NOTES RELATED TO IMMATURE OVARY OF THE FOREST CATERPILLAR HUNTER ADULT CALOSOMA SYCOPHANTA (LINNAEUS, 1758) (COLEOPTERA: CARABIDAE)-LIGHT AND ELECTRON MICROSCOPY STUDIES
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Jun 5, 2024
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Abstract
Calosoma sycophanta (Linnaeus, 1758) (Coleoptera: Carabidae) is one of the most important predators of pine processionary moth, Thaumetopoea pityocampa (Denis & Schiffermüller) (Lepidoptera: Thaumetopoeidae) larvae and pupae. Therefore, it is an important species in biological control. Relatively few studies have focused on the female reproductive system in C. sycophanta. We use light and electron microscopy to study the female reproductive anatomy and histology of C. sycophanta. The female reproductive organs of C. sycophanta consist of paired ovaries, lateral oviducts, a common oviduct, and a genital chamber. Each ovary is formed of about 12 polytrophic meroistic ovarioles. In the longitudinal section of the ovary, it was noticed that the vitellarium region located after the germarium contains egg chambers that develop in a linear order, and it is distinguished that each chamber consists of an oocyte and nurse cells formed by incomplete cytokinesis from the same germ cell. The ovary connects to the lateral canal through a pedicel, and within each chamber, there's an oocyte alongside 16 food cells, all encircled by follicular cells. The epithelium of the pedicel and lateral oviduct is formed of monolayered cells overlaid by a muscle layer. The intima layer is distinguished on the side of the epithelium facing the lumen. Spines are seen in the intima. The purpose of this study is to describe ovarian histoanatomy in C. sycophanta and compare it with other coleopteran species, including Carabidae.
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Özyurt Koçakoğlu, N., Arslan, H., & Candan, S. (2024). NOTES RELATED TO IMMATURE OVARY OF THE FOREST CATERPILLAR HUNTER ADULT CALOSOMA SYCOPHANTA (LINNAEUS, 1758) (COLEOPTERA: CARABIDAE)-LIGHT AND ELECTRON MICROSCOPY STUDIES. Acta Entomologica Serbica, 29(1), 53-62. https://doi.org/10.5281/zenodo.11487034
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References
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Camargo Mathias, M. I., Sánchez, P., Denardi, S. E., & Caetano, F. H. (2011). Rhyncophorus palmarum L.(Linnaeus, 1758): A morphological and histological study of the female reproductive system. Microscopy Research and Technique, 74(9), 853-862. https://doi:10.1002/jemt.20969.
Chapman, R. (2004). The reproductive system, The insects structure and function (4b.). Cambridge: Cambridge University Press, Cambridge, 4th ed., 319-377.
Cheetham. T. (1992). Anatomy and histology of tissues associated with egg deposition in Chrysomela scripta Fabr. (Coleoptera: Chrysomelidae). Journal of the Kansas Entomological Society, 65(2), 101-114. https://www.jstor.org/stable/25085340.
Church, S. H., de Medeiros, B. A. S., Donoughe, S., Marquez Reyes, N. L., & Extavour, C. G. (2021). Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution. Proceedings of the Royal Society B: Biological Sciences, 288(1950). https://doi.org/10.1098/rspb.2021.0150.
Crowson, R. A. (1960). The phylogeny of Coleoptera. Annual Review of Entomology, 5, 111-134. https://doi.org/10.1146/annurev.en.05.010160.000551.
Devasahayam, S., Vidyasagar, P. S .P. V., & Koya, K. M. (1998). Reproductive system of pollu beetle, Longitarsus nigripennis Motschulsky (Coleoptera: Chrysomelidae), a major pest of black pepper, Piper nigrum Linnaeus. Journal of the Entomological Research Society, 22(1), 77-82
Duran, D .P., & Gough, H. M. (2020). Validation of tiger beetles as distinct family (Coleoptera: Cicindelidae), review and reclassification of tribal relationships. Systematic Entomology, 45, 723-729. https://doi.org/10.1111/syen.12440.
El Naggar, S. E., Mohamed, H. F., & Mahmoud, E. A. (2010). Studies on the morphology and histology of the ovary of red palm weevil female irradiated with gamma rays. Journal of Asia-Pacific Entomology, 13(1), 9-16. https://doi.org/10.1016/j.aspen.2009.08.004.
Escherich, K. (1942). Leben und Forschen. Anzeiger für Schädlingskunde, 18(10), 109-111.
Gao, J., Wang, J., & Chen, H. (2021). Ovary Structure and Oogenesis of Trypophloeus klimeschi (Coleoptera: Curculionidae: Scolytinae). Insects, 12(12), 1099. doi: 10.3390/insects12121099.
Gomez, R. A., Mercati, D., Lupetti, P., Fanciulli, P. P., & Dallai, R. (2023). Morphology of male and female reproductive systems in the ground beetle Apotomus and the peculiar sperm ultrastructure of A. rufus (P. Rossi, 1790) (Coleoptera, Carabidae). Arthropod Structure & Development, 72, 101217. doi: 10.1016/j.asd.2022.101217.
Gullan, P. J., & Cranston, P. S. (2010). The Insects: an Outline of Entomology, WileyBlackwell Publication; Böcekler: Entomolojinin Ana Hatları. Çeviri Editörü; Ali Gök, 4. basımdan çeviri, Nobel Akademik Yayıncılık, 580pp.
Hurka, K. (1996). Carabidae of the Czech and Slovak Republics Print Centrum. Kabourek Yayınları, 565pp.
Jaglarz, M. K. (1998). The number that counts. Phylogenetic implications of the number of nurse cells in ovarian follicles. Folia Histochemica et Cytobiologica, 36,167-178.
Klowden, M. J. (2007). The Reproductive System, Physiological Systems in Insects, (2nd ed). U.S.A: Academic Press, 181-223.
Korman, A. K., & Oseto, C. Y. (1989). Structure of the female reproductive system and maturation of oöcytes in Smicronyx fulvus (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 82(1), 94-100. https://doi.org/10.1093/aesa/82.1.94.
Lee, W. Y., Tseung, C. K., & Chang, T. H. (1985). An ultrastructural study on the ovariole, development in the oriental fruit fly. Bulletin of the Institute of Zoology, Academia Sinica, 24,1-10.
Lodos, N. (1989). Türkiye Entomolojisi IV. Ege Üniversitesi Ziraat Fakültesi Ofset Basımevi, Bornova-İzmir, 250pp.
Lodos, N. (1995). Silphidae, Türkiye Entomolojisi IV (Kısım I). Ege Üniversitesi Yayınları No: 493. İzmir, 68-76.
Lövei, G. L. and Sunderland, K. D. (1996). Ecology and behavior of Ground Beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41, 231-256. https://doi.org/10.1146/annurev.en.41.010196.001311.
Ma, N., & Hua, B. (2010). Structure of ovarioles and oogenesis in Panorpa liui Hua (Mecoptera: Panorpidae). Acta Entomologica Sinica, 53(11), 1220-1226.
Maffei, E. M. D., Fragoso, D. D. B., Pompolo, S. D. G., & Serrão, J. E. (2001). Morphological and cytogenetical studies on the female and male reproductive organs of Eriopis connexa Mulsant (Coleoptera, Polyphaga, Coccinellidae). Netherlands Journal of Zoology, 51(4), 483-496. doi:10.1163/156854201X00224.
Özyurt Koçakoğlu, N., Candan, S., & Arslan, H. (2023). Notes on the female reproductive system of the red and black froghopper, Cercopis vulnerata Rossi, 1807 (Hemiptera: Cercopidae) light and electron microscopy studies. Acta Zoologica. https://doi.org/10.1111/azo.12465.
Özyurt Koçakoğlu, N., Candan, S., & Güllü, M. (2021). Morphology of the reproductive tract of females of leaf beetle Chrysomela populi (Chrysomelidae: Coleoptera). Biologia, 76(11), 3257-3265. Doi: 10.1007/s11756-021-00796-9.
Özyurt Koçakoğlu, N., Candan, S., & Güllü, M. (2022). Structural and ultrastructural characters of the reproductive tract in females of the mint leaf beetle Chrysolina herbacea (Duftschmid 1825)(Coleoptera: Chrysomelidae). Acta Zoologica, 103(3), 365-375. https://doi.org/10.1111/azo.12379.
Parks, J. J., & Larsen, J. R. (1965). A morphological study of the female reproductive system and follicular development in the mosquito Aedes aegypti (L.). Transactions of the American Microscopical Society, 84(1), 88-98. https://www.jstor.org/stable/3224545.
Salazar, K., Boucher, S., & Serrão, J. E. (2017). Structure and ultrastructure of the ovary in the South American Veturius sinuatus (Eschscholtz)(Coleoptera, Passalidae). Arthropod Structure & Development, 46(4), 613-626.
doi: 10.1016/j.asd.2017.03.007.
Serttaş, A., & Çetin, H. (2014). Biyolojik Mücadelede Kullanılan Calosoma sycophanta L.'nın Laboratuvarlardaki Üretim Miktarının Arttırılması. II. Ulusal Akdeniz Orman Ve Çevre Sempozyumu “Akdeniz ormanlarının geleceği: Sürdürülebilir toplum ve çevre” 22-24 Ekim 2014, Isparta, Türkiye. 444-448.
Shirai, Y., Takahashi, M., Ote, M., Kanuka, H., & Daimon, T. (2023). DIPA-CRISPR gene editing in the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). Applied Entomology and Zoology, 58(3), 273-278. https://doi.org/10.1101/2023.04.07.535996.
Stein, F. (1847). Vergleichende Anatomie und Physiologie der Insekten, 1. Die weiblichen Geschlechtsorgane der Käfer. Berlin: Duncker ve Humblot. 139 pp.
Stys, P., Bilinski, S., (1990). Ovarioles types and the phylogeny of Hexapods. Biological Reviews, 65, 401-429. https://doi.org/10.1111/j.1469-185X.1990.tb01232.x.
Szklarzewicz, T., Michalik, A., Kalandyk‐Kołodziejczyk, M., Kobiałka, M., & Simon, E. (2014). Ovary of Matsucoccus pini (Insecta, Hemiptera, Coccinea: Matsucoccidae): morphology, ultrastructure, and phylogenetic implications. Microscopy Research and Technique, 77(5), 327-334. doi: 10.1002/jemt.22347.
Vommaro, M. L., Donato, S., & Giglio, A. (2022). Virtual sections and 3D reconstructions of female reproductive system in a carabid beetle using synchrotron X - ray phase - contrast microtomography. Zoologischer Anzeiger, 298, 123-130. https://doi.org/10.1016/j.jcz.2022.04.001.
Wan, N. A., Nurul, W., Yaakop, S., & Norefrina, S. (2018). Morphology and histology of reproductive organ and first screening of Wolbachia in the ovary of Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Dryophthoridae). Serangga, 23(2), 183-193. doi: 10.13140/RG.2.2.22070.34882.
Wigglesworth, V. B. (1950). Reproductive system, The Principles of Insect Physiology. Methuen, (4), 459-494.
Yel, M. & Eren, E. (2000). Pieris rapae L. Lepidoptera: Pieridae nin Dişi Üreme Sisteminin Anatomik-Histolojik Yapısı. Türk Hijyen ve Deneysel Biyoloji Dergisi, 57(1), 25-34.
Żelazowska, M. (2005). Structure of the ovary and the differentiation of follicular epithelium in the pig louse, Haematopinus suis (Insecta: Phthiraptera). Folia biologica (Kraków), 53 (1-2), 51-60. https://doi.org/10.3409/1734916054663456.
Zhang, Z., Men, L., Peng, Y., Li, J., Deng, A., Chen, Y., Liu, X., & Ma, R. (2017). Morphological differences of the reproductive system could be used to predict the optimum Grapholita molesta (Busck) control period. Scientific Reports, 7(1), 8198. https://doi: 10.1038/s41598-017-08549-y
Beutel, R. G., & Leschen, R. A. B. (2005). Handbook of Zoology, Volume IV: Arthropoda: Insecta, Part 38: Coleoptera, Beetles. Volume 1: Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim), Walter de Gruyer, Berlin and New York, 288-296.
Beutel, R. G., Ribera, I., Fikácek, M., Vasilikopoulos, A., Misof, B., & Balke, M. (2020). The morphological evolution of the Adephaga (Coleoptera). Systematic Entomology, 45, 378-395. https://doi.org/10.1111/syen.12403.
Bonhag, P. F. (1958). Ovarian structure and vitellogenesis in insects, Annual Review of Entomology (3), 137-160. https://doi.org/10.1146/annurev.en.03.010158.001033.
Büning, J. (1994). The Insect Ovary. Ultrastructure, previtellogenic growth and evolution. Chapman & Hall, London, 410 pp.
Camargo Mathias, M. I., Sánchez, P., Denardi, S. E., & Caetano, F. H. (2011). Rhyncophorus palmarum L.(Linnaeus, 1758): A morphological and histological study of the female reproductive system. Microscopy Research and Technique, 74(9), 853-862. https://doi:10.1002/jemt.20969.
Chapman, R. (2004). The reproductive system, The insects structure and function (4b.). Cambridge: Cambridge University Press, Cambridge, 4th ed., 319-377.
Cheetham. T. (1992). Anatomy and histology of tissues associated with egg deposition in Chrysomela scripta Fabr. (Coleoptera: Chrysomelidae). Journal of the Kansas Entomological Society, 65(2), 101-114. https://www.jstor.org/stable/25085340.
Church, S. H., de Medeiros, B. A. S., Donoughe, S., Marquez Reyes, N. L., & Extavour, C. G. (2021). Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution. Proceedings of the Royal Society B: Biological Sciences, 288(1950). https://doi.org/10.1098/rspb.2021.0150.
Crowson, R. A. (1960). The phylogeny of Coleoptera. Annual Review of Entomology, 5, 111-134. https://doi.org/10.1146/annurev.en.05.010160.000551.
Devasahayam, S., Vidyasagar, P. S .P. V., & Koya, K. M. (1998). Reproductive system of pollu beetle, Longitarsus nigripennis Motschulsky (Coleoptera: Chrysomelidae), a major pest of black pepper, Piper nigrum Linnaeus. Journal of the Entomological Research Society, 22(1), 77-82
Duran, D .P., & Gough, H. M. (2020). Validation of tiger beetles as distinct family (Coleoptera: Cicindelidae), review and reclassification of tribal relationships. Systematic Entomology, 45, 723-729. https://doi.org/10.1111/syen.12440.
El Naggar, S. E., Mohamed, H. F., & Mahmoud, E. A. (2010). Studies on the morphology and histology of the ovary of red palm weevil female irradiated with gamma rays. Journal of Asia-Pacific Entomology, 13(1), 9-16. https://doi.org/10.1016/j.aspen.2009.08.004.
Escherich, K. (1942). Leben und Forschen. Anzeiger für Schädlingskunde, 18(10), 109-111.
Gao, J., Wang, J., & Chen, H. (2021). Ovary Structure and Oogenesis of Trypophloeus klimeschi (Coleoptera: Curculionidae: Scolytinae). Insects, 12(12), 1099. doi: 10.3390/insects12121099.
Gomez, R. A., Mercati, D., Lupetti, P., Fanciulli, P. P., & Dallai, R. (2023). Morphology of male and female reproductive systems in the ground beetle Apotomus and the peculiar sperm ultrastructure of A. rufus (P. Rossi, 1790) (Coleoptera, Carabidae). Arthropod Structure & Development, 72, 101217. doi: 10.1016/j.asd.2022.101217.
Gullan, P. J., & Cranston, P. S. (2010). The Insects: an Outline of Entomology, WileyBlackwell Publication; Böcekler: Entomolojinin Ana Hatları. Çeviri Editörü; Ali Gök, 4. basımdan çeviri, Nobel Akademik Yayıncılık, 580pp.
Hurka, K. (1996). Carabidae of the Czech and Slovak Republics Print Centrum. Kabourek Yayınları, 565pp.
Jaglarz, M. K. (1998). The number that counts. Phylogenetic implications of the number of nurse cells in ovarian follicles. Folia Histochemica et Cytobiologica, 36,167-178.
Klowden, M. J. (2007). The Reproductive System, Physiological Systems in Insects, (2nd ed). U.S.A: Academic Press, 181-223.
Korman, A. K., & Oseto, C. Y. (1989). Structure of the female reproductive system and maturation of oöcytes in Smicronyx fulvus (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 82(1), 94-100. https://doi.org/10.1093/aesa/82.1.94.
Lee, W. Y., Tseung, C. K., & Chang, T. H. (1985). An ultrastructural study on the ovariole, development in the oriental fruit fly. Bulletin of the Institute of Zoology, Academia Sinica, 24,1-10.
Lodos, N. (1989). Türkiye Entomolojisi IV. Ege Üniversitesi Ziraat Fakültesi Ofset Basımevi, Bornova-İzmir, 250pp.
Lodos, N. (1995). Silphidae, Türkiye Entomolojisi IV (Kısım I). Ege Üniversitesi Yayınları No: 493. İzmir, 68-76.
Lövei, G. L. and Sunderland, K. D. (1996). Ecology and behavior of Ground Beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41, 231-256. https://doi.org/10.1146/annurev.en.41.010196.001311.
Ma, N., & Hua, B. (2010). Structure of ovarioles and oogenesis in Panorpa liui Hua (Mecoptera: Panorpidae). Acta Entomologica Sinica, 53(11), 1220-1226.
Maffei, E. M. D., Fragoso, D. D. B., Pompolo, S. D. G., & Serrão, J. E. (2001). Morphological and cytogenetical studies on the female and male reproductive organs of Eriopis connexa Mulsant (Coleoptera, Polyphaga, Coccinellidae). Netherlands Journal of Zoology, 51(4), 483-496. doi:10.1163/156854201X00224.
Özyurt Koçakoğlu, N., Candan, S., & Arslan, H. (2023). Notes on the female reproductive system of the red and black froghopper, Cercopis vulnerata Rossi, 1807 (Hemiptera: Cercopidae) light and electron microscopy studies. Acta Zoologica. https://doi.org/10.1111/azo.12465.
Özyurt Koçakoğlu, N., Candan, S., & Güllü, M. (2021). Morphology of the reproductive tract of females of leaf beetle Chrysomela populi (Chrysomelidae: Coleoptera). Biologia, 76(11), 3257-3265. Doi: 10.1007/s11756-021-00796-9.
Özyurt Koçakoğlu, N., Candan, S., & Güllü, M. (2022). Structural and ultrastructural characters of the reproductive tract in females of the mint leaf beetle Chrysolina herbacea (Duftschmid 1825)(Coleoptera: Chrysomelidae). Acta Zoologica, 103(3), 365-375. https://doi.org/10.1111/azo.12379.
Parks, J. J., & Larsen, J. R. (1965). A morphological study of the female reproductive system and follicular development in the mosquito Aedes aegypti (L.). Transactions of the American Microscopical Society, 84(1), 88-98. https://www.jstor.org/stable/3224545.
Salazar, K., Boucher, S., & Serrão, J. E. (2017). Structure and ultrastructure of the ovary in the South American Veturius sinuatus (Eschscholtz)(Coleoptera, Passalidae). Arthropod Structure & Development, 46(4), 613-626.
doi: 10.1016/j.asd.2017.03.007.
Serttaş, A., & Çetin, H. (2014). Biyolojik Mücadelede Kullanılan Calosoma sycophanta L.'nın Laboratuvarlardaki Üretim Miktarının Arttırılması. II. Ulusal Akdeniz Orman Ve Çevre Sempozyumu “Akdeniz ormanlarının geleceği: Sürdürülebilir toplum ve çevre” 22-24 Ekim 2014, Isparta, Türkiye. 444-448.
Shirai, Y., Takahashi, M., Ote, M., Kanuka, H., & Daimon, T. (2023). DIPA-CRISPR gene editing in the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). Applied Entomology and Zoology, 58(3), 273-278. https://doi.org/10.1101/2023.04.07.535996.
Stein, F. (1847). Vergleichende Anatomie und Physiologie der Insekten, 1. Die weiblichen Geschlechtsorgane der Käfer. Berlin: Duncker ve Humblot. 139 pp.
Stys, P., Bilinski, S., (1990). Ovarioles types and the phylogeny of Hexapods. Biological Reviews, 65, 401-429. https://doi.org/10.1111/j.1469-185X.1990.tb01232.x.
Szklarzewicz, T., Michalik, A., Kalandyk‐Kołodziejczyk, M., Kobiałka, M., & Simon, E. (2014). Ovary of Matsucoccus pini (Insecta, Hemiptera, Coccinea: Matsucoccidae): morphology, ultrastructure, and phylogenetic implications. Microscopy Research and Technique, 77(5), 327-334. doi: 10.1002/jemt.22347.
Vommaro, M. L., Donato, S., & Giglio, A. (2022). Virtual sections and 3D reconstructions of female reproductive system in a carabid beetle using synchrotron X - ray phase - contrast microtomography. Zoologischer Anzeiger, 298, 123-130. https://doi.org/10.1016/j.jcz.2022.04.001.
Wan, N. A., Nurul, W., Yaakop, S., & Norefrina, S. (2018). Morphology and histology of reproductive organ and first screening of Wolbachia in the ovary of Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Dryophthoridae). Serangga, 23(2), 183-193. doi: 10.13140/RG.2.2.22070.34882.
Wigglesworth, V. B. (1950). Reproductive system, The Principles of Insect Physiology. Methuen, (4), 459-494.
Yel, M. & Eren, E. (2000). Pieris rapae L. Lepidoptera: Pieridae nin Dişi Üreme Sisteminin Anatomik-Histolojik Yapısı. Türk Hijyen ve Deneysel Biyoloji Dergisi, 57(1), 25-34.
Żelazowska, M. (2005). Structure of the ovary and the differentiation of follicular epithelium in the pig louse, Haematopinus suis (Insecta: Phthiraptera). Folia biologica (Kraków), 53 (1-2), 51-60. https://doi.org/10.3409/1734916054663456.
Zhang, Z., Men, L., Peng, Y., Li, J., Deng, A., Chen, Y., Liu, X., & Ma, R. (2017). Morphological differences of the reproductive system could be used to predict the optimum Grapholita molesta (Busck) control period. Scientific Reports, 7(1), 8198. https://doi: 10.1038/s41598-017-08549-y