Morphometric Identification of An Unknown Honey Bee Colony: An Example From North India

Abrol, D. P. (2004). Introduction of Apis mellifera in Jammu and Kashmir: Present status and future prospects. Bee World, 85(2), 37-40. https://doi.org/10.1080/0005772X.2004.11099616 Search in Google Scholar

Albrecht, G. H. (1992). Assessing the affinities of fossils using canonical variates and generalized distances. Human Evolution, 7(4), 49-69. https://doi.org/10.1007/BF02436412 Search in Google Scholar

Atwal, A. S., & Goyal, N. P. (1973). Introduction of Apis mellifera in Punjab plains. Indian Bee Journal, 35(1/4), 1-9. Search in Google Scholar

Baken, E. K., Collyer, M. L., Kaliontzopoulou, A., Adams, D. C. (2021). geomorph v4.0 and gmShiny: Enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Methods in Ecology and Evolution, 12(12), 2355-2363. https://doi.org/10.1111/2041-210X.13723 Search in Google Scholar

Bookstein, F. L. (1991). Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press. Search in Google Scholar

Bouga, M., Alaux, C., Bienkowska, M., Büchler, R., Carreck, N. L., Cauia, E., … Wilde, J. (2011). A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50(1), 51-84. https://doi.org/10.3896/IBRA.1.50.1.06 Search in Google Scholar

Bustamante, T., Fuchs, S., Grünewald, B., Ellis, J. D. (2021). A geometric morphometric method and web application for identifying honey bee species (Apis spp.) using only forewings. Apidologie, 52(3), 697-706. https://doi.org/10.1007/s13592-021-00857-7 Search in Google Scholar

Carpenter, M. H., & Harpur, B. A. (2021). Genetic past, present, and future of the honey bee (Apis mellifera) in the United States of America. Apidologie, 52(1), 63-79. https://doi.org/10.1007/s13592-020-00836-4 Search in Google Scholar

Cornuet, J. M., Garnery, L., Solignac, M. (1991). Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics, 128(2), 393-403. https://doi.org/10.1093/genetics/128.2.393 Search in Google Scholar

De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I., Serrano, J. (2009). Biodiversity, conservation and current threats to European honeybees. Apidologie, 40(3), 263-284. https://doi.org/10.1051/apido/2009027 Search in Google Scholar

Dryden, I. L. (2021). Shapes package. R Foundation for Statistical Computing. Search in Google Scholar

DuPraw, E. J. (1965a). Non-Linnean taxonomy and the systematics of honeybees. Systematic Zoology, 14(1), 1-24. Search in Google Scholar

DuPraw, E. J. (1965b). The recognition and handling of honeybee specimens in non-Linnean taxonomy. Journal of Apicultural Research, 4(2), 71-84. Search in Google Scholar

Ellis, J. S., Soland-Reckeweg, G., Buswell, V. G., Huml, J. V., Brown, A., Knight, M. E. (2018). Introgression in native populations of Apis mellifera mellifera L: implications for conservation. Journal of Insect Conservation, 22(3), 377-390. https://doi.org/10.1007/s10841-018-0067-7 Search in Google Scholar

Estoup, A., Garnery, L., Solignac, M., Cornuet, J. M. (1995). Microsatellite variation in honey bee (Apis mellifera L.) populations: Hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics, 140(2), 679-695. https://doi.org/10.1093/genetics/140.2.679 Search in Google Scholar

Evans, J. D., Schwarz, R. S., Chen, Y. P., Budge, G., Cornman, R. S., Rua, P. D. la, … Pinto, M. A. (2013). Standard methods for molecular research in Apis mellifera. Journal of Apicultural Research, 52(4), 1-54. https://doi.org/10.3896/IBRA.1.52.4.11 Search in Google Scholar

Francoy, T. M., Wittmann, D., Drauschke, M., Müller, S., Steinhage, V., Bezerra-Laure, M. A., De Jong, D., Gonçalves, L. S. (2008). Identification of Africanized honey bees through wing morphometrics: Two fast and efficient procedures. Apidologie, 39(5), 488–494. https://doi.org/10.1051/apido:2008028 Search in Google Scholar

Galataud, J., Delatte, H., Techer, M. A., Simiand, C., Sookar, P., Reynaud, B., Clémencet, J. (2020). When European meets African honeybees (Apis mellifera L.) in the tropics: Morphological changes related to genetics in Mauritius Island (South-West Indian Ocean). PLoS ONE, 15(11), e0242053. https://doi.org/10.1371/journal.pone.0242053 Search in Google Scholar

Goyal, N. P. (1974). Apis cerana indica and Apis mellifera as complementary to each other for the development of apiculture. Bee World, 55(3), 98-101. https://doi.org/10.1080/0005772X.1974.11097506 Search in Google Scholar

Goyal, N. P. (1990). Introduction of Apis mellifera in India: Background and present status. Indian Bee Journal, 52(1-4), 57-59. Search in Google Scholar

Ibrahim, M. M., Chandel, Y. S., Anil. (2017). Morphometrics of Apis mellifera after five decades of its introduction in North-Western Himalayan region of India. Pakistan Journal of Zoology, 49(4), 1397-1403. https://doi.org/10.17582/journal.pjz/2017.49.4.1397.1403 Search in Google Scholar

Janczyk, A., & Tofilski, A. (2021). Monthly changes in honey bee forewings estimated using geometric morphometrics. Journal of Apicultural Science, 65(1), 139-146. https://doi.org/10.2478/jas-2021-0002 Search in Google Scholar

Jensen, A. B., Palmer, K. A., Boomsma, J. J., Pedersen, B. V. (2005). Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, 14(1), 93-106. https://doi.org/10.1111/j.1365-294X.2004.02399.x Search in Google Scholar

Kandemir, İ., Meixner, M. D., Ozkan, A., Sheppard, W. S. (2006). Genetic characterization of honey bee (Apis mellifera cypria) populations in northern Cyprus. Apidologie, 37(5), 547-555. https://doi.org/10.1051/apido:2006029 Search in Google Scholar

Kaur, H., Ganie, S. A., Tofilski, A. (2023). Fore wings of honey bee (Apis mellifera) from Jammu and Kashmir, India. Zenodo. https://doi.org/10.5281/zenodo.8071014 Search in Google Scholar

Kaur, H., Nedić, N., Tofilski, A. (2024). Influence of honey bee (Apis mellifera) breeding on wing venation in Serbia and neighbouring countries. PeerJ, 12, e17247. https://doi.org/10.7717/peerj.17247 Search in Google Scholar

Kekecoglu, M. (2018). Morphometric divergence of anatolian honeybees through loss of original traits: A dangerous outcome of Turkish apiculture. Sociobiology, 65(2), 232-243. https://doi.org/10.13102/sociobiology.v65i2.1895 Search in Google Scholar

Kekecoglu, M., Bouga, M., Soysal, M. İ., Harizanis, P. (2007). Morphometrics as a tool for the study of genetic variability of honey bees. Journal of Tekirdag Agricultural Faculty, 4(1), 7-15. Search in Google Scholar

Litvinoff, L., Menescardi, F., Porrini, L., Russo, R., Liendo, M. C., Nucci, A., … Galindo-Cardona, A. (2023). Morphometric and genetic characterization as tools for selection of Apis mellifera (Hymenoptera: Apidae) stocks in an area of natural hybridization in Argentina. Frontiers in Insect Science, 2. https://doi.org/10.3389/finsc.2022.1073999 Search in Google Scholar

Magnus, R. M., Tripodi, A. D., Szalanski, A. L. (2011). Mitochondrial DNA diversity of honey bees, Apis mellifera L. (Hymenoptera: Apidae) from queen breeders in the United States. Journal of Apicultural Science, 55(1), 37-46. Search in Google Scholar

Masaquiza, D., Ferrán, M. O., Guamán, S., Naranjo, E., Vaca, M., Curbelo, L. M., Arenal, A. (2023). Geometric morphometric analysis of wing shape to identify populations of Apis mellifera in Camagüey, Cuba. Insects, 14(3), 306. https://doi.org/10.3390/insects14030306 Search in Google Scholar

Maul, V., & Hähnle, A. (1994). Morphometric studies with pure bred stock of Apis mellifera carnica Pollmann from Hessen. Apidologie, 25(2), 119-132. https://doi.org/10.1051/apido:19940201 Search in Google Scholar

Meixner, M. D., Costa, C., Kryger, P., Hatjina, F., Bouga, M., Ivanova, E., Büchler, R. (2010). Conserving diversity and vitality for honey bee breeding. Journal of Apicultural Research, 49(1), 85-92. https://doi.org/10.3896/IBRA.1.49.1.12 Search in Google Scholar

Meixner, M. D., Pinto, M. A., Bouga, M., Kryger, P., Ivanova, E., Fuchs, S. (2013). Standard methods for characterising subspecies and ecotypes of Apis mellifera. Journal of Apicultural Research, 52(4), 1-28. https://doi.org/10.3896/IBRA.1.52.4.05 Search in Google Scholar

Meixner, M. D., Sheppard, W. S., Poklukar, J. (1993). Asymmetrical distribution of a mitochondrial DNA polymorphism between 2 introgressing honey bee subspecies. Apidologie, 24(2), 147-153. https://doi.org/10.1051/apido:19930207 Search in Google Scholar

Meixner, M. D., Worobik, M., Wilde, J., Fuchs, S., Koeniger, N. (2007). Apis mellifera mellifera in eastern Europe - morphometric variation and determination of its range limits. Apidologie, 38(2), 191-197. https://doi.org/10.1051/apido:2006068 Search in Google Scholar

Momeni, J., Parejo, M., Nielsen, R. O., Langa, J., Montes, I., Papoutsis, L., … Estonba, A. (2021). Authoritative subspecies diagnosis tool for European honey bees based on ancestry informative SNPs. BMC Genomics, 22(1), 101. https://doi.org/10.1186/s12864-021-07379-7 Search in Google Scholar

Nawrocka, A., Kandemir, İ., Fuchs, S., Tofilski, A. (2018). Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie, 49(2), 172-184. https://doi.org/10.1007/s13592-017-0538-y Search in Google Scholar

Oleksa, A., Căuia, E., Siceanu, A., Puškadija, Z., Kovačić, M., Pinto, M. A., … Tofilski, A. (2022). Collection of wing images for conservation of honey bees (Apis mellifera) biodiversity in Europe. Zenodo. https://doi.org/10.5281/zenodo.7244070 Search in Google Scholar

Oleksa, A., Căuia, E., Siceanu, A., Puškadija, Z., Kovačić, M., Pinto, M. A., … Tofilski, A. (2023). Honey bee (Apis mellifera) wing images: A tool for identification and conservation. GigaScience, 12, giad019. https://doi.org/10.1093/gigascience/giad019 Search in Google Scholar

Oleksa, A., Chybicki, I., Tofilski, A., Burczyk, J. (2011). Nuclear and mitochondrial patterns of introgression into native dark bees (Apis mellifera mellifera) in Poland. Journal of Apicultural Research, 50(2), 116-129. https://doi.org/10.3896/IBRA.1.50.2.03 Search in Google Scholar

Parejo, M., Henriques, D., Pinto, M. A., Soland-Reckeweg, G., Neuditschko, M. (2018). Empirical comparison of microsatellite and SNP markers to estimate introgression in Apis mellifera mellifera. Journal of Apicultural Research, 57(4), 504-506. https://doi.org/10.1080/00218839.2018.1494894 Search in Google Scholar

Porrini, L. P., Quintana, S., Brasesco, C., Maggi, M. D., Porrini, M. P., Garrido, M. P., Fernández Iriarte, P. J., Eguaras, M. J. (2022). Current genetic diversity of managed and commercially produced Apis mellifera colonies in Argentina inferred by wing geometric morphometrics and COI-COII mtDNA locus. Apidologie, 53(5), 61. https://doi.org/10.1007/s13592-022-00970-1 Search in Google Scholar

Porrini, L. P., Quintana, S., Brasesco, C., Porrini, M. P., Garrido, P. M., Eguaras, M. J., Müller, F., Fernandez Iriarte, P. (2020). Southern limit of Africanized honey bees in Argentina inferred by mtDNA and wing geometric morphometric analysis. Journal of Apicultural Research, 59(4), 648-657. https://doi.org/10.1080/00218839.2019.1681116 Search in Google Scholar

R Core Team. (2018). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/ Search in Google Scholar

Rahman, A. (2017). Apiculture in India. Directorate of Knowledge Management in Agriculture, Indian Council of Agricultural Research. Search in Google Scholar

Rao, G. M., Rao, K. S., Chaudhary, O. P. (1993). Introduction of Apis mellifera in India. Khadi Gramodyog, 34(11 & 12), 815-819. Search in Google Scholar

Rinderer, T. E., Buco, S. M., Rubink, W. L., Daly, H. V., Stelzer, J. A., Riggio, R. M., Baptista, F. C. (1993). Morphometric identification of Africanized and European honey bees using large reference populations. Apidologie, 24(6), 569-585. https://doi.org/10.1051/apido:19930605 Search in Google Scholar

Rodrigues, P. J., Gomes, W., Pinto, M. A. (2022). DeepWings©: Automatic wing geometric morphometrics classification of honey bee (Apis mellifera) subspecies using deep learning for detecting landmarks. Big Data and Cognitive Computing, 6(3), Article 3. https://doi.org/10.3390/bdcc6030070 Search in Google Scholar

Ruttner, F. (1988a). Biogeography and taxonomy of honeybees. Springer. Search in Google Scholar

Ruttner, F. (1988b). Breeding techniques and selection for breeding of the honeybee. British Isles Bee Breeders’ Association. Search in Google Scholar

Ruttner, F. (1991). Biometrical control of breeding. Journal of Apicultural Research, 30(2), 113-115. Search in Google Scholar

Ruttner, F., Tassencourt, L., Louveaux, J. (1978). Biometrical-statistical analysis of the geographic variability of Apis mellifera L. Apidologie, 9(4), 363-381. https://doi.org/10.1051/apido:19780408 Search in Google Scholar

Silva, F. L. da, Grassi Sella, M. L., Francoy, T. M., Costa, A. H. R. (2015). Evaluating classification and feature selection techniques for honeybee subspecies identification using wing images. Computers and Electronics in Agriculture, 114, 68-77. https://doi.org/10.1016/j.compag.2015.03.012 Search in Google Scholar

Tofilski, A. (2008). Using geometric morphometrics and standard morphometry to discriminate three honeybee subspecies. Apidologie, 39(5), 558-563. https://doi.org/10.1051/apido:2008037 Search in Google Scholar

Venables, W. N., & Ripley, B. D. (2002). Modern Applied Statistics with S (Fourth). Springer. https://www.stats.ox.ac.uk/pub/MASS4/ Search in Google Scholar