honey bee subspecies Apis mellifera sinisxinyuan n. ssp. Molecular Biology and Evolution 33: 1337–1348. DOI: 10.1093/molbev/msw017.
Dáttilo W, Cruz CP, Luna P, Ratoni B, Hinojosa-Díaz IA, Neves FS, Leponce M, Villalobos F, Guevara R. 2020. The Impact of the Honeybee Apis mellifera on the Organization of Pollination Networks Is Positively Related with Its Interactive Role throughout Its Geographic Range. Diversity 14: 917. DOI:10.3390/d14110917.
Dukku UH, Danailu G. 2020. An appraisal of subspecific classification of Apis mellifera L. in parts of West and Central Africa through landmark-based geometric morphometric analysis of forewings. Journal of Apicultural Research. 59(4):722-9. DOI: 10.1080/00218839.2019.1696009.
DuPraw EJ. 1964. Non-Linnean taxonomy, Nature 202: 849–852.
DuPraw EJ. 1965. Non-Linnean taxonomy and the systematics of honeybees. Systematic Zoology 14: 1–24. DOI: 10.2307/2411899.
Frisch K, Voigt S, Voigt T, Hellwig A, Verestek V, Weber Y. 2009. Extreme aridity prior to lake expansion deciphered from facies evolution in the Miocene Ili Basin, south?east Kazakhstan. Sedimentology 66: 1716-1745. DOI: 10.1111/sed.12556.
García CA, Rodrigues PJ, Tofilski A, Elen D, McCormak GP, Oleksa A, Henriques D, Ilyasov R, Kartashev A, Bargain C, Fried B. 2022. Using the software DeepWings© to classify honey bees across Europe through wing geometric morphometrics. Insects 13(12):1132. DOI: 10.3390/insects13121132.
Gerula D, Tofilski A, W?grzynowicz P, Skowronek W. 2009. Computer-assisted discrimination of honey bee subspecies used for breeding in Poland. Journal of Apicultural Science 53: 105–114.
Gomeh H, Rafie JN, Modaber M. 2016. Comparison of standard and geometric morphometric methods for discrimination of honey bees populations (Apis mellifera L.) in Iran. Biology Journal of entomology and zoology studies 4: 47-53.
Henriques D, Chávez-Galarza J, Teixeira JSG, Ferreira H, Neves CJ, Francoy TM, Pinto MA. 2020. Wing geometric morphometrics of workers and drones and single nucleotide polymorphisms provide similar genetic structure in the Iberian honey bee (Apis mellifera iberiensis). Insects 11 (2): 89. DOI:10.3390/insects11020089.
Ilyasov RA, Lee ML, Takahashi JI. Kwon HW, Nikolenko AG. 2020. A revision of subspecies structure of western honey bee Apis mellifera. Saudi Journal of Biological Sciences 27: 3615–3621. DOI:10.1016/j.sjbs.2020.08.001.
Janczyk A, Tofilski A. 2021. Monthly changes in honey bee forewings estimated using geometric morphometrics. Journal of Apicultural Science 65(1):139-46. DOI: 10.2478/jas-2021-0002.
Kambur M, Kekeço?lu, M. 2018. The current situation of Turkey honey bee (Apis mellifera L.) biodiversity and conservations studies. Biological Diversity and Conservation 11(1): 105-119. DOI: 10.13140/RG.2.2.12203.54568
Kandemir ?, Özkan A, Fuchs S. 2011. Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach. Apidologie 42: 618–627. DOI: 10.1007/s13592-011-0063-3.
Kekeço?lu M, Kambur M, Münir UÇ, Çaprazli T. 2020. Biodiversity of honey bees (Apis mellifera L.) in Turkey by geometric morphometric analysis. Biyolojik Çe?itlilik ve Koruma 12;13(3):282-9. DOI: 10.46309/biodicon.2020.773984.
Masaquiza D, Ferrán MO, Guamán S, Naranjo E, Vaca M, Curbelo LM, Arenal A. 2023. Geometric Morphometric Analysis of Wing Shape to Identify Populations of Apis mellifera in Camagüey, Cuba. Insects 22;14(3):306. DOI: 10.3390/insects14030306.
Meixner MD, Pinto MA, Bouga M, Kryger P, Ivanova E, Fuchs S. 2013. Standard methods for characterising subspecies and ecotypes of Apis mellifera. Journal of Apicultural Research 52: 1–28. DOI: 10.3896/IBRA.
Miguel I, Baylac M, Iriondo M, Manzano C, Garnery L, Estonba A. 2011. Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie 42: 150–161. DOI: 10.1051/apido/2010048.
Moldakhmetova GA, Mayer AA, Omarova KM, Grankin NN. 2022. Morphometric and economicly useful features of honeybees in east Kazakhstan region. Herald of science of s Seifullin Kazakh agro technical university 3 (114): 144-152. DOI: 10.51452/kazatu.2022.3(114).1148.
Nawrocka ?, Kandemir ?, Fuchs S, Tofilski ?. 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie 49: 172–184. DOI: 10.1007/s13592-017-0538-y.
Nedi? N, Francis RM, Stanisavljevi? L, Pihler I, Kezi? N, Bendixen C, Kryger P. 2014. Detecting population admixture in honey bees of Serbia. Journal of Apicultural Research 53 :303-13.DOI: 10.3896/IBRA.
Oleksa A, Tofilski A. 2015. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie 46: 49–60. DOI: 10.1007/s13592-014-0300-7.
Prabucki J, Samborski J, Chuda-Mickiewicz B. 2002. The use of three taxonomic characters for race identification of Middle European bee. Journal of Apicultural Science 46: 41–47.
Puškadija Z, Kova?i? M, Raguž N, Luki? B, Prešern J, Tofilski A. 2020. Morphological diversity of Carniolan honey bee (Apis mellifera carnica) in Croatia and Slovenia. Journal of Apicultural Research 60: 326-36. DOI: 10.1080/00218839.2020.1843847.
Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Springer, Berlin
Ruttner F, Tassencourt L, Louveaux J. 1978. Biometrical-Statistical Analysis of the Geographic Variability of Apis mellifera LI Material and Methods. Apidologie 9: 363-381. DOI: 10.1051/apido:19780408.
Salnikov V, Talanov Y, Polyakova S, Assylbekova A. Kauazov A, Bultekov N, Musralinova G, Kissebayev D, Beldeubayev Y. 2023. An Assessment of the Present Trends in Temperature and Precipitation Extremes in Kazakhstan. Climate 11: 33. DOI: 10.3390/cli11020033.
Janczyk A, Tofilski A. 2021. Monthly changes in honey bee forewings estimated using geometric morphometrics. Journal of Apicultural Science 65(1): 139-46. DOI: 10.2478/jas-2021-0002.
Sheppard WS, Arias MC, Grech A, Meixner MD. 1997. Apis mellifera ruttneri, a new honey bee subspecies from Malta. Apidologie 28: 287–293. DOI: 10.1051/apido:19970505.
Sheppard WS, Meixner MD. 2003. Apis mellifera pomonella, a new honeybee subspecies from central Asia. Apidologie 34: 367–375. DOI: 10.1051/apido:2003037.
Shimelkova RZ, Parzhanov ZA, Demidova IV, Aldiyarova AK. 2020. Reproduction of queen bees and Apis Mellifera Carnica colonies in the South of Kazakhstan. EurAsian Journal of BioSciences14.
Suleimenova N, Orynbasarova G, Suleimenova M, Bozhbanov A, Yerekeyeva S. 2021. Environmental Monitoring of the Sustainability and Productivity of the Agroecosystem of Oilseeds in South-East Kazakhstan. Journal of Ecological Engineering 22: 89-99. DOI:10.12911/22998993/139114.
Tofilski A. 2004. DrawWing, a program for numerical description of insect wings. Journal of Insect Science 4: 17. DOI: 10.1093/jis/4.1.17.
Tofilski A, MacLeod N. 2007. Automatic measurements of honeybee wings. Automated taxon identification in systematics: theory, approaches and applications, CRC Press, Boca Raton: 289–298.
Tofilski A. 2008. Using geometric morphometrics and standard morphometry to discriminate three honeybee subspecies. Apidologie 39: 558–563. DOI: 10.1051/apido:2008037.
Zahara I, Fahri F, Lamerkabel JS, Qashiratuttarafi Q, Juliandi B, Raffiudin R. 2022. Landmark-Based Geometric Morphometric of Apis dorsata and A. d. binghami Wing Venation in Indonesian Archipelagos. HAYATI Journal of Biosciences 29(5):658-68. DOI: 10.4308/hjb.29.5.658-668.