Comparative aspects of kidney morphology of fish
Abstract
In fish kidneys not only allow the excretion of waste but also are essential for osmoregulation and hemopoiesis. Microscopic observation differentiates two zones in the kidneys, a cranial part where there is a greater proportion of haemolymphopoietic and endocrine tissue, and other caudal whose morphology is related to the elimination of metabolic wastes and control of osmotic balance. Embryologically, the cranial portion derives from pronephros and caudal portion from mesonephros. The latter, in adult animals is called opistonefric and is formed by the excretory tissue (nephrons and collecting ducts) and lymphoid interstitial tissue. The degree of development of the nephrons differs between different groups, but in general, they are composed of the renal corpuscle and renal tubule or urine tubule, the latter can be divided into several segments. The renal tubules are reunited at collecting tubules. The main objective of this review is to describe renal morphology and its relation to environmental requirements.
Keywords: nephrons, fish, marine environments, freshwater environments.
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References
Agius C. (1980) Phylogenetic development of melano-macrophage centres in fish. J Zool; 191: 11-31.
Agius C, Roberts RJ. (1981) Effects of starvation on the melanomacrophage centers of fish. J Fish Biol; 19: 161-169.
Agius C, Roberts RJ. (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis; 26: 499-509.
Ahmad MF, Alim A, Sen NS, Lakra G, Mishra KP, Raza B, Chakarborty B, Rao NVA, Bonga SEW. (2002) Electron microscopic studies of the corpuscles of Stannius of an airbreathing teleost (Heteropneustes fossilis). J Biosci; 27(5): 509-513.
Ahmad MF, Prasad DK, Rao NVA. (2010) Ultrastructure of the corpuscles of the Stannius of an airbreathing catfish Clarias batrachus Linn. Proc. Natl. Acad. Sci. India Section B Biol Sci; 80: 230-234.
Aida K, Nishioka RS, Bern HA. (1980) Degranulation of the Stannius corpuscles of Coho salmon (Onchorhynchus kisutch) in response to ionic changes in vitro. Gen Comp Endocrinol; 41: 305-313.
Bhattacharyya TK, Butler DG. (1978) Fine structure of the corpuscles of Stannius in the toadfish. J Morphol; 155(3): 271-285.
Bone Q, Moore RH. (2008) Chapter 6. Osmoregulation and ion balance. En: Biology of fishes. 3er. Ed. Abingdon, UK. Taylor & Francis Group. Pp. 161-187.
Bucher F, Hofer R. (1993) Histological and enzyme histochemical changes in the kidney of male bullhead (Cottus gobio) during the spawning period. J Fish Biol; 42: 403-409.
Butler DG, Zhang DH. (2001) Corpuscles of Stannius secrte rennin and isorenin that regulates cardiovascular function in freshwater North American eels, Anguilla rostrata LeSueur. Gen Com Endocrinol; 124: 199-217.
Cousseau MB. (2010) Capítulo 5. Los peces óseos (Clases Actinopterygii y Sarcopterygii). En: Ictiología. Aspectos fundamentales. La vida de los peces sudamericanos. 1r. Ed. EUDEM, Argentina. Pp. 239-461.
Díaz AO, Devicenti CV, Ricci L, Goldemberg AL. (1996) Comparative histology and histochemistry of hake (Merluccius hubbsi) and white croaker (Micropogonias furnieri) kidney. J Anim Morphol Physiol; 43(1): 59-63.
Díaz AO, Goldemberg AL. (2004) Capítulo 6. Sistema excretor en peces. En: Temas de Histología y Embriología Animal. Parte 3. Analía Nessi y col. Ed. Inarbite (Buenos Aires). 2° edición. Pp. 85-92.
Domitrovic HA. (2000) Histología e histopatología del riñón de Cichlasoma dimerus (Pisces, Cichlidae). Universidad Nacional Del Nordeste. Comunicaciones Científicas y Tecnológicas 2000.
Ellis AE, Roberts RJ, Tytler P. (1989) The anatomy and physiology of teleosts. En: Fish Pathology, 2nd. Ed., R.J. Roberts ed., Bailliere Tindall (London). Pp. 13-55.
Ericsson JLE, Olsen S. (1970) On the fine structure of the aglomerular renal tubule in Lophius piscatorius. Z Zellforsch; 104: 240-258.
Gheng CC, Chen L, Near TJ, Jin Y. (2003) Functional antifreeze glycoprotein genes in temperate-water New Zealand nototheniid fish infer an Antarctic evolutionary origin. Mol Biol Evol; 20(11): 1897-1908.
González G, Crespo S, Brusle J. (1993) Histo-cytological study of the liver of the cabrilla sea bass, Serranus cabrilla (Teleostei, Serranidae), an available model for marine fish experimental studies. J Fish Biol; 43: 363-73.
Grizzle JM, Rogers WA. (1976) Excretory system. En: Anatomy and histology of the channel catfish. Auburn Pinting Inc., Auburn University, Agr. Exptl. Station. pp. 35-39.
Herraez MP, Zapata AG. (1991) Structural characterization of the melanomacrophage centres (MMC) of goldfish Carassius auratus. Eur J Morphol; 29(2): 89-102.
Hill RW, Wise GA, Anderson M. (2006) Capítulo 26. Fisiología hidrosalina: de los animales en sus hábitats. En: Fisiología Animal. Editorial Médica Panamericana S.A. Pp. 811-855.
Jarial MS, Wilkins JH. (2010) Structure of the kidney in the coelacanth Latimeria chalumnae with reference to osmoregulation. J Fish Biol; 76: 655-668.
Jiménez A, Esteban FJ, Sánchez-López AM, Pedrosa JA, Del Moral ML, Hernández R, Blanco S, Barroso JB, Rodrigo J, Peinado MA. (2001) Immunohistochemical localisation of neuronal nitric oxide synthase in the rainbow trout kidney. J Chem Neuroanatomy; 21: 289-294.
Kaneko T, Hirano T. (1993) Role of prolactin and somatolactin in calcium regulation in fish. J Exp Biol; 184: 31-45.
Kardong KV. (2007) Capítulo 14. El sistema urogenital. En: Vertebrados. Anatomía comparada, función y evolución. 4ta. Ed. McGraw Hill Interamericana. Pp. 538-584.
Krishnamurthy VG, Bern HA. (1969) Correlative histological study of the corpuscles of Stannius and juxtaglomerular cells of teleost fishes. Gen Comp Endocrinol; 13: 313-335.
Lagler KF, Bardach JE, Miller RR, May Passino DR. (1984) Capítulo 9. Excreción y regulación osmótica. En: Ictiología. AGT Ed., S. A. México. Pp. 247-262.
Macchi GJ, Romano LA, Christiansen HE. (1992) Melano macrophage centres in whitemouth croacker Micropogonias furneri, as biological indicators of environmental changes. J Fish Biol; 40: 971-973.
Meats M, Ingleton PM, Chestor Jones I, Garland HC, Kenyon CJ. (1978) Fine structure of the corpuscles of Stannius of the trout, Salmo gairdneri: Structural changes in response to increased environmental salinity and calcium ions. Gen Comp Endocrinol; 36: 451-461.
Norris DO. (2007) Bioregulation of calcium and phosphate homeostasis: Calcium and phosphate homeostasis in non-mammalian vertebrates. En: Vertebrate Endocrinology, fourth edition, Elsevier Academic Press, USA, pp. 501-510.
Ojeda JL, Icardo JM, Domezain A. (2003) Renal corpuscle of the sturgeon kidney: an ultrastructural, chemical dissection, and lectin-binding study. Anat Rec A; 272A: 563-573.
Ojeda JL, Icardo JM, Wong WP, Ip YK. (2006) Microanatomy and ultrastructure of the kidney of the African lungfish Protopterus dolloi. Anat Rec A; 288A: 609-625.
Ozaka C, Yamamoto N, Somiya H. (2009) The aglomerular kidney of the deep-sea fish, Ateleopus japonicas (Ateleopodiformes: Ateleopodidae): Evidence of wider occurrence of the aglomerular condition in teleostei. Copeia; 3: 609-617.
Powell DV. (2000) Immune system. Gross functional anatomy. En: The laboratory fish. (Ostrander, G.K., ed.) London: Academic Press. Pp. 219-223.
Resende AD, Lobo-da-Cunha L, Malhão F, Franquinho F, Montero RAF, Rocha E. (2010) Histological and stereological charactetization of Brown Trout (Salmo trotta f. fario) trunk kidney. Microsc Microanal; 16: 677-687.
Schein V, Cardoso JCR, Pinto PIS, Anjos L, Silva N, Power DM, Canário AVM. (2012). Four stanniocalcin genes in teleost fish: Structure, phylogenetic analysis, tissue distribution and expression during hypercalcemic challenge. Gen Comp Endocr; 175(2): 344-356.
Takashima F, Hibiya T. (1995) An atlas of fish histology. Normal and pathological features. Ed. Kodansha Ltd. (Tokyo, Japon). Pp. 116.
Trump BF, Jones RT, Sahaphong S. (1975) Cellular effects of mercury on fish kidney tubules En: The Pathology of Fishes, Eds. W.E. Ribelin y G. Migaki, Univ. Wisconsin Press (Madison, Wisconsin): 585-612.
Urasa FM, Wendelaar Bonga SE. (1987) Effects of calcium and phosphate on the corpuscles of Stannius of the teleost fish Oreochromis mossambicus. Cell Tissue Res; 241: 219-227.
Verde C, Giordano D, Russo R, Riccio A, Coppola D, di Prisco G. (2011) Evolutionary adaptations in antarctic fish: the oxygen-transport system. Oecol Aust; 15(1): 40-50.
Vigliano F, Bermúdez R, Nieto JM, Quiroga MI. (2009) Ultrastructure of haemopoietic organs of the Argentinean silverside (Odontesthes bonariensis). Acta Microsc; 18: 677-678.
Wendelaar Bonga SE, Greven JAA. (1975) A second cell type in Stannius bodies of two euryhaline teleost species. Cell Tissue Res; 159: 287-290.
Wendelaar Bonga SE, Van der Meij JCA, Pang PKT. (1980) Evidence for two secretory cell types in the Stannius bodies of the teleosts Fundulus heteroclitus and Carassius auratus. Cell Tissue Res; 212: 295-306.
Wolke RE, Murchelano RA, Dickstein C., George CJ. (1985) Preliminary evaluation of the use of macrophage aggregates (MA) as fish health monitors. Bull Environ Contam Toxicol; 35: 222-227.
Wood EM, Yasutake BA. (1956) Ceroid in fish. American J Pathol; 32: 591-603.
Yasutake WT, Wales JH. (1983) Microscopic anatomy of salmonids: an atlas. U.S. Fish Wildlife Serv., Res. Publ. 150. Pp. 190.
Younson JH. (2007) Peripheral endocrine glands. II. The adrenal glands and the corpuscle Stannius. Fish Physiol; 26: 457-513.
Zapata AG, Chibá A, Varas A. (1996) Cells and tissues of the immune system of fish. En: The fish immune system. Organism, pathogen, and environment. (Iwama G., Nakanishi T., eds.). San Diego: Academic Press. Pp. 1-62.
Agius C, Roberts RJ. (1981) Effects of starvation on the melanomacrophage centers of fish. J Fish Biol; 19: 161-169.
Agius C, Roberts RJ. (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis; 26: 499-509.
Ahmad MF, Alim A, Sen NS, Lakra G, Mishra KP, Raza B, Chakarborty B, Rao NVA, Bonga SEW. (2002) Electron microscopic studies of the corpuscles of Stannius of an airbreathing teleost (Heteropneustes fossilis). J Biosci; 27(5): 509-513.
Ahmad MF, Prasad DK, Rao NVA. (2010) Ultrastructure of the corpuscles of the Stannius of an airbreathing catfish Clarias batrachus Linn. Proc. Natl. Acad. Sci. India Section B Biol Sci; 80: 230-234.
Aida K, Nishioka RS, Bern HA. (1980) Degranulation of the Stannius corpuscles of Coho salmon (Onchorhynchus kisutch) in response to ionic changes in vitro. Gen Comp Endocrinol; 41: 305-313.
Bhattacharyya TK, Butler DG. (1978) Fine structure of the corpuscles of Stannius in the toadfish. J Morphol; 155(3): 271-285.
Bone Q, Moore RH. (2008) Chapter 6. Osmoregulation and ion balance. En: Biology of fishes. 3er. Ed. Abingdon, UK. Taylor & Francis Group. Pp. 161-187.
Bucher F, Hofer R. (1993) Histological and enzyme histochemical changes in the kidney of male bullhead (Cottus gobio) during the spawning period. J Fish Biol; 42: 403-409.
Butler DG, Zhang DH. (2001) Corpuscles of Stannius secrte rennin and isorenin that regulates cardiovascular function in freshwater North American eels, Anguilla rostrata LeSueur. Gen Com Endocrinol; 124: 199-217.
Cousseau MB. (2010) Capítulo 5. Los peces óseos (Clases Actinopterygii y Sarcopterygii). En: Ictiología. Aspectos fundamentales. La vida de los peces sudamericanos. 1r. Ed. EUDEM, Argentina. Pp. 239-461.
Díaz AO, Devicenti CV, Ricci L, Goldemberg AL. (1996) Comparative histology and histochemistry of hake (Merluccius hubbsi) and white croaker (Micropogonias furnieri) kidney. J Anim Morphol Physiol; 43(1): 59-63.
Díaz AO, Goldemberg AL. (2004) Capítulo 6. Sistema excretor en peces. En: Temas de Histología y Embriología Animal. Parte 3. Analía Nessi y col. Ed. Inarbite (Buenos Aires). 2° edición. Pp. 85-92.
Domitrovic HA. (2000) Histología e histopatología del riñón de Cichlasoma dimerus (Pisces, Cichlidae). Universidad Nacional Del Nordeste. Comunicaciones Científicas y Tecnológicas 2000.
Ellis AE, Roberts RJ, Tytler P. (1989) The anatomy and physiology of teleosts. En: Fish Pathology, 2nd. Ed., R.J. Roberts ed., Bailliere Tindall (London). Pp. 13-55.
Ericsson JLE, Olsen S. (1970) On the fine structure of the aglomerular renal tubule in Lophius piscatorius. Z Zellforsch; 104: 240-258.
Gheng CC, Chen L, Near TJ, Jin Y. (2003) Functional antifreeze glycoprotein genes in temperate-water New Zealand nototheniid fish infer an Antarctic evolutionary origin. Mol Biol Evol; 20(11): 1897-1908.
González G, Crespo S, Brusle J. (1993) Histo-cytological study of the liver of the cabrilla sea bass, Serranus cabrilla (Teleostei, Serranidae), an available model for marine fish experimental studies. J Fish Biol; 43: 363-73.
Grizzle JM, Rogers WA. (1976) Excretory system. En: Anatomy and histology of the channel catfish. Auburn Pinting Inc., Auburn University, Agr. Exptl. Station. pp. 35-39.
Herraez MP, Zapata AG. (1991) Structural characterization of the melanomacrophage centres (MMC) of goldfish Carassius auratus. Eur J Morphol; 29(2): 89-102.
Hill RW, Wise GA, Anderson M. (2006) Capítulo 26. Fisiología hidrosalina: de los animales en sus hábitats. En: Fisiología Animal. Editorial Médica Panamericana S.A. Pp. 811-855.
Jarial MS, Wilkins JH. (2010) Structure of the kidney in the coelacanth Latimeria chalumnae with reference to osmoregulation. J Fish Biol; 76: 655-668.
Jiménez A, Esteban FJ, Sánchez-López AM, Pedrosa JA, Del Moral ML, Hernández R, Blanco S, Barroso JB, Rodrigo J, Peinado MA. (2001) Immunohistochemical localisation of neuronal nitric oxide synthase in the rainbow trout kidney. J Chem Neuroanatomy; 21: 289-294.
Kaneko T, Hirano T. (1993) Role of prolactin and somatolactin in calcium regulation in fish. J Exp Biol; 184: 31-45.
Kardong KV. (2007) Capítulo 14. El sistema urogenital. En: Vertebrados. Anatomía comparada, función y evolución. 4ta. Ed. McGraw Hill Interamericana. Pp. 538-584.
Krishnamurthy VG, Bern HA. (1969) Correlative histological study of the corpuscles of Stannius and juxtaglomerular cells of teleost fishes. Gen Comp Endocrinol; 13: 313-335.
Lagler KF, Bardach JE, Miller RR, May Passino DR. (1984) Capítulo 9. Excreción y regulación osmótica. En: Ictiología. AGT Ed., S. A. México. Pp. 247-262.
Macchi GJ, Romano LA, Christiansen HE. (1992) Melano macrophage centres in whitemouth croacker Micropogonias furneri, as biological indicators of environmental changes. J Fish Biol; 40: 971-973.
Meats M, Ingleton PM, Chestor Jones I, Garland HC, Kenyon CJ. (1978) Fine structure of the corpuscles of Stannius of the trout, Salmo gairdneri: Structural changes in response to increased environmental salinity and calcium ions. Gen Comp Endocrinol; 36: 451-461.
Norris DO. (2007) Bioregulation of calcium and phosphate homeostasis: Calcium and phosphate homeostasis in non-mammalian vertebrates. En: Vertebrate Endocrinology, fourth edition, Elsevier Academic Press, USA, pp. 501-510.
Ojeda JL, Icardo JM, Domezain A. (2003) Renal corpuscle of the sturgeon kidney: an ultrastructural, chemical dissection, and lectin-binding study. Anat Rec A; 272A: 563-573.
Ojeda JL, Icardo JM, Wong WP, Ip YK. (2006) Microanatomy and ultrastructure of the kidney of the African lungfish Protopterus dolloi. Anat Rec A; 288A: 609-625.
Ozaka C, Yamamoto N, Somiya H. (2009) The aglomerular kidney of the deep-sea fish, Ateleopus japonicas (Ateleopodiformes: Ateleopodidae): Evidence of wider occurrence of the aglomerular condition in teleostei. Copeia; 3: 609-617.
Powell DV. (2000) Immune system. Gross functional anatomy. En: The laboratory fish. (Ostrander, G.K., ed.) London: Academic Press. Pp. 219-223.
Resende AD, Lobo-da-Cunha L, Malhão F, Franquinho F, Montero RAF, Rocha E. (2010) Histological and stereological charactetization of Brown Trout (Salmo trotta f. fario) trunk kidney. Microsc Microanal; 16: 677-687.
Schein V, Cardoso JCR, Pinto PIS, Anjos L, Silva N, Power DM, Canário AVM. (2012). Four stanniocalcin genes in teleost fish: Structure, phylogenetic analysis, tissue distribution and expression during hypercalcemic challenge. Gen Comp Endocr; 175(2): 344-356.
Takashima F, Hibiya T. (1995) An atlas of fish histology. Normal and pathological features. Ed. Kodansha Ltd. (Tokyo, Japon). Pp. 116.
Trump BF, Jones RT, Sahaphong S. (1975) Cellular effects of mercury on fish kidney tubules En: The Pathology of Fishes, Eds. W.E. Ribelin y G. Migaki, Univ. Wisconsin Press (Madison, Wisconsin): 585-612.
Urasa FM, Wendelaar Bonga SE. (1987) Effects of calcium and phosphate on the corpuscles of Stannius of the teleost fish Oreochromis mossambicus. Cell Tissue Res; 241: 219-227.
Verde C, Giordano D, Russo R, Riccio A, Coppola D, di Prisco G. (2011) Evolutionary adaptations in antarctic fish: the oxygen-transport system. Oecol Aust; 15(1): 40-50.
Vigliano F, Bermúdez R, Nieto JM, Quiroga MI. (2009) Ultrastructure of haemopoietic organs of the Argentinean silverside (Odontesthes bonariensis). Acta Microsc; 18: 677-678.
Wendelaar Bonga SE, Greven JAA. (1975) A second cell type in Stannius bodies of two euryhaline teleost species. Cell Tissue Res; 159: 287-290.
Wendelaar Bonga SE, Van der Meij JCA, Pang PKT. (1980) Evidence for two secretory cell types in the Stannius bodies of the teleosts Fundulus heteroclitus and Carassius auratus. Cell Tissue Res; 212: 295-306.
Wolke RE, Murchelano RA, Dickstein C., George CJ. (1985) Preliminary evaluation of the use of macrophage aggregates (MA) as fish health monitors. Bull Environ Contam Toxicol; 35: 222-227.
Wood EM, Yasutake BA. (1956) Ceroid in fish. American J Pathol; 32: 591-603.
Yasutake WT, Wales JH. (1983) Microscopic anatomy of salmonids: an atlas. U.S. Fish Wildlife Serv., Res. Publ. 150. Pp. 190.
Younson JH. (2007) Peripheral endocrine glands. II. The adrenal glands and the corpuscle Stannius. Fish Physiol; 26: 457-513.
Zapata AG, Chibá A, Varas A. (1996) Cells and tissues of the immune system of fish. En: The fish immune system. Organism, pathogen, and environment. (Iwama G., Nakanishi T., eds.). San Diego: Academic Press. Pp. 1-62.
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PLAUL, S., DIAZ, A. O., & BARBEITO, C. G. (2014). Comparative aspects of kidney morphology of fish. Revista Ciencias Morfológicas, 14(1). Retrieved from https://revistas.unlp.edu.ar/Morfol/article/view/900
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