Splenic Pigmented Macrophage Aggregates in Barbel (Barbus peloponnesius, Valenciennes, 1844) from River Bregalnica — Influences of Age, Sex and Season on a Pollution Biomarker

Macrophages are involved in innate and acquired immune responses, being key players in immunotoxicology. Changes in the quantities of pigmented macrophage aggregates (PMQ) in fish are often used as biomarkers of pollution. Most studies offer only qualitative data on PMQ changes, and effects of age, sex and season are poorly known. We present a stereological study of the relative and total volumes of PMQ in the barbel, Barbus peloponnesius spleen. Our focus is to disclose influences of age, sex and season on PMQ, and check if the there is any positive association with aging. The females had a significantly higher spleen and body weights and length. PMQ loaded with lipofuscin/ceroid and hemosiderin were dispersed throughout both spleen pulps. Seasons impacted on PMQ, despite no too markedly. Differences existed between sexes, with males having significantly higher relative volumes of PMQ: the total volumes had similar tendencies. The volumes of PMQ were positively associated with age. The new data reinforce the importance of studying influences of both intrinsic and extrinsic factors that model the quantities of PMQ so to better interpret their changes seen in biomonitoring works

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Agius, C. 1979. The role of melano-macrophage centers in iron storage in normal and diseased fish. Journal of Fish Diseases, 2: 337-343. doi: 10.1111/j.1365- 2761.1979.tb00175.x

Agius, C. 1980. Phylogenetic development of melanomacrophage centres in fish. Journal of Zoology, 191: 11-31. doi: 10.1111/j.1469-7998.1980.tb01446.x

Agius, C. 1981. The effects of splenectomy and subsequent starvation on the storage of haemosiderin by melanomacrophages of rainbow trout Salmo gairdneri Richardson. Journal of Fish Biology, 18: 41-44. doi:10.1111/j.1095-8649.1981.tb03757.x

Agius, C. 1985. The melano-macrophage centres of fish: A review. In: Ed:, M.J. Manning and M.F Tatner (Eds), Fish Immunology, Acad. press, London: 85-105.

Agius, C., and Agbede S.A. 1984. An electron microscopic study on the genesis of lipofuscin, melanin and hemosiderin in the haemopoietic tissues of fish. Journal of Fish Biology, 24: 471- 488. doi:10.1111/j.1095-8649.1984.tb04818.x.

Agius, C., and Roberts, R.J. 1981. Effects of starvation on the melano-macrophage centers of fish. Journal of Fish Diseases, 19:161-169. doi:10.1111/j.1095- 8649.1981.tb05820.x

Agius, C., and Roberts R.J. 2003. Melano-macrophage centres and their role in fish pathology. Review. Journal of Fish Disease, 26: 499-509. doi:10.1046/j.1365-2761.2003.00485.x.

Al Hazzaa, R. 2005. Some Biological Aspects of the Himri Barbel, Barbus luteus, in the Intermediate Reaches of the Euphrates River. Turkisk Journal of Zoology, 29: 311-315.

Armero-Lituañas, M.A. and Ocampo, P.P. 2015. Melanomacrophage proliferation in the spleen of Nile tilapia (Oreochromis niloticus L.) as biomarker of insecticides loading from the waters of Laguna de Bay, Municipality of Bay, Laguna, Philippines. International Journal of Agricultural Resources, Governance and Ecology, 11(1): 11-23. doi:org/10.1504/IJARGE.2015.069783

Álvarez, F., Razquin, B.E., Villena, A.J. and Zapata A.G. 1998. Seasonal changes in the lymphoid organs of wild brown trout, Salmo trutta L: A morphometrical study. Veterinary Immunology and Immunopathology, 64:267–278. doi:10.1016/S0165- 2427(98)00137-8.

Anderson, D.P.1990. Immunological indicators: effects of environmental stress on immune protection and disease outbreaks. In S. M. Adams (Eds), Biological indicators of stress in Fish American Fisheries Society Bethesda MD, Sump., 8:38-50.

Balamurugan, S., Deivasigamani, B., Kumaran, S., Sakthivel, M., Rajsekar, T. and Priyadharsini, P. 2012. Melanomacrophage centers aggregation in P. lineatus spleen as bio-indicator of environmental change. Asian Pacific Journal of Tropical Disease, S635-S638. doi 10.1016/S2222-1808(12)60235-7.

Balvanera, P., Pfisterer , A.B., Buchmann, N., He, J.S., Nakashizuka, T., Raffaelli, D. and Schmid B. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9: 1146–1156. doi: 10.1111/j.1461-0248.2006.00963.x.

Beso, G.A., Candelaria, V.Y., dela Cruz, J.F., Tolentino, M.S., Tameta, A D.C. and Espinosa, A. 2016. Effects of unleaded petroleum on the macrophage aggregates (MA) formation in red king tilapia (Oreochromis sp.) Fingerlings bioRxiv 044537; doi: http://dx.doi.org/10.1101/04453 7

Blazer, V.S., Wolke, R.E., Brown, J. and Powell, C.A. 1987. Piscine macrophage aggregate parameters as health monitors: effect of age, sex, relative weight, season and site quality in largemouth bass (Micropterus salmoides). Aquatic Toxicology, 10: 199–215. doi:10.1016/0166-445X(87)90012-9.

Brooks, T.M., Mittermeier, R.A., da Fonseca, G.A.B., Gerlach, J., Hoffmann, M., Lamoreux, J.F., Mittermeier, C.G., Pilgrim, J.D. and Rodrigues, A.S.L. 2006. Global biodiversity conservation priorities. Science, 313: 58–61. doi: 10.1126/science.1127609.

Brown, C.L., and George, C.J. 1985. Age-dependent accumulations of macrophage aggregates in the yellow perch, Perca flavescens (Mitchill). Journal of Fish Diseases, 8: 135-138. doi:10.1111/j.1365- 2761.1985.tb01195.x.

CEN EN14011, 2003 Water analysis-fishing with electricity for wadable and non-wadable rivers. European Committee for Standardization.

Chovanec, A., Hofer, R., and Schiemer, F. (2003): Fish as bioindicators. In: B.A. Market, , A.M. Brue, and , H.G. Zechmeister, (Eds.), Bioindicators and biomarkers: principles concepts and applications. Elsevier, 639–676.

Couillard, C.M. and Hodson, P.V. 1996. Pigmented macrophage aggregates: a toxic response in fish exposed to bleached-kraft mill effluent? Environmental Toxicology and Chemistry, 15: 1844- 1854. doi:10.1002/etc.5620151027

Covich, A.P., Austen, M.C., Bärlocher, F., Chauvet, E., Cardinale, B.J., Biles, C.L., Inchausti, P., Dangles, O., Solan, M., Gessner, M.O., Statzner, B. and Moss, B. 2004. The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. BioScience, 54: 767–775. doi:10.1641/0006- 3568(2004)054[0767:TROBIT]2.0.CC

Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z.I., Knowler, D.J., Leveque, C., Naiman, R.J., Prieur-Richard, A.H., Soto, D., Stiassny, M.L.J. and Sullivan, C.A. 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biology Reviews, 81: 163–182. doi: 10.1017/S1464793105006950

Ellis, A.E. 1980. Antigen-trapping in the spleen and kidney of the plaice, Pleuronectes platessa (L.). Journal of Fish Diseases, 3: 413-426. doi:10.1111/j.1365- 2761.1980.tb00425.x.

Facey D.E., Blazer, V.S., Gasper, M.M. and Turcotte, C.L. 2005. Using fish biomarkers to monitor improvements in environmental quality. Journal of Aqatic Animal Health. 17(3): 263-266. doi:10.1577/H04-055.1

Fänge, R., and Nilsson, S. 1985. The fish spleen: structure and function. Experientia., 41:152–158. doi:10.1007/BF02002607

Ferguson, H.W. 1976. The relationship between ellipsoids and melano-macrophage centres in the spleen of turbot (Scophthalmus maximus). J. Comparative Patology, 86: 377–380. doi:10.1016/0021- 9975(76)90005-0

Figueiredo-Fernandes, A.M, Fontainhas-Fernandes A.A, Monteiro R.A.F, Reis-Henriques M.A, Erocha E. 2006. Temperature and gender influences on the hepatic stroma (and associated pancreatic acini) of nile tilapia, Oreochromis niloticus (Teleostei, Cichlidae): A stereological analysis by light microscopy. Journal of Morphology 267: 221-230. doi:10.1002/jmor.1039.

Fishelson, L. and Becker, K. 2001. Development and Aging of the Liver and Pancreas in the Domestic Carp, Cyprinus carpio: From Embryogenesis to 15-year-old Fish. Environmental Biololy of Fishes, 61: 85–97. doi: 10.1023/A:1011076722505

Fournie, J.W., Summers, J.K., Courtiney, L.A. and Engle, V.D. 2001. Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. Journal of Aquatic Animal Health, 13: 105–116. doi: 10.1577/1548- 8667(2001)013<0105:UOSMAA>2.0.CO;2.

Freere, H and Weibel, E.R. 1967. Stereologic techniques in microscopy. Journal of Royal Microscopy Society 87: 25–34.

Froese R. 2006. Cube law, condition factor and weight– length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology, 22: 241–253. doi: 10.1111/j.1439-0426.2006.00805.x.

Fulop, G.M.I. and McMillan, D.B. 1984. Phagocytosis in the spleen of the sunfish Lepomis spp. Journal of Morphology, 179: 175–195. doi: 10.1002/jmor.1051790205.

Garcia-Abiado, M.A., Mbahinzireki, G., Rinchard, J., Lee, K.J. and Dabrowski, K. 2004 Effect of diets containing gossypol on blood parameters and spleen structure in tilapia, Oreochromis sp., reared in a recirculating system. Journal of Fish Disease, 27(6): 359–68. doi:10.1111/j.1365-2761.2004.00551.x

Gregori, M.,Miragliotta, V., Leotta, R., Cecchini, S., Prearo, M. and Abramo, M. 2014. Morphometric evaluation of interrenal gland and kidney macrophages aggregates in normal healthy rainbow trout (Oncorhynchus mykiss) and after bacterial challenge with Yersinia ruckeri. Veterinary Medicine International, 1-7. doi:org/10.1155/2014/210625

Haaparanta, A., Valtonen, E.T., Hoffmann, R. and Holmes, J. 1996. Do macrophage centres in freshwater fishes reflect the differences in water quality? Aquatic Toxicology, 34: 253–272. doi:10.1016/0166- 445X(95)00042-3

Hadidi, S., Glenney, G.W., Welch, T.J., Silverstein, J.T. and Wiens, G.D. 2008. Spleen Size Predicts Resistance of Rainbow Trout to Flavobacterium psychrophilum Challenge. The Journal of Immunology, 180: 4156- 4165. doi: 10.4049/jimmunol.180.6.4156

Hampton, J.A., Lantz, R.C. and Hinton, D.E. 1989. Functional units in rainbow trout (Salmo gairdneri, Richardson) liver: III. Morphometric analysis of parenchyma, stroma, and component cell types. American Journal of Anatomy, 185: 58–73. doi:10.1002/aja.1001850107.

Herráez, M.P. and Zapata, A.G. 1986. Structure and function of the melano-macrophage centres of the goldfish Carassius auratus. Veterenary Immunology and Immunopathology, 12: 117–126. doi:10.1016/0165-2427(86)90116-9

Hinck, J.E., Blazer, V.S., Denslow, N.D., Myers, M.S., Gross, T.S. and Tillitt, D.E. 2007. Biomarkers of Contaminant Exposure in Northern Pike (Esox lucius) from the Yukon River Basin, Alaska. Archivesof Environmental Contamination and Toxicology, 52: 549–562. doi:10.1007/s00244-006-0134-z

Hinton, D.E. 1993 Toxicology-histopathology of fishes: A systematic approach and overview. In: J.A Couch, and J.W. Fournie, (Eds.) Pathobiology of Marine and estuarine organisms, CRC Press, Boca Raton, F.L., 177–215.

Hinton, D.E., Baumann, P.C., Gardner, G.R., Hawkins, W.E., Hendricks, J.D., Murchelano, R.A. and Okihiro, M.S. 1992. Histopathologic biomarkers. In: Biomarkers – Biochemical, Physiological and Histological Markers of R. Huggett, R.A. Kimerle, P.M. Meherle and H.L. Bergman (Eds),Anthropogenic StressA special publication of SETAC Lewis Publichers Boca Raton, Ann. Arbor, London, Tokyo, 155-212.

Hung, S.W., Tu, C.Y. and Wang, W.S. 2007. In vivo effects of adding singular or combined anti-oxidative vitamins and/or minerals to diets on the immune system of tilapia (Oreochromis hybrids) peripheral blood monocyte-derived, anterior kidney-derived, and spleen-derived macrophages. Veterinary Immunology and Immunopathology 115: 87–99. doi.org/10.1016/j.vetimm.2006.09.004

Iwanoviwcz L. R., Blazer, V.S., Hitt, N.P, McCormick, S.D., DeVault, D.S. and Ottinger, C.A. 2012. Histologic, immunologic and endocrine biomarkers indicate contaminant effects in fishes of the Ashtabula River. Ecotoxicology, 21(1): 165-182 doi:10.1007/s10646-011-0776-0

Jordanova, M., Miteva, N. and Rocha, E. 2008. A quantitative and qualitative study of the hepatic pigmented macrophage aggregates during the breeding cycle of Ohrid trout, Salmo letnica Kar. (Teloestei, Salmonidae). Microscopy Research and Technique, 71: 822–830. doi:10.1002/jemt.20626

Jordanova, M., Rocha, M.J., Rebok, K. and Rocha, E. 2011. Changes in the amount of kidney pigmented macrophage aggregates throughout the breeding cycle of female Ohrid trout, Salmo letnica Kar. (Teloestei, Salmonidae). Microscopy research and technique, 75(2): 176–181.doi:10.1002/jemt.21040

Kelly-Reay, K. and Weeks-Perkins, B.A. 1994. Determination of the macrophage chemiluminescent response in Fundulus heteroclitus as a function of pollution stress. Fish Shellfish Immunology, 4:95– 105. doi:10.1006/fsim.1994.1008

Khallaf, E., Galal, M. and Athuman, M. 2003. The biology of Oreochromis niloticus in a polluted canal. Ecotoxicology, 12: 405–416. doi:10.1023/A:1026156222685

Kortet, R., Taskinen, J., Sinisalo, T., and I. Jokinen. 2003. Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus, L. Biological Journal of Linnean Society, 78: 117–127. doi:10.1046/j.1095- 8312.2003.00136.x

Kranz, H. 1989. Changes in splenic melano-macrophage centres of dab Limanda limanda during and after infection with ulcer disease. Diseases of Aquatic Organism, 6: 167–173.

Kranz, H. and Gercken, J. 1987. Effects of sublethal concentrations of potassium dichromate on the occurrence of splenic melano-macrophage centers in juvenile plaice, Pleuronectes platessa, L. Journal of Fish Biology, 31: 75–80. doi: 10.1111/j.1095- 8649.1987.tb05296.x

Kranz, H. and Peters, N. 1984. Melano-macrophage centers in liver and spleen of ruffe (Gymnocephalus cernua) from the Elbe Estuary. Helgoländer Meeresuntersuchunger, 37: 415–424. doi:10.1007/BF01989320

Krüger, R., Pietrock, M., Meinelt, T., Yoshida, T., Steffens, W. and Steinberg, Ch. 1996. Distribution of macrophage centres in bream (Abramis brama L.) liver from the Oder river (Germany/Poland) within the nature reserve “Unteres Odertal” near the town of Schwedt. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 81(4):635–644. doi: 10.1002/iroh.19960810420

Lamková, K., Šimková, A., Paliková, M., Jurajda P. and Lojek, A. 2007. Seasonal changes of immunocompetence and parasitism in chub Leuciscus cephalus, a freshwater cyprinid fish. Parasitology Research, 101(3): 775-789. doi:10.1007/s00436-007- 0546-3

Long, E.R., MacDonald, D.D., Smith, S.L. and Calder, F.D. 1995. Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management, 19: 81–97. doi: 10.1007/BF02472006

Manera, M. 1997. Gli aggregati dei macrofagi in orate (Sparus aurata Linneo, 1758) di allevamento sperimentalmente alimentate con diete arricchite degli oligoelementi rame, ferro, zinco. Tesi di Dottorato di Ricerca: Bologna.

Manera, M., Serra, R., Isani, G. and Carpené, E. 2000. Macrophage aggregates in gilthead sea bream fed copper, iron and zinc enriched diets. Journal of Fish Biology, 57: 457–465. doi:10.1111/j.1095- 8649.2000.tb02184.x

Marth Е., Jelovcan, S., Kleinhappl, B., Gutschi, A. and Barth, S. 2001. The effect of heavy metals on the immune system at low concentrations. International Journal of Occupational Medicine and Environmental Health, 14(4): 375-386.

Mayer, F.L., Versteeg, D.J., McKee, M.J., Folmar, L.C., Graney, R.L., McCume, D.C. and Rattner, B.A. 1992. Metabolic products as biomarkers. In: R.J.Huggett, R.A.Kimerly, P.M.Mehrle, and H.L. Bergman (Eds) Biomarkers: biochemical, physiological and histological markers of anthropogenic stress, Lewis Publishers, Chelsea, MI, 5-86.

Meador, M.R., Carlisle, D.M. and Coles, J.F. 2008. Use of tolerance values to diagnose water-quality stressors to aquatic biota in New England streams. Ecological Indicators, 8: 718–728. doi:10.1016/j.ecolind.2008.01.002

Meinelt, T., Kriiger, R., Pietrock, M., Osten, R. and Steinberg, C. 1997. Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Environmental Science and Pollution Research, 4(1): 32–36. doi:10.1007/BF02986262

Mizuno, S.N., Misaka, N., Miyakoshi, Y., Takeuchi, K., Kasahara, N. 2002. Effects of starvation on melanomacrophages in the kidney of masu salmon (Oncorhynchus masou). Aquaculture, 209:247–255. doi:10.1016/S0044-8486(01)00716-5

Nehemia, А., Justin D. Maganira, J.D. and Rumisha, C. 2012. Length-Weight relationship and condition factor of tilapia species grown in marine and fresh water ponds. Agriculture and Biology Journal of Nort America, 3(3): 117–124. doi:10.5251/abjna.2012.3.3.117.124

Omnes, M.H., Silva, F.C.P., Moriceau, J., Kaushik, S. and Gatesoupe F.J. 2015. Influence of lupin and repessed meals on the integrity of digestive tract and organs in gilthead seabream (Sparus aurata L.) and goldfish (Carassius auratus L.) juveniles. Aquaculture Nutrition, 21(2): 223-233. doi: org/10.1111/anu.1262

Peters, G. and Schwarzer, R. 1985. Changes in hemopoetic tissues of rainbow trout under influence of stress. Diseases of Aquatic organisms, 1: 1-10.

Pulsford, A.L., Ryan, K.P. and Nott, J.A. 1992. Metals and melanomacrophages in flounder, Platichthys flesus, spleen and kidney. Journal of Marine Biological Association of the United Kingdom, 72:483–498. doi: http://dx.doi.org/10.1017/S002531540003784X

Rabitto, I.S., Alves Costa, J.R.M., Silva de Assis, H.C., Pelletier, E., Akaishi, F.M., Anjos, A., Randi M.A.F. and Ribeiro O. 2005. Effects of dietary Pb (II) and tributylin an neotroptical fish Hoplias malabarius: Histopathological and biochemical findings Ecotoxicology and Environmental Safety., 60: 147– 156. doi:10.1016/j.ecoenv.2004.03.002

Rebok. 2013. A toxicopathology survey of the river Bregalnica using the barbel (Barbus peloponnesius, Valenciennes, 1844) as bioindicator. Doctoral Thesis. Ss Kyril and Methodius University, Skopje. Republic of Macedonia.

Rebok, K., Jordanova, M. and Tavciovska-Vasileva, I., 2011. Spleen histology in the female Ohrid trout, Salmo letnica (Kar.) (Teleostei, Salmonidae) during the reproductive cycle. Archive of Biological Sciences Belgrade, 63(4): 1023–1030. doi:10.2298/ABS1104023R

Roberts, R.J. 1975. Melanin-containing cells of teleost fish and their relation to disease. In: W.E.Ribelin,, and G. Migiaki (Eds.) The pathology of fish. University of Wisconsin press, Madison, 399–423.

Rocha, E. Monteiro, R.A.F. and Pereira, C.A. 1997. Liver of the brow trout, Salmo trutta (Teloestei, Salmonidae). A stereological study at light and electron microskopic levels. Anatomy Record, 247: 317–328. doi: 10.1002/(SICI)1097- 0185(199703)247:33.3.CO;2-F

Russo, R., Yanong R.P.E., Terrell SP. 2007. Preliminary morphometrics of spleen and kidney macrophage aggregates in clinically normal blue gourami Trichogaster trichopterus and freshwater angelfish Pterophyllum Scalare. Journal of Aquatic Animal Health, 19: 60-67. doi: 10.1577/H05-023.1

Schwindt, A.R., Truelove, N., Schreck, C.B., Fournie, J.W., Landers, D.H. and Kent, M.L. 2006. Quantitative evaluation of macrophage aggregates in brook trout Salvelinus fontinalis and rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms, 68: 101–113. doi:10.3354/dao068101

Šorić, V. 1992. The structure of population and reproductive potential of Barbus peloponnesius petenyi (Cyprinidae, Pisces) in the Gruza River. Collection of Scientific Papers, Faculty of Science Kragujevac 13:65–75.

Šorić, V. and Janković, D. 1989. Characteristics of growth and sexual maturity of Barbus meridionalis. Ichthyologia. 21(1):27–37.

Swansburg, E., Chaput, G., Moore, D., Caissie, D. and ElJabi, N. 2002. Size variability of juvenile Atlantic salmon: links to environmental conditions. Journal of Fish Biology, 61(3): 661–683. doi: 10.1111/j.1095- 8649.2002.tb00903.x

Thilakaratne, I.D.S.I.P., Mclaughlin J.D. and Marcogliese D.J. 2007. Effects of pollution and parasites on biomarkers of fish health in spottail shiners Notropis hudsonius (Clinton). Journal of Fish Biology, 71: 519–538. doi: 10.1111/j.1095-8649.2007.01511.x

Tischendorf, F. 1985. On the evolution of spleen. Experientia., 41:145–152. doi: 10.1007/BF02002606 Vasiliou, A. and Economidis, P.S. 2005. On the life-history of Barbus peloponnesius and Barbus cyclolepis in Macedonia, Greece. Folia Zoologica 54(3): 316–336.

Vogelbein, W.K., Fourine, J.W. and Overstreet, R.M. 1987. Sequential development and morphology of experimentally induced hepatic melano-macrophage centres in Rivulus marmoratus. Journal of Fish Biology, 31: 145–153. doi: 10.1111/j.1095- 8649.1987.tb05306.x

Weeks, B.A. and Warinner, J.E. 1986. Functional evaluation of macrophages in fish from a polluted estuary. Veterinary Immunology and Immunopathology, 12: 313–320. doi:10.1016/0165- 2427(86)90135-2

Weeks, B.A., Warinner, J.E., Mason, P.L. and McGinnis, D.S. 1986. Influence of toxic chemicals on the chemotactic response of fish macrophages. Journal of Fish Biolohy, 28:653–658. doi: 10.1111/j.1095- 8649.1986.tb05200.x

Wolke, R. E. 1992. Piscine macrophage aggregates: a review. Annual Review of Fish Diseases, 2: 91–108. doi:10.1016/0959-8030(92)90058-6

Woodward, G., Ebenman B., Emmerson, M., Montoya, J.M., Olesen, J.M., Valido, A. and Warren, P.H. 2005. Body-size in ecological networks. Trends in Ecology and Evolution, 20: 402–409. doi:10.1016/j.tree.2005.04.005

Wynn, TA, Chawla A. And Pollard W. 2013. Macrophage biology in development, homeostasis and disease. Nature, 496: 445-497. doi:10.1038/nature12034

Yildirim, A., Arslan, M., Bektas, S., and Pegg, M. 2006. Spatial and seasonal variations in condition of Barbus plebejus escherichi in the upper Çoruh River, Turkey. Journal of Freshwater Ecology, 21(3): 379–384. doi:10.1080/02705060.2006.9665013

Zapata, A. and Cooper, E.L. 1990. The immune system: Comparative Histophysiology. Chichester: John Wiley
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  • ISSN: 1303-2712
  • Başlangıç: 2015
  • Yayıncı: Su Ürünleri Merkez Araştırma Enstitüsü - Trabzon
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