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Gavruseva T. V., Sigacheva T. B., Chesnokova I. I. Pathomorphological and biochemical study of the golden grey mullet Chelon auratus (Risso, 1810) in the waters of the southwestern Crimea (the Black Sea). Marine Biological Journal, 2022, vol. 7, no. 1, pp. 14-33. https://doi.org/10.21072/mbj.2022.07.1.02

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Abstract

The golden grey mullet Chelon auratus (Risso, 1810) (Mugilidae) is a valuable commercial and recreational species ranking first in terms of catch volume of the Black Sea indigenous mullets. The importance of this species in the regional fishery among demersal fish requires the development of a system for assessing its health status. Such research is based on an integrated approach involving biochemical and pathomorphological methods: these allow to investigate the alterations in fish prior the occurrence of visible manifestations, disruption of the processes of growth and reproduction, reduction of commercial size, and decrease in abundance. The aim of our work was to study both pathomorphological alterations and several biochemical parameters of golden grey mullet tissues for assessing its health status. Fish visual examination and pathological autopsy were carried out. For histological analysis, samples of the gills, liver, kidneys, gastrointestinal tract, spleen, and pancreas were fixed in Davidson’s solution and processed by standard methods. Based on the histological studies, the fish health status was investigated by a modified semi-quantitative analysis of alterations according to the Bernet et al. protocol and by assessing the distribution of lesion in organs using a scoring system. We determined the importance factors of alterations for C. auratus, the values of organ alteration indices, and the total index of fish pathology. The biochemical studies permitted to reveal the level of protein oxidation, lipid and urea peroxidation, and the activity of aminotransferases and alkaline phosphatase in the liver; moreover, we quantified albumin and glucose concentration in the blood serum. In the organs of the golden grey mullet, the histopathological alterations referring to four types of the reaction patterns were detected (circulatory disorders, regressive and progressive alterations, and inflammatory processes). Furthermore, parasites representing several species of different systematic groups (Protozoa, Monogenea, Trematoda, and Nematoda) were identified. It was established that the most severe histopathological alterations were caused by a parasitic protozoan, presumably Ichthyophonus sp. When carrying out a semi-quantitative analysis of alterations, the mullets were conventionally divided into conditionally healthy individuals and infected ones. Pathomorphological data were obtained, and the set of biochemical parameters was compared in these two groups. Significant differences were revealed in the values of organ alteration indices in C. auratus in the kidneys, liver, gastrointestinal tract, and pancreas. The values of the total index of fish pathology also differed significantly. The biochemical studies revealed a significant increase in urea content in the liver of fish from the group 2, that may indicate the kidney and gill excretory dysfunction (it was confirmed histologically). No significant differences were found in the level of lipid peroxidation, protein oxidation, and activity of aminotransferases in the liver of conditionally healthy and infected fish. The results of our investigation confirm high informativeness of the studied parameters for assessing the health status of the golden grey mullet.

Authors

T. V. Gavruseva

senior researcher, PhD

https://orcid.org/0000-0002-9102-0861

https://www.elibrary.ru/author_profile.asp?id=292944

T. B. Sigacheva

senior researcher, PhD

https://orcid.org/0000-0003-3125-898X

https://elibrary.ru/author_items.asp?id=814387

I. I. Chesnokova

senior researcher, PhD

https://orcid.org/0000-0002-7883-0755

https://www.elibrary.ru/author_profile.asp?id=772853

References

Болтачёв А. Р., Карпова Е. П. Ихтиофауна прибрежной зоны Севастополя (Чёрное море) // Морской экологический журнал. 2012. Т. 11, № 2. С. 10–27. [Boltachev A. R., Karpova E. P. The ichthyofauna of the Sevastopol coastal zone (the Black Sea). Morskoj ekologicheskij zhurnal, 2012, vol. 11, no. 2, pp. 10–27. (in Russ.)]

Гаврюсева Т. В. Первый случай ихтиофоноза у молоди кижуча Oncorhynchus kisutch (Walbaum) в условиях аквакультуры на Камчатке // Биология моря. 2007. Т. 33, № 1. С. 49–53. [Gavryuseva T. V. The first report of Ichthyophonus hoferi infection in coco salmon Oncorhynchus kisutch juveniles at a fish hatchery in Kamchatka. Russian Journal of Marine Biology, 2007, vol. 33, no. 1, pp. 49–53. (in Russ.)]

Гаевская А. В. Паразиты и болезни морских и океанических рыб в природных и искусственных условиях. Севастополь : ЭКОСИ-Гидрофизика, 2004. 237 с. [Gaevskaya A. V. Parasites and Diseases of Marine and Oceanic Fishes in Natural and Culture Conditions. Sevastopol : EKOSI-Gidrofizika, 2004, 237 p. (in Russ.)]

Дмитриева Е. В., Гаевская А. В. Паразитологические аспекты марикультуры и интродукции кефалевых рыб в Азово-Черноморском бассейне // Экология моря. 2001. Вып. 55. С. 73–78. [Dmitrieva E. V., Gaevskaya A. V. Parasitological aspects of mugilids mariculture and of their introduction into the Sea of Azov and the Black Sea. Ekologiya morya, 2001, iss. 55, pp. 73–78. (in Russ.)]

Дмитриева Е. В., Герасев П. И. Моногенеи рода Ligophorus (Ancyrocephalidae) – паразиты черноморских кефалей (Mugilidae) // Паразитология. 1996. Т. 30, № 5. С. 440–449. [Dmitrieva E. V., Gerasev P. I. Monogeneans of the genus Ligophorus (Ancyrocephalidae) – parasites of the Black Sea mullets (Mugilidae). Parazitologiya, 1996, vol. 30, no. 5, pp. 440–449. (in Russ.)]

Дубинина Е. Е., Бурмистов С. О., Ходов Д. А., Поротов И. Г. Окислительная модификация белков сыворотки крови человека, метод её определения // Вопросы медицинской химии. 1995. Т. 41, вып. 1. С. 24–26. [Dubinina E. E., Burmistrov S. O., Khodov D. A., Porotov I. G. Okislitel’naya modifikatsiya belkov syvorotki krovi cheloveka, metod ee opredeleniya. Voprosy meditsinskoi khimii, 1995, vol. 41, iss. 1, pp. 24–26. (in Russ.)]

Завьялова Е. А., Дрошнев А. Е., Гулюкин М. И., Калинина Н. Р. Анестезия радужной форели // Российский ветеринарный журнал. Сельскохозяйственные животные. 2012. № 4. С. 22–24. [Zav’yalova E. A., Droshnev A. E., Gulyukin M. I., Kalinina N. R. Anesthesia of the rainbow trout. Rossiiskii veterinarnyi zhurnal. Sel’skokhozyaistvennye zhivotnye, 2012, no. 4, pp. 22–24. (in Russ.)]

Кожурин Е. А., Шляхов В. А., Губанов Е. П. Динамика уловов промысловых рыб Крыма в Чёрном море // Труды ВНИРО. 2018. Т. 171. С. 157–169. [Kozhurin E. A., Shlyakhov V. A., Gubanov E. P. Crimea commercial fish dynamics in the Black Sea. Trudy VNIRO, 2018, vol. 171, pp. 157–169. (in Russ.)]

Корниенко Г. Г., Дудкин С. И., Сергеева С. Г., Ружинская Л. П., Цема Н. И., Бугаев Л. А., Войкина А. В. Физиолого-биохимическая характеристика рыб Азово-Черноморского бассейна в условиях современной антропогенной нагрузки // Вестник Камчатского государственного технического университета. 2017. № 40. С. 58–66. [Kornienko G. G., Dudkin S. I., Sergeeva S. G., Ruzhinskaya L. P., Tsema N. I., Bugaev L. A., Voykina A. V. Physiological and biochemical characteristics of the Azov and Black Sea fishes undergoing anthropogenic pressure. Bulletin of Kamchatka State Technical University, 2018, no. 40, pp. 58–66. (in Russ.)]

Лукина Ю. Н. Проблемы здоровья рыб в водных экосистемах Европейско-Сибирской области Палеарктики : автореф. дис. … д-ра биол. наук : 03.02.08, 03.02.06. Петрозаводск, 2014. 37 с. [Lukina Yu. N. Problemy zdorov’ya ryb v vodnykh ekosistemakh Evropeisko-Sibirskoi oblasti Palearktiki : avtoref. dis. … d-ra biol. nauk : 03.02.08, 03.02.06. Petrozavodsk, 2014, 37 p. (in Russ.)]

Моисеенко Т. И., Гашев С. Н., Селюков А. Г., Жигилева О. Н., Алешина О. А. Биологические методы оценки качества вод: часть 1. Биоиндикация // Вестник Тюменского государственного университета. 2010. № 7. С. 20‒40. [Moiseenko T. I., Gashev S. N., Selyukov A. G., Zhigileva O. N., Aleshina O. A. Biologicheskie metody otsenki kachestva vod: chast’ 1. Bioindikatsiya. Vestnik Tyumenskogo gosudarstvennogo universiteta, 2010, no. 7, pp. 20‒40. (in Russ.)]

Пронькина Н. В., Белофастова И. П. Новые данные о нематодах черноморского сингиля Liza aurata (Pisces: Mugilidae) // Экология моря. 2005. Вып. 68. С. 77–82. [Pronkina N. V., Belofastova I. P. New date about nematodes of the Black Sea golden grey mullet Liza aurata (Pisces: Mugilidae). Ekologiya morya, 2005, iss. 68, pp. 77–82. (in Russ.)]

Стальная И. Д., Гаришвили Т. Г. Метод определения малонового диальдегида с помощью тиобарбитуровой кислоты // Современные методы в биохимии. Москва : Медицина, 1977. С. 66–68. [Stal’naya I. D., Garishvili T. G. Metod opredeleniya malonovogo dial’degida s pomoshch’yu tiobarbiturovoi kisloty. In: Sovremennye metody v biokhimii. Moscow : Meditsina, 1977, pp. 66–68. (in Russ.)]

Юрахно В. М. Болезни черноморских и азовских рыб, вызываемые миксоспоридиями (Myxozoa: Myxosporea) // Экология моря. 2009. Вып. 77. С. 33–37. [Yurakhno V. M. The Black Sea and the Sea of Azov fish diseases induced by myxosporeans (Myxozoa: Myxosporea). Ekologiya morya, 2009, iss. 77, pp. 33–37. (in Russ.)]

Au D. W. T. The application of histo-cytopathological biomarkers in marine pollution monitoring: A review. Marine Pollution Bulletin, 2004, vol. 48, iss. 9–10, pp. 817–834. https://doi.org/10.1016/j.marpolbul.2004.02.032

Banaee M., Sureda A., Mirvaghefi A. R., Ahmadi K. Effects of diazinon on biochemical parameters of blood in rainbow trout (Oncorhynchus mykiss). Pesticide Biochemistry and Physiology, 2012, vol. 99, iss. 1, pp. 1–6. http://dx.doi.org/10.1016/j.pestbp.2010.09.001

Banaee M., Sureda A., Zohiery F., Nematdoust Hagi B., Garanzini D. S. Alterations in biochemical parameters of the freshwater fish, Alburnus mossulensis, exposed to sub-lethal concentrations of fenpropathrin. International Journal of Aquatic Biology, 2014, vol. 2, no. 2, pp. 58–68. https://doi.org/10.22034/IJAB.V2I2.32

Bancroft D., Stevens A., Turner D. R. Theory and Practice of Histological Techniques. Edinburgh ; London ; Melbourne ; New York : Churchill Livingstone Inc., 1990, 725 p.

Bernet D., Schmidt H., Meier W., Burkhard-Holm P., Wahli T. Histopathology in fish: Proposal for protocol to assess aquatic pollution. Journal of Fish Diseases, 1999, vol. 22, iss. 1, pp. 25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x

Bruno D. W., Novak B., Elliott D. G. Guide to the identification of fish protozoan and metazoan parasites in stained tissue sections. Diseases of Aquatic Organisms, 2006, vol. 70, no. 1–2, pp. 1–36. https://doi.org/10.3354/dao070001

Costa P. M., Diniz M. S., Caeiro S., Lobo J., Martins M., Ferreira A. M., Caetano M., Vale C., DelValls T. Á., Costa M. H. Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: A weighted indices approach. Aquatic Toxicology, 2009, vol. 92, iss. 3, pp. 202–212. https://doi.org/10.1016/j.aquatox.2008.12.009

Frasca S. Jr., Wolf J. C., Kinsel M. J., Camus A. C., Lombardini E. D. 39. Osteichthyes (freshwater & marine). In: Pathology of Wildlife and Zoo Animals / K. A. Terio, D. McAloose, J. St. Leger (Eds). London ; San Diego ; Cambridge ; Oxford : Academic Press : Elsevier Inc., 2018, pp. 953–1001. https://doi.org/10.1016/C2015-0-01586-6

Feist S. W., Stentiford G. D., Kent M. L., Santos A. R., Lorance P. Histopathological assessment of liver and gonad pathology in continental slope fish from the northeast Atlantic Ocean. Marine Environmental Research, 2015, vol. 106, pp. 42–50. https://doi.org/10.1016/j.marenvres.2015.02.004

Floyd-Rump T. P., Horstmann-Dehn L. A., Atkinson S., Skaugstad C. Effect of Ichthyophonus on blood plasma chemistry spawning Chinook salmon and their resulting offspring in a Yukon River tributary. Diseases of Aquatic Organisms, 2017, vol. 122, no. 3, pp. 223–236. https://doi.org/10.3354/dao03077

ICES. Report of the Working Group on Pathology and Diseases of Marine Organisms (WGPDMO), 24–28 February, 2015, Helsinki, Finland, 2015. Copenhagen : ICES, 2015, 124 p. (ICES CM 2015/SSGEPI:01). https://doi.org/10.17895/ices.pub.8495

Kavitha C., Malarvizhi A., Senthil Kumaran S., Ramesh M. Toxicological effects of arsenate exposure on hematological, biochemical and liver transaminases activity in an Indian major carp, Catla catla. Food and Chemical Toxicology, 2010, vol. 48, iss. 10, pp. 2848–2854. http://dx.doi.org/10.1016/j.fct.2010.07.017

Kole D., Pal S., Mukherjee A. K., Samanta P., Ghosh A. R. Effects of chromium on tissue-specific biochemical parameters in freshwater catfish, Anabas testudineus (Bloch). In: HydroMedit 2014 : 1st International Congress of Applied Ichthyology & Aquatic Environment, 13–15 Nov., Volos, Greece : [proceedings]. [Nea-Ionia], 2014, pp. 168–174.

Kundu I., Bandyopadhyay P. K., Mandal D. R., Gürelli G. Study of pathophysiological effects of the nematode parasite Eustrongylides sp. on freshwater fish Channa punctatus by hematology, serum biochemical, and histological studies. Türkiye Parazitoloji Derneği, 2016, vol. 40, iss. 1, pp. 42–47. https://doi.org/10.5152/tpd.2016.4551

Kurhalyuk N., Tkachenko H. Induction of oxidative stress and antioxidant defenses in the livers of sea trout, Salmo trutta L., with ulcerative dermal necrosis. Archives of Polish Fisheries, 2011, vol. 19, fasc. 4, pp. 229–240.

Marcogliese D. J., Brambilla L. G., Gagne F., Gendron A. D. Joint effects of parasitism and pollution on oxidative stress biomarkers in yellow perch Perca flavescens. Diseases of Aquatic Organisms, 2005, vol. 63, pp. 77–84. https://doi.org/10.3354/dao063077

Nnabuchi U. O., Ejikeme O. G., Didiugwu N. C., Ncha O. S., Onahs S. P., Amarachi A. C. Effect of parasites on the biochemical and haematological indices of some clariid (Siluriformes) catfishes from Anambra River, Nigeria. International Journal of Fisheries and Aquatic Studies, 2015, vol. 3, iss. 2, pt. E, pp. 331–336.

Noga E. J. Fish Disease: Diagnosis and Treatment. 2nd edition. Ames, Iowa : Wiley-Blackwell, 2010, 519 p.

Noor El-Deen A. E., Mona M. Ismaiel, Mohamed A. E., Omima A. A. El-Ghany. Comparative studies on the impact of humic acid and formalin on ectoparasitic infestation in Nile tilapia Oreochromis niloticus. Nature and Science, 2010, vol. 8, no. 2, pp. 121–125. https://doi.org/10.7537/marsnsj080210.16

Osman H. A. M., Fadel N. G., Ali A. T. Biochemical and histopathological alterations in catfish, Clarias gariepinus, infected with trypanosomiasis with special reference to immunization. Egyptian Journal of Comparative Pathology and Clinical Pathology, 2009, vol. 22, no. 3, pp. 164–181.

Osman H. A. M., El-Refaey A. M. E., Rahman A., Al-Zahrani Q., Hazzaa M. S. Field studies on ichthyophonasis (ichthyosporidiosis) infecting Red Sea cultured grouper, taradi, Plectropomus areolatus in Jeddah, Saudi Arabia with a special trial for treatment using Moringa oleifera. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 2015, vol. 6, no. 4, pp. 2207–2217.

Ovcharenko M. O. Microparasites of worldwide mullets. Annals of Parasitology, 2015, vol. 61, no. 4, pp. 229–239. https://doi.org/10.17420/ap6104.12

Saleh Y. S., Marie M.-A. S. Use of Arius thalassinus fish in a pollution biomonitoring study, applying combined oxidative stress, hematology, biochemical and histopathological biomarkers: A baseline field study. Marine Pollution Bulletin, 2016, vol. 106, iss. 1–2, pp. 308–322. https://doi.org/10.1016/j.marpolbul.2016.03.030

Santos D. M. S., Melo M. R. S., Mendes D. C. S., Rocha I. K. B. S., Silva J. P. L., Cantanhêde S. M., Meletti P. C. Histological changes in gills of two fish species as indicators of water quality in Jansen Lagoon (São Luís, Maranhão State, Brazil). International Journal of Environmental Research and Public Health, 2014, vol. 11, no. 12, pp. 12927–12937. https://doi.org/10.3390/ijerph111212927

Saraiva A., Costa J., Serrão J., Cruz C., Eiras J. C. A histology-based fish health assessment of farmed seabass (Dicentrarchus labrax L.). Aquaculture, 2015, vol. 448, pp. 375–381. https://doi.org/10.1016/j.aquaculture.2015.06.028

Stentiford G. D., Bignell J. P., Lyons B. P., Feist S. W. Site-specific disease profiles in fish and their use in environmental monitoring. Marine Ecology Progress Series, 2009, vol. 381, pp. 1–15. https://doi.org/10.3354/meps07947

Öztürk T. Parasites of juvenile golden grey mullet Liza aurata Risso, 1810 in Sarıkum Lagoon Lake at Sinop, Turkey. Acta Parasitologica, 2013, vol. 58, iss. 4, pp. 531–540. https://doi.org/10.2478/s11686-013-0173-3

Yurakhno V. M., Ovcharenko M. O. Study of Myxosporea (Myxozoa), infecting worldwide mullets with description of a new species. Parasitological Research, 2014, vol. 113, pp. 3661–3674. https://doi.org/10.1007/s00436-014-4031-5

Funding

This work was carried out within the framework of the IBSS state research assignments “Regularities of formation and anthropogenic transformation of biodiversity and biological resources of the Sea of Azov – Black Sea basin and other areas of the World Ocean” (No. 121030100028-0) and “Functional, metabolic, and toxicological aspects of hydrobionts and their populations existence in biotopes with different physical and chemical regimes” (No. 121041400077-1).

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