Histomorphological description of the reproductive system in mated honey bee queens

References

• Alaux, C., Folschweiller, M., McDonnell, C., Beslay, D., Cousin, M., Dussaubat, C., Brunet, J.-L., & Conte, Y. L. (2011). Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). Journal of Invertebrate Pathology, 106(3), 380–385. https://doi.org/https://doi.org/10.1016/j.jip.2010.12.005
   PubMed Web of Science ®Google Scholar
• Amiri, E., Strand, M. K., Rueppell, O., & Tarpy, D. R. (2017). Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health. Insects, 8(2), 48. https://doi.org/https://doi.org/10.3390/insects8020048
   PubMed Web of Science ®Google Scholar
• Baer, B., Collins, J., Maalaps, K., Boer, S. P. A. & den, (2016). Sperm use economy of honeybee (Apis mellifera) queens. Ecology and Evolution, 6(9), 2877–2885. https://doi.org/https://doi.org/10.1002/ece3.2075
   PubMed Web of Science ®Google Scholar
• Berger, B., & da Cruz-Landim, C. (2009). Ultrastructural analysis of the effect of mating delay on cell death in the ovaries of virgin honey bee (Apis mellifera L.) queens. Journal of Apicultural Research, 48(1), 60–66. https://doi.org/https://doi.org/10.3896/IBRA.1.48.1.12
   Web of Science ®Google Scholar
• Berger-Twelbeck, P., & Dorn, A. (1994). Larval-adult oviduct transformation in an insect (Oncopeltus fasciatus): Cytological study. Tissue and Cell, 26(5), 785–795. https://doi.org/https://doi.org/10.1016/0040-8166(94)90061-2
   PubMed Web of Science ®Google Scholar
• Bernet, D., Schmidt, H., Meier, W., Burkhardt‐Holm, P., & Wahli, T. (1999). Histopathology in fish: Proposal for a protocol to assess aquatic pollution. Journal of Fish Diseases, 22(1), 25–34. https://doi.org/https://doi.org/10.1046/j.1365-2761.1999.00134.x
   Web of Science ®Google Scholar
• Beyer, M., Junk, J., Eickermann, M., Clermont, A., Kraus, F., Georges, C., Reichart, A., & Hoffmann, L. (2018). Winter honey bee colony losses, Varroa destructor control strategies, and the role of weather conditions: Results from a survey among beekeepers. Research in Veterinary Science, 118, 52–60. https://doi.org/https://doi.org/10.1016/j.rvsc.2018.01.012
   PubMed Web of Science ®Google Scholar
• Biliński, S. M., & Jaglarz, M. K. (1999). Organization and possible functions of microtubule cytoskeleton in hymenopteran nurse cells. Cell Motility and the Cytoskeleton, 43(3), 213–220. https://doi.org/https://doi.org/10.1002/(SICI)1097-0169(1999)43:3 < 213::AID-CM4 > 3.0.CO;2-I
   PubMed Web of Science ®Google Scholar
• Bresslau, E. (1905). Der samenblasengang der bienenkönigin (Studien über den geschlechtsapparat und die fortpflanzung der bienen. I).
   Google Scholar
• Brown, A. P., Drew, P., Knight, B., Marc, P., Troth, S., Wuersch, K., & Zandee, J. (2016). Graphical display of histopathology data from toxicology studies for drug discovery and development: An industry perspective. Regulatory Toxicology and Pharmacology : RTP, 82, 167–172. https://doi.org/https://doi.org/10.1016/j.yrtph.2016.10.009
   PubMed Web of Science ®Google Scholar
• Burkle, L. A., Marlin, J. C., & Knight, T. M. (2013). Plant-pollinator interactions over 120 years: Loss of species, co-occurrence, and function. Science (New York, N.Y.), 339(6127), 1611–1615. https://doi.org/https://doi.org/10.1126/science.1232728
   PubMed Web of Science ®Google Scholar
• Camargo, J., & Mello, M. (1970). Anatomy and histology of the genital tract, spermatheca, spermathecal duct and glands of Apis Mellifica queens (Hymenoptera: Apidae). Apidologie, 1(4), 351–373. https://doi.org/https://doi.org/10.1051/apido:19700401
   Google Scholar
• Carreck, N. L., Andree, M., Brent, C. S., Cox-Foster, D., Dade, H. A., Ellis, J. D., Hatjina, F., Englesdorp, D. & van, (2013). Standard methods for Apis mellifera anatomy and dissection. Journal of Apicultural Research, 52(4), 1–40. https://doi.org/https://doi.org/10.3896/IBRA.1.52.4.03
   Web of Science ®Google Scholar
• Colin, M. E., Ball, B. V., & Kilani, M. (1999, May 19–30). Bee disease diagnosis. In Options Méditerranéennes. Série B : Etudes et Recherches (CIHEAM). Presented at the Course on Bee Disease Diagnosis. CIHEAM-IAMZ.
   Google Scholar
• Crissman, J. W., Goodman, D. G., Hildebrandt, P. K., Maronpot, R. R., Prater, D. A., Riley, J. H., Seaman, W. J., & Thake, D. C. (2004). Best practices guideline: Toxicologic histopathology. Toxicologic Pathology, 32(1), 126–131. https://doi.org/https://doi.org/10.1080/01926230490268756
   PubMed Web of Science ®Google Scholar
• Cruz-Landim, C., & Patrício, K. (2010). Nuclear activity in Apis mellifera L. (Hymenoptera, Apidae) queen ovary cells demonstrated by silver nitrate impregnation and ultrastructure. Brazilian Journal of Biology = Revista Brasleira de Biologia, 70(4), 1069–1073. https://doi.org/https://doi.org/10.1590/s1519-69842010000500023
   PubMed Web of Science ®Google Scholar
• de Almeida Rossi, C., Roat, T. C., Tavares, D. A., Cintra-Socolowski, P., & Malaspina, O. (2013). Brain morphophysiology of Africanized bee Apis mellifera exposed to sublethal doses of imidacloprid. Archives of Environmental Contamination and Toxicology, 65(2), 234–243. https://doi.org/https://doi.org/10.1007/s00244-013-9897-1
   PubMed Web of Science ®Google Scholar
• DiDio, L. J. (1995). Marcello Malpighi: The father of microscopic anatomy. Italian journal of anatomy and embryology = Archivio italiano di anatomia ed embriologia, 100, 3–9.
   PubMedGoogle Scholar
• Domingues, C. E. C., Abdalla, F. C., Balsamo, P. J., Pereira, B. V. R., Hausen, M. d A., Costa, M. J., & Silva-Zacarin, E. C. M. (2017). Thiamethoxam and picoxystrobin reduce the survival and overload the hepato-nephrocitic system of the Africanized honeybee. Chemosphere, 186, 994–1005. https://doi.org/https://doi.org/10.1016/j.chemosphere.2017.07.133
   PubMed Web of Science ®Google Scholar
• Fiette, L., & Slaoui, M. (2011). Necropsy and sampling procedures in rodents. In J.-C. Gautier (Ed.), Drug safety evaluation: Methods and protocols, methods in molecular biology (pp. 39–67). Humana Press. https://doi.org/https://doi.org/10.1007/978-1-60761-849-2_3
   Google Scholar
• Fischer, A. H., Jacobson, K. A., Rose, J., & Zeller, R. (2008). Hematoxylin and eosin staining of tissue and cell sections. CSH Protocols, 2008, pdb.prot4986. https://doi.org/https://doi.org/10.1101/pdb.prot4986
   PubMedGoogle Scholar
• Forfert, N., Troxler, A., Retschnig, G., Gauthier, L., Straub, L., Moritz, R. F. A., Neumann, P., & Williams, G. R. (2017). Neonicotinoid pesticides can reduce honeybee colony genetic diversity. Plos One, 12(10), e0186109. https://doi.org/https://doi.org/10.1371/journal.pone.0186109
   PubMed Web of Science ®Google Scholar
• Gauthier, L., Ravallec, M., Tournaire, M., Cousserans, F., Bergoin, M., Dainat, B., Miranda, J. R. & de, (2011). Viruses associated with ovarian degeneration in Apis mellifera L. queens. Plos One, 6(1), e16217. https://doi.org/https://doi.org/10.1371/journal.pone.0016217
   PubMed Web of Science ®Google Scholar
• Gerber, G. H., Neill, G. B., & Westdal, P. H. (1978). The anatomy and histology of the internal reproductive organs of the sunflower beetle, Zygogramma exclamationis (Coleoptera: Chrysomelidae). Canadian Journal of Zoology, 56(12), 2542–2553. https://doi.org/https://doi.org/10.1139/z78-342
   Web of Science ®Google Scholar
• Grozinger, C. M., & Flenniken, M. L. (2019). Bee viruses: Ecology, pathogenicity, and impacts. Annual Review of Entomology, 64, 205–226. https://doi.org/https://doi.org/10.1146/annurev-ento-011118-111942
   PubMed Web of Science ®Google Scholar
• Gutzeit, H. O., Zissler, D., & Fleig, R. (1993). Oogenesis in the honeybee Apis mellifera: Cytological observations on the formation and differentiation of previtellogenic ovarian follicles. Roux’s. Roux's Archives of Developmental Biology : The Official Organ of the EDBO, 202(3), 181–191. https://doi.org/https://doi.org/10.1007/BF00365309
   PubMedGoogle Scholar
• Haarmann, T., Spivak, M., Weaver, D., Weaver, B., & Glenn, T. (2002). Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. Journal of Economic Entomology, 95(1), 28–35. https://doi.org/https://doi.org/10.1603/0022-0493-95.1.28
   PubMed Web of Science ®Google Scholar
• Halpern, W. G., Ameri, M., Bowman, C. J., Elwell, M. R., Mirsky, M. L., Oliver, J., Regan, K. S., Remick, A. K., Sutherland, V. L., Thompson, K. E., Tremblay, C., Yoshida, M., & Tomlinson, L. (2016). Scientific and regulatory policy committee points to consider review: Inclusion of reproductive and pathology end points for assessment of reproductive and developmental toxicity in pharmaceutical drug development. Toxicologic Pathology, 44(6), 789–809. https://doi.org/https://doi.org/10.1177/0192623316650052
   PubMed Web of Science ®Google Scholar
• Higes, M., Martín‐Hernández, R., Botías, C., Bailón, E. G., González, ‐Porto, A. V., Barrios, L., Nozal, M. J., del, Bernal, J. L., Jiménez, J. J., Palencia, P. G., & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(10), 2659–2669. https://doi.org/https://doi.org/10.1111/j.1462-2920.2008.01687.x
   PubMed Web of Science ®Google Scholar
• Jackson, J. T., Tarpy, D. R., & Fahrbach, S. E. (2011). Histological estimates of ovariole number in honey bee queens, Apis mellifera, reveal lack of correlation with other queen quality measures. Journal of Insect Science (Online), 11, 82. https://doi.org/https://doi.org/10.1673/031.011.8201
   PubMed Web of Science ®Google Scholar
• Kapil, R. P. (1962). Anatomy and histology of the female reproductive system ofApis indica F. (Hymenoptera, Apidae). Insectes Sociaux, 9(2), 145–163. https://doi.org/https://doi.org/10.1007/BF02224261
   Google Scholar
• Klenk, M., Koeniger, G., Koeniger, N., & Fasold, H. (2004). Proteins in spermathecal gland secretion and spermathecal fluid and the properties of a 29 kDa protein in queens of Apis mellifera. Apidologie, 35(4), 371–381. https://doi.org/https://doi.org/10.1051/apido:2004029
   Web of Science ®Google Scholar
• Koziy, R. V., Wood, S. C., Kozii, I. V., van Rensburg, C. J., Moshynskyy, I., Dvylyuk, I., & Simko, E. (2019). Deformed wing virus infection in honey bees (Apis mellifera L.). Veterinary Pathology, 56(4), 636–641. https://doi.org/https://doi.org/10.1177/0300985819834617
   PubMed Web of Science ®Google Scholar
• Laidlaw, H. H. (1944). Artificial insemination of the queen bee (Apis mellifera L.): Morphological basis and results. Journal of Morphology, 74(3), 429–465. https://doi.org/https://doi.org/10.1002/jmor.1050740307
   Google Scholar
• Landim, C. D. C., & Yabuki, A. T. (1995). Fine-structure and morphogenesis of the micropyle apparatus in bees eggs. Biocell, 9(2), 125–132.
   Web of Science ®Google Scholar
• Luna, L. G. (1968). Manual of histologic staining methods of the Armed Forces Institute of Pathology. Pathology, 3(3), 249.
   Google Scholar
• Mackensen, O., & Tucker, K. W. (1970). Instrumental insemination of queen bees. U.S. Agricultural Research Service.
   Google Scholar
• Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology Research, 109(3), 605–612. https://doi.org/https://doi.org/10.1007/s00436-011-2292-9
   PubMed Web of Science ®Google Scholar
• Martins, J. R., Anhezini, L., Dallacqua, R. P., Simões, Z. L. P., & Bitondi, M. M. G. (2011). A honey bee hexamerin, HEX 70a, is likely to play an intranuclear role in developing and mature ovarioles and testioles. Plos One, 6(12), e29006. https://doi.org/https://doi.org/10.1371/journal.pone.0029006
   PubMed Web of Science ®Google Scholar
• Mepham, B. L. (1991). Theory and practice of histological techniques, 3rd ed. J. D. Bancroft, A. Stevens (Eds). Churchill Livingstone, Edinburgh, 1990. No. of pages: 740. Price: £55. ISBN: 0 443 03559 8. The Journal of Pathology, 164(3), 281–281. https://doi.org/https://doi.org/10.1002/path.1711640316
   Google Scholar
• Morse, R. A., & Calderone, N. W. (2000). The value of honey bees as pollinators of U.S. crops in 2000. Bee culture, 128(3), 1–15.
   Google Scholar
• Mpakou, V. E., Nezis, I. P., Stravopodis, D. J., Margaritis, L. H., & Papassideri, I. S. (2006). Programmed cell death of the ovarian nurse cells during oogenesis of the silkmoth Bombyx mori. Development, Growth & Differentiation, 48(7), 419–428. https://doi.org/https://doi.org/10.1111/j.1440-169X.2006.00878.x
   PubMed Web of Science ®Google Scholar
• Nelson, J. A. (1915). The embryology of the honey bee. Princeton University Press.
   Google Scholar
• Patrício, K., & Cruz-Landim, C. (2002). Mating influence in the ovary differentiation in adult queens of Apis mellifera L. (Hymenoptera, Apidae). Brazilian Journal of Biology = Revista Brasleira de Biologia, 62(4A), 641–649. https://doi.org/https://doi.org/10.1590/s1519-69842002000400012
   PubMedGoogle Scholar
• Patrício, K., & Cruz-Landim, C. D. (2008). Morphological aspects of cell reabsorption in laying queens and workers of Apis mellifera (Hymenoptera, Apidae). Iheringia. Série Zoologia, 98(4), 421–424. https://doi.org/https://doi.org/10.1590/S0073-47212008000400001
   Web of Science ®Google Scholar
• Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution, 25(6), 345–353. https://doi.org/https://doi.org/10.1016/j.tree.2010.01.007
   PubMed Web of Science ®Google Scholar
• Ramamurty, P. S. (1977). Unusual intertrophocytic position of follicle cells in the nurse chamber of the honeybee queen ovary (Apis mellifica). Apidologie, 8(2), 205–216. https://doi.org/https://doi.org/10.1051/apido:19770208
   Web of Science ®Google Scholar
• Ricketts, T. H., Regetz, J., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S. S., Klein, A. M., Mayfield, M. M., Morandin, L. A., Ochieng', A., Potts, S. G., & Viana, B. F. (2008). Landscape effects on crop pollination services: Are there general patterns? Ecology Letters, 11(5), 499–515. https://doi.org/https://doi.org/10.1111/j.1461-0248.2008.01157.x
   PubMed Web of Science ®Google Scholar
• Sánchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., & Desneux, N. (2016). Are bee diseases linked to pesticides? A brief review. Environment International, 89–90, 7–11. https://doi.org/https://doi.org/10.1016/j.envint.2016.01.009
   PubMed Web of Science ®Google Scholar
• Simeunovic, P., Stevanovic, J., Cirkovic, D., Radojicic, S., Lakic, N., Stanisic, L., & Stanimirovic, Z. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research, 53(5), 545–554. https://doi.org/https://doi.org/10.3896/IBRA.1.53.5.09
   Web of Science ®Google Scholar
• Snodgrass, R. E. (1985). Anatomy of the honey bee. Cornell University Press.
   Google Scholar
• Stell, I. M. (2012). Understanding bee anatomy: A full colour guide. The Catford Press.
   Google Scholar
• Tanaka, É. D., Capella, I. C. S., & Hartfelder, K. (2006). Cell death in the germline – mechanisms and consequences for reproductive plasticity in social bees. Journal of Morphological Sciences, 23(1), 13.
   Google Scholar
• Tanaka, E. D., & Hartfelder, K. (2004). The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Structure & Development, 33(4), 431–442. https://doi.org/https://doi.org/10.1016/j.asd.2004.06.006
   PubMed Web of Science ®Google Scholar
• Tarpy, D. R., Keller, J. J., Caren, J. R., & Delaney, D. A. (2011). Experimentally induced variation in the physical reproductive potential and mating success in honey bee queens. Insectes Sociaux, 58(4), 569–574. https://doi.org/https://doi.org/10.1007/s00040-011-0180-z
   Web of Science ®Google Scholar
• Tomé, H. V. V., Martins, G. F., Lima, M. A. P., Campos, L. A. O., & Guedes, R. N. C. (2012). Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS One, 7(6), e38406. https://doi.org/https://doi.org/10.1371/journal.pone.0038406
   PubMed Web of Science ®Google Scholar
• Traver, B. E., & Fell, R. D. (2012). Low natural levels of Nosema ceranae in Apis mellifera queens. Journal of Invertebrate Pathology, 110(3), 408–410. https://doi.org/https://doi.org/10.1016/j.jip.2012.04.001
   PubMed Web of Science ®Google Scholar
• Vanbergen, A. J., & Initiative., T. I. P. (2013). Threats to an ecosystem service: Pressures on pollinators. Frontiers in Ecology and the Environment, 11(5), 251–259. https://doi.org/https://doi.org/10.1890/120126
   Web of Science ®Google Scholar
• West, J. B. (2013). Marcello Malpighi and the discovery of the pulmonary capillaries and alveoli. American Journal of Physiology. Lung Cellular and Molecular Physiology, 304(6), L383–L390. https://doi.org/https://doi.org/10.1152/ajplung.00016.2013
   PubMed Web of Science ®Google Scholar
• Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G., & Aizen, M. A. (2009). A meta-analysis of bees' responses to anthropogenic disturbance. Ecology, 90(8), 2068–2076. https://doi.org/https://doi.org/10.1890/08-1245.1
   PubMed Web of Science ®Google Scholar
• Wood, S. C., Kozii, I. V., Koziy, R. V., Epp, T., & Simko, E. (2018). Comparative chronic toxicity of three neonicotinoids on New Zealand packaged honey bees. Plos One, 13(1), e0190517. https://doi.org/https://doi.org/10.1371/journal.pone.0190517
   PubMed Web of Science ®Google Scholar
• Woyke, J. (2011). The mating sign of queen bees originates from two drones and the process of multiple mating in honey bees. Journal of Apicultural Research, 50(4), 272–283. https://doi.org/https://doi.org/10.3896/IBRA.1.50.4.04
   Web of Science ®Google Scholar
• Wu-Smart, J., & Spivak, M. (2016). Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Scientific Reports, 6, 32108. https://doi.org/https://doi.org/10.1038/srep32108
   PubMed Web of Science ®Google Scholar
• Zaluski, R., Justulin, L. A., & de Oliveira Orsi, R. (2017). Field-relevant doses of the systemic insecticide fipronil and fungicide pyraclostrobin impair mandibular and hypopharyngeal glands in nurse honeybees (Apis mellifera). Scientific Reports, 7(1), 15217. https://doi.org/https://doi.org/10.1038/s41598-017-15581-5
   PubMed Web of Science ®Google Scholar