Abstract
Lake Van is the largest lake in Turkey. It is one of the few soda lakes in the world. Its water is brackish and soda. The lake water has a salinity rate of 19‰ and a pH of 9.8. The salty-soda content of the lake greatly limits biodiversity. Since the Lake Van fish is anadromous, it migrates from the extreme conditions of Lake Van to the freshwater pouring into the lake to spawn. In the same way, once they have emerged from the eggs, the newly hatched fish return to the lake environment to feed again. In this study, the changes in Lake Van fish gill mucus cell histochemistry were examined using different histological stains. The area and density of the mucus cells were observed to have changed in the aquatic areas of different physicochemical properties due to reproductive migration. The intensity of the mucus staining was also found to vary in different aquatic locations and gill regions. As a result, it was clearly demonstrated that mucus cell glycoprotein contents and levels found in Lake Van fish gills varied in different lake freshwater and aquatic environments. In addition, it was determined that the area and density of the mucus cells varied during reproductive migration. It is thought that the change in mucus cells was caused by salinity, pH, and bacterial and parasitic infections encountered in different aquatic environments. These changes in the gill mucus cells play an important role in the aquatic adaptation of fish.
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References
Boat TF, Cheng PW (1980) Biochemistry of airway mucus secretions. Fed Proc 39(13):3067–3074
Cinar K, Aksoy A, Emre Y, Aşti RN (2009) The histology and histochemical aspects of gills of the flower fish, Pseudophoxinus antalyae. Vet Res Comm 33(5):453–460
Culling CF, Reid PE (1979) The histochemistry of colonic mucins. J Histochem Cytochem 27:1177–1179
Danulat E, Kempe S (1992) Nitrogeneus waste excretion and accumulation of urea and ammonia in Chalcalburnus tarichi (Cyprinidae) endemic to Lake Van (eastern Turkey). Fish Physiol Biochem 9:377–386
Danulat E, Selçuk B (1992) Life history and environmental conditions of the anadromous Chalcalburnus tarichi (Cyprinidae) in the highly alkaline Lake Van, eastern Anatolia, Turkey. Arch Hydrobiol 126(1):105–125
Dekker J, Rossen J, Büller H, Einerhand A (2002) The MUC family: an obituary. Trends Biochem Sci 27(3):126–131
Dezfuli BS, Giari L, Konecny R, Jaeger P, Manera M (2003) Immunohistochemistry, ultrastructure and pathology of gills of Abramis brama from Lake Mondsee, Austria, infected with Ergasilus sieboldi (Copepoda). Dis Aquat Org 53(3):257–262
Díaz AO, García AM, Escalante AH, Goldemberg AL (2010) Glycoproteins histochemistry of the gills of Odontesthes bonariensis (Teleostei, Atherinopsidae). J Fish Biol 77(7):1665–1673
Domeneghini C, Pannelli SR, Veggetti A (1998) Gut glycoconjugates in Sparus aurata L. (Pisces, Teleostei). A comparative histochemical study in larval and adult ages. Histol Histopathol 13(2):359–372
Esteban MA (2012) An overview of the immunological defenses in fish skin. ISRN Immunol 853470:1–29
Ferguson HW, Morrison D, Ostland VE, Lumsden J, Byrne P (1992) Responses of mucus-producing cells in gill disease of rainbow trout (Oncorhynchus mykiss). J Comp Pathol 106(3):255–265
Fletcher TC (1978) Defense mechanism in fish. J Histochem Cytochem 32:681–689
Genten F, Terwinghe E, Danguy A (2009) Atlas of fish histology. CRC Press, USA. https://doi.org/10.1201/9780367803599
Hellio C, Pons AM, Beaupoil C, Bourgougnon N, Le Gal Y (2002) Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. Int J Antimicrob Agents 20(3):214–219
Hibiya T, Yokote M, Oguri M, Sato H, Takashima F, Aida K (1997) An atlas of fish histology: normal and pathological features. Gustav Fischer Verlo, New York, p 145
Kabata Z (1982) Copepoda (Crustacea) parasitic on fishes: problems and perspectives. Adv Parasitol 19:1–71
Lai SK, Wang YY, Wirtz D, Hanes J (2009) Micro- and macrorheology of mucus. Adv Drug Deliv Rev 61:86–100
Lease HM, Hansen JA, Bergman HL, Meyer JS (2003) Structural changes in gills of Lost River suckers exposed to elevated pH and ammonia concentrations. Comp Biochem Physiol C: Toxicol Pharmacol 134(4):491–500
Laurent P (1984) Gill internal morphology. In Fish Physiol 10:73–183 Academic Press
Mir IH, Channa A (2009) Gills of the snow trout, Schizothorax curvifrons Heckel: a SEM study. Pak J Biol Sci 12(23):1511–1515
Mittal AK, Ueda T, Fujimori O, Yamada K (1994) Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton). Histochem J 26:666–677
Moron SE, Andrade CAD, Fernandes MN (2009) Response of mucous cells of the gills of traíra (Hoplias malabaricus) and jeju (Hoplerythrinus unitaeniatus) (Teleostei: Erythrinidae) to hypo-and hyper-osmotic ion stress. Neotrop Ichthyol 7(3):491–498
Nagashima Y, Sendo A, Shimakura K, Shiomi K, Kobayashi T, Kimura B, Fujii T (2001) Antibacterial factors in skin mucus of rabbitfishes. J Fish Biol 58(6):1761–1765
Oğuz AR (2013) Environmental regulation of mitochondria-rich cells in Chalcalburnus tarichi (Pallas, 1811) during reproductive migration. J Membr Biol 246(3):183–188
Oğuz AR (2015) Histological changes in the gill epithelium of endemic Lake Van fish (Chalcalburnus tarichi) during migration from alkaline water to freshwater. North-West J Zool 11(1):51–57
Oğuz AR (2018) Development of osmoregulatory tissues in the Lake Van fish (Alburnus tarichi) during larval development. Fish Physiol Biochem 44(1):227–233
Powell MD, Parsons HJ, Nowak BF (2001) Physiological effects of freshwater bathing of Atlantic salmon (Salmo salar) as a treatment for amoebic gill disease. Aquacult 199(3–4):259–266
Reverter M, Tapissier-Bontemps N, Lecchini D, Banaigs B, Sasal P (2018) Biological and ecological roles of external fish mucus: a review. Fishes 3(4):41
Roberts SD, Powell MD (2003) Comparative ionic flux and gill mucous cell histochemistry: effects of salinity and disease status in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol A: Mol Int Physiol 134(3):525–537
Shephard KL (1994) Functions for fish mucus. Rev Fish Biol Fish 4(4):401–429
Srivastava N, Kumari U, Rai AK, Mittal S, Mittal AK (2012) Histochemical analysis of glycoproteins in the gill epithelium of an Indian major carp, Cirrhinus mrigala. Acta Histochem 114(6):626–635
Tharton DJ, Davies JR, Krayanbrink M, Richardson PS, Sheehan JK, Carlstedt I (1990) Mucus glycoproteins from “normal” human tracheobranchial secretions. Biochem J 265:179–186
Uçar A, Atamanalp M (2008) Balıklarda toksikopatolojik lezyonlar II/toxicopathological lesions in fish II. Atatürk Üniv Ziraat Fak Derg 40(1):95–101
Wilson JM, Laurent P (2002) Fish gill morphology: inside out. J Exp Zool 293(3):192–213
Zayed AE, Mohamed SA (2004) Morphological study on the gills of two species of freshwater fishes: Oreochromis niloticus and Clarias gariepinus. Ann Anat 186:295–304
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This research was supported by the Van Yüzüncü Yıl University, Scientific Research Projects Department (FYL-2019-7879).
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Ahmet Regaib Oğuz conceived the study and designed the experiments. Zehra Alkan carried out the experiments, analyzed the data, and wrote the manuscript. Ahmet Regaib Oğuz wrote and revised the manuscript. All the authors read and approved the final manuscript.
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All of the animal experimental procedures were performed in accordance with the animal study protocols approved by the Animal Researchers Local Ethic Committee of Van Yüzüncü Yıl University (protocol no: 2019/5) and the Republic of Turkey Ministry of Agriculture and Forestry (24/04/2018–11,602).
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Alkan, Z., Oğuz, A.R. Investigation of gill mucus cells of Lake Van fish (Alburnus tarichi) during reproductive migration. Fish Physiol Biochem 47, 409–419 (2021). https://doi.org/10.1007/s10695-020-00921-6
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DOI: https://doi.org/10.1007/s10695-020-00921-6