BACKGROUND: The basic function of the immune system is to protect an organism against infection in order to minimize the fitness costs of being infected. According to life-history theory, energy resources are in a trade-off between the costly demands of immunity and other physiological demands. Concerning fish, both physiology and immunity are influenced by seasonal changes (i.e. temporal variation) associated to the changes of abiotic factors (such as primarily water temperature) and interactions with pathogens and parasites. In this study, we investigated the potential associations between the physiology and immunocompetence of common carp (Cyprinus carpio) collected during five different periods of a given year. Our sampling included the periods with temporal variability and thus, it presented a different level in exposure to parasites. We analyzed which of two factors, seasonality or parasitism, had the strongest impact on changes in fish physiology and immunity. RESULTS: We found that seasonal changes play a key role in affecting the analyzed measurements of physiology, immunity and parasitism. The correlation analysis revealed the relationships between the measures of overall host physiology, immunity and parasite load when temporal variability effect was removed. When analyzing separately parasite groups with different life-strategies, we found that fish with a worse condition status were infected more by monogeneans, representing the most abundant parasite group. The high infection by cestodes seems to activate the phagocytes. A weak relationship was found between spleen size and abundance of trematodes when taking into account seasonal changes. CONCLUSIONS: Even if no direct trade-off between the measures of host immunity and physiology was confirmed when taking into account the seasonality, it seems that seasonal variability affects host immunity and physiology through energy allocation in a trade-off between life important functions, especially reproduction and fish condition. Host immunity measures were not found to be in a trade-off with the investigated physiological traits or functions, but we confirmed the immunosuppressive role of 11-ketotestosterone on fish immunity measured by complement activity. We suggest that the different parasite life-strategies influence different aspects of host physiology and activate the different immunity pathways.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

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Koskivaara M, Tellervo EV, Prost M. Seasonal occurrence of gyrodactylid monogeneans on the roach (Rutilus rutilus) and variations between four lakes of differing water quality in Finland. Aqua Fenn. 1991;21:47–55.

Rohde K, Hayward C, Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol. 1995;25:945–970. doi: 10.1016/0020-7519(95)00015-T. PubMed DOI

Bly JE, Clem LW. Temperature and teleost immune functions. Fish Shellfish Immun. 1992;2:159–171. doi: 10.1016/S1050-4648(05)80056-7. DOI

Hutchinson TH, Manning MJ. Seasonal trends in serum lysozyme activity and total protein concentration in dab (Limanda limanda L.) sampled from Lyme Bay, UK. Fish Shellfish Immun. 1996;6:473–482. doi: 10.1006/fsim.1996.0045. DOI

Le Morvan C, Troutaud D, Deschaux P. Differential effects of temperature on specific and nonspecific immune defences in fish. J Exp Biol. 1998;201:165–168. PubMed

Langston AL, Hoare R, Stefansson M, Fitzgerald R, Wergeland H, Mulcahy M. The effect of temperature on non-specific defence parameters of three strains of juvenile Atlantic halibut (Hippoglossus hippoglossus L.) Fish Shellfish Immun. 2002;12:61–76. doi: 10.1006/fsim.2001.0354. PubMed DOI

Hernández A, Tort L. Annual variation of complement, lysozyme and haemagglutinin levels in serum of the gilthead sea bream Sparus aurata. Fish Shellfish Immun. 2003;15:479–481. doi: 10.1016/S1050-4648(03)00024-X. PubMed DOI

Duffy JE, Carlson E, Li Y, Prophete C, Zelikoff JT. Impact of polychlorinated biphenyls (PCBs) on the immune function of fish: age as a variable in determining adverse outcome. Mar Environ Res. 2002;54:559–563. doi: 10.1016/S0141-1136(02)00176-9. PubMed DOI

Carlson E, Zelikoff J. The immune system of fish: a target organ of toxicity. Washington DC: Taylor and Francis; 2008.

Du Pasquier L. Evolution of the Immune System. New York: Raven Press; 1993.

Ainsworth AJ, Dexiang C, Waterstrat PR, Greenway T. Effect of temperature on the immune system of channel catfish (Ictalurus punctatus). I. Leucocyte distribution and phagocyte function in the anterior kidney at 10°C. Comp Biochem Phys A. 1991;100:907–912. doi: 10.1016/0300-9629(91)90313-2. PubMed DOI

Ellis AE. Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol. 2001;25:827–839. doi: 10.1016/S0145-305X(01)00038-6. PubMed DOI

Magnadóttir B, Jónsdóttir H, Helgason S, Björnsson B, Jørgensen TO, Pilström L. Humoral immune parameters in Atlantic cod (Gadus morhua L.) - II. The effects of size and gender under different environmental conditions. Comp Biochem Phys B. 1999;122:181–188. PubMed

Saha NR, Usami T, Suzuki Y. Seasonal changes in the immune activities of common carp (Cyprinus carpio) Fish Physiol Biochem. 2002;26:379–387.

Aydogdu A, Altunel FN. Helminth parasites (Plathelminthes) of common carp (Cyprinus carpio L.) in Iznik Lake. B Eur Assoc Fish Pat. 2002;22:343–348.

Buchmann K, Lindenstrøm T. Interactions between monogenean parasites and their fish hosts. Int J Parasitol. 2002;32:309–319. doi: 10.1016/S0020-7519(01)00332-0. PubMed DOI

Muñoz G, Grutter AS, Cribb TH. Structure of the parasite communities of a coral reef fish assemblage (Labridae): Testing ecological and phylogenetic host factors. J Parasitol. 2007;93:17–30. doi: 10.1645/GE-969R.1. PubMed DOI

Lamková K, Šimková A, Palíková M, Jurajda P, Lojek A. Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res. 2007;101:775–789. doi: 10.1007/s00436-007-0546-3. PubMed DOI

Alvarez-Pellitero P. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet Immunol Immunop. 2008;126:171–198. doi: 10.1016/j.vetimm.2008.07.013. PubMed DOI

Sitja-Bobadilla A. Living off a fish: A trade-off between parasites and the immune system. Fish Shellfish Immun. 2008;25:358–372. doi: 10.1016/j.fsi.2008.03.018. PubMed DOI

Sorci G, Bouliner T, Gauthier-Clerc M, Faivre B. Écologie évolutive de la Réponse Immunitaire (in French) Bruxelles: De Boeck & Larcier; 2007.

Šimková A, Lafond T, Ondračková M, Jurajda P, Ottová E, Morand S. Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evol Biol. 2008;8:29. doi: 10.1186/1471-2148-8-29. PubMed DOI PMC

Roff DA. The Evolution of Life Histories. Routledge: Chapman & Hall, Inc.; 1992.

Keymer AE, Read AF. Behavioural Ecology: the Impact of Parasitism in Parasite-Host Associations: Coexistence or Conflict? Oxford: University Press; 1991.

Zuk M, Stoehr AM. Immune defense and host life history. Am Nat. 2002;160:S9–S22. doi: 10.1086/342131. PubMed DOI

Owens IPF, Wilson K. Immunocompetence: a neglected life history trait or conspicuous red herring? Trends Ecol Evol. 1999;14:170–172. doi: 10.1016/S0169-5347(98)01580-8. DOI

Tschirren B, Richner H. Parasites shape the optimal investment in immunity. Proc Biol Sci. 2006;273:1773–1777. doi: 10.1098/rspb.2006.3524. PubMed DOI PMC

Folstad I, Karter AJ. Parasites, bright males, and the immunocompetence handicap. Am Nat. 1992;139:603–622. doi: 10.1086/285346. DOI

Ottová E, Šimková A, Jurajda P, Dávidová M, Ondračková M, Pečínková M, Gelnar M. Sexual ornamentation and parasite infection in males of common bream (Abramis brama): a reflection of immunocompetence status or simple cost of reproduction? Evol Ecol Res. 2005;7:581–593.

Rohlenová K, Šimková A. Are the immunocompetence and the presence of metazoan parasites in cyprinid fish affected by reproductive efforts of cyprinid fish? J Biomed Biotechnol. 2010. Article Number:418382. PubMed PMC

Pravda D, Svobodová Z. Haematology of Fishes (in Czech) Brno: Noviko; 2003.

Ergens R, Lom J. Causative Agents of Parasitic Fish Diseases (in Czech) Prague: Academia; 1970.

Secombes CJ. In: The Fish Immune System - Organism, Pathogen and Environment. Iwama G, Nakanishi T, editor. San Diego: Academic Press; 1996. The nonspecific immune system: Cellular defence; pp. 63–103.

Scott AL, Rogers WA, Klesius PH. Chemiluminescence by peripheral blood phagocytes from channel catfish: function of opsonin and temperature. Dev Comp Immunol. 1985;9:241–250. doi: 10.1016/0145-305X(85)90115-6. PubMed DOI

Nikoskelainen S, Bylund G, Lilius EM. Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Dev Comp Immunol. 2004;28:581–592. doi: 10.1016/j.dci.2003.10.003. PubMed DOI

Kubala L, Lojek A, Číž M, Vondráček J, Dušková M, Slavíková H. Determination of phagocyte activity in whole blood of carp (Cyprinus carpio) by luminol-enhanced chemiluminescence. Vet Med (in Czech) 1996;41:323–327. PubMed

Ellis AE. Immunity to bacteria in fish. Fish Shellfish Immun. 1999;9:291–308. doi: 10.1006/fsim.1998.0192. DOI

Buchmann K. Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea) Dis Aquat Organ. 1998;32:195–200. PubMed

Harris PD, Soleng A, Bakke TA. Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology. 1998;117:137–143. doi: 10.1017/S003118209800287X. PubMed DOI

Virta M, Karp M, Rönnemaa S, Lilius EM. Kinetic measurement of the membranolytic activity of serum complement using bioluminescent bacteria. J Immunol Methods. 1997;201:215–221. doi: 10.1016/S0022-1759(96)00225-6. PubMed DOI

Nikoskelainen S, Lehtinen J, Lilius EM. Bacteriolytic activity of rainbow trout (Oncorhynchus mykiss) complement. Dev Comp Immunol. 2002;26:797–804. doi: 10.1016/S0145-305X(02)00032-0. PubMed DOI

Buchtíková S, Vetešníková Šimková A, Rohlenová K, Flajšhans M, Lojek A, Esa-Matti Lilius, Hyršl P. The seasonal changes in innate immunity of the common carp (Cyprinus carpio) Aquaculture. 2011;318:169–175. doi: 10.1016/j.aquaculture.2011.05.013. DOI

Harding FA, Amemiya CT, Litman RT, Cohen N, Litman GW. Two distinct immunoglobulin heavy chain isotypes in a primitive, cartilaginous fish, Raja erinacea. Nucleic Acids Res. 1990;18:6369–6376. doi: 10.1093/nar/18.21.6369. PubMed DOI PMC

Danilová N, Bussmann J, Jekosch K, Steiner LA. The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat Immunol. 2005;6:295–302. doi: 10.1038/ni1166. PubMed DOI

Hansen JD, Landis ED, Phillips RB. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. P Natl Acad Sci USA. 2005;102:6919–6924. doi: 10.1073/pnas.0500027102. PubMed DOI PMC

Sánchez C, Babin M, Tomillo J, Ubeira FM, Domínguez J. Quantification of low levels of rainbow trout immunoglobulin by enzyme immunoassay using two monoclonal antibodies. Vet Immunol Immunopathol. 1993;36:65–74. doi: 10.1016/0165-2427(93)90006-P. PubMed DOI

Secombes CJ, Chappell LH. Fish immune responses to experimental and natural infection with helminth parasites. Annu Rev Fish Dis. 1996;6:167–177.

Griffin BR. Opsonic effect of rainbow trout (Salmo gairdneri) antibody on phagocytosis of Yersinia ruckeri by trout leukocytes. Dev Comp Immunol. 1983;7:253–259. doi: 10.1016/0145-305X(83)90006-X. PubMed DOI

McEwan AD, Fischer EW, Selman IE. Observations on the immune globulin levels of neonatal calves and their relationship to disease. J Comp Pathol. 1970;80:259–265. doi: 10.1016/0021-9975(70)90093-9. PubMed DOI

Borg B. Androgens in teleost fishes. Comp Biochem Phys C. 1994;109:219–245. doi: 10.1016/0305-0491(94)90005-1. DOI

Lusková V. Annual Cycles and Normal Values of Hematological Parameters in Fishes. Brno: Acta Scientiarum Naturalium; 1997.

Modrá H, Svobodová Z, Kolářová J. Comparison of differential leukocyte counts in fish of economic and indicator importance. Acta Vet Brno. 1998;67:215–226. doi: 10.2754/avb199867040215. DOI

Ruane NM, Nolan DT, Rotllant J, Costelloe J, Bonga SEW. Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Kroyer) influences the physiological response to an acute stressor. Fish Shellfish Immun. 2000;10:451–463. doi: 10.1006/fsim.1999.0260. PubMed DOI

Doubek J. Veterinary Haematology (in Czech) Brno: Noviko; 2003.

Svobodová Z, Pravda D, Paláčková J. Universal methods of hematological investigations in fish (in Czech) Vodňany: Edice Metodik; 1986.

Lusková V. Annual cycles and normal values of hematological parameters in fishes. Brno: Acta Scientiarum Naturalium; 1997.

Manning MJ. In: Immunology, A comparative approach. Turner RJ, editor. New York: Wiley; 1994. Fishes; pp. 69–100.

Dalmo RA, Ingebrigtsen K, Bogwald J. Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES) J Fish Dis. 1997;20:241–273. doi: 10.1046/j.1365-2761.1997.00302.x. DOI

Taskinen J, Kortet R. Dead and alive parasites: sexual ornaments signal resistance in the male fish, Rutilus rutilus. Evol Ecol Res. 2002;4:919–929.

Kortet R, Taskinen J. Parasitism, condition and number of front head breeding tubercles in roach (Rutilus rutilus L.) Ecol Freshw Fish. 2004;13:119–124. doi: 10.1111/j.1600-0633.2004.00039.x. DOI

Lefebvre F, Mounaix B, Poizat G, Crivelli AJ. Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses. J Fish Biol. 2004;64:435–447. doi: 10.1111/j.0022-1112.2004.00309.x. DOI

Piersma T, Lindström Å. Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol. 1997;12:134–138. doi: 10.1016/S0169-5347(97)01003-3. PubMed DOI

Bolger T, Connolly PL. The selection of suitable indexes for the measurement and analysis of fish condition. J Fish Biol. 1989;34:171–182. doi: 10.1111/j.1095-8649.1989.tb03300.x. DOI

Malmberg G. Excretory systems and marginal hooks as a basis for systematics of Gyrodactylus (Trematoda, Monogenea) Ark Zool. 1970;23:1–235.

Georgiev B, Biserkov V, Genov T. In toto staining method for cestodes with iron acetocarmine. Helminthologia. 1986;23:279–291.

Gusev AV. Part I. Identification Key to Parasites of Freshwater Fish (in Russian) Leningrad: Nauka; 1985.

Khotenovsky IA. Monogenea (in Russian) Leningrad: Nauka; 1985.

Scholz T. Amphilinida and Cestoda, Parasites of Fish in Czechoslovakia. Brno: Acta Scientiarum Naturalium; 1989.

Kadlec D, Šimková A, Gelnar M. The microhabitat distribution of two Dactylogyrus species parasitizing the gills of the barbel, Barbus barbus. J Helminthol. 2003;77:317–325. doi: 10.1079/JOH2003183. PubMed DOI

Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol. 1997;83:575–583. doi: 10.2307/3284227. PubMed DOI

Poisot T, Šimková A, Hyršl P, Morand S. Interactions between immunocompetence, somatic condition and parasitism in the chub Leuciscus cephalus in early spring. J Fish Biol. 2009;75:1667–1682. doi: 10.1111/j.1095-8649.2009.02400.x. PubMed DOI

Vainikka A, Taskinen J, Loytynoja K, Jokinen E, Kortet R. Measured immunocompetence relates to the proportion of dead parasites in a wild roach population. Funct Ecol. 2009;23:187–195. doi: 10.1111/j.1365-2435.2008.01482.x. DOI

Esch GW, Bush AO, Aho JM. Parasite Communities: Patterns and Progresses. London: Chapman and Hall; 1990.

Hanzelová V, Gerdeaux D. Seasonal occurrence of the tapeworm Proteocephalus longicollis and its transmission from copepod intermediate host to fish. Parasitol Res. 2003;91:130–136. doi: 10.1007/s00436-003-0939-x. PubMed DOI

Chubb JC. Seasonal ocurrence of helminths in freshwater fishes Part. I. Monogenea. Adv Parasit. 1977;15:133–139. PubMed

Kappe A, Seifert T, El-Nobi G, Brauer G. Occurrence of Atractolytocestus huronensis (Cestoda, Caryophyllaeidae) in German pond-farmed common carp Cyprinus carpio. Dis Aquat Organ. 2006;70:255–259. PubMed

Reimchen TE, Nosil P. Ecological causes of sex-biased parasitism in threespine stickleback. Biol J Linn Soc. 2001;73:51–63. doi: 10.1006/bijl.2001.0523. DOI

Ersdal C, Midtlyng PJ, Jarp J. An epidemiological study of cataracts in seawater farmed Atlantic salmon (Salmo salar) Dis Aquat Organ. 2001;45:229–236. PubMed

Pennycuick L. Seasonal variations in the parasite infections in a population of three-spinned sticklebacks, Gasterosteus aculeatus L. Parasitology. 1971;63:378–388. PubMed

McKeown CA, Irwin SWB. Accumulation of Diplostomum spp. (Digenea: Diplostomatidae) Metacercariae in the eyes of 0+ and 1+ roach (Rutilus rutilus) Int J Parasitol. 1997;27:377–380. doi: 10.1016/S0020-7519(96)00204-4. PubMed DOI

Burrough RJ. The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd. J Fish Biol. 1978;13:19–32. doi: 10.1111/j.1095-8649.1978.tb03409.x. DOI

Walker PD, Russon IJ, Duijf R, Bonga SEW. The effect of temperature on the biology, survival and viability of the fish parasite, Argulus japonicus Thiele. Comp Biochem Phys A. 2005;141:S90–S90.

Hakalahti T, Pasternak AF, Valtonen ET. Seasonal dynamics of egg laying and egg-laying strategy of the ectoparasite Argulus coregoni (Crustacea: Branchiura) Parasitology. 2004;128:655–660. doi: 10.1017/S0031182004004986. PubMed DOI

Harrison AJ, Gault NFS, Dick JTA. Seasonal and vertical patterns of egg-laying by the freshwater fish louse Argulus foliaceus (Crustacea: Branchiura) Dis Aquat Organ. 2006;68:167–173. PubMed

Hakalahti T, Valtonen ET. Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitology. 2003;127:79–85. doi: 10.1017/S0031182003003196. PubMed DOI

Busacker GP, Adelman IR, Goolish EM. Methods for Fish Biology. Maryland: American Fisheries Society; 1990.

Johansen K, Weber RE. In: Perspectives in Experimental Biology. Davies PS, editor. Oxford: Pergamon; 1976. On the adaptability of haemoglobin function to environmental conditions; pp. 219–234.

Weber RE. In: Animal Nutrition and Transport Processes, 2 - Transport, Respiration and Excretion: Comparative and Environmental Aspects. Truchot JP, Lahlou B, editor. Basel: Karger; 1990. Functional significance and structural basis of multiple hemoglobins with special reference to ectothermic vertebrates; pp. 58–75.

Lenhardt M. Seasonal changes in some blood chemistry parameters and in relative liver and gonad weights of pike (Esox lucius L.) from the river danube. J Fish Biol. 1992;40:709–718. doi: 10.1111/j.1095-8649.1992.tb02618.x. DOI

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

Skarstein F, Folstad I, Liljedal S. Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Can J Zoolog. 2001;79:271–278.

Suzuki Y, Orito M, Iigo M, Kezuka H, Kobayashi M, Aida K. Seasonal changes in blood IgM levels in goldfish, with special reference to water temperature and gonadal maturation. Fisheries Sci. 1996;62:754–759.

Avtalion RR. Temperature effect on antibody production and immunological memory, in carp (Cyprinus carpio) immunized against bovine serum albumin (BSA) Immunology. 1969;17:927–931. PubMed PMC

Stolen JS, Gahn T, Kasper V, Nagle JJ. The effect of environmental temperature on the immune response of a marine teleost (Paralichthys dentatus) Dev Comp Immunol. 1984;8:89–98. doi: 10.1016/0145-305X(84)90013-2. PubMed DOI

Suzuki Y, Otaka T, Sato S, Hou YY, Aida K. Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol Biochem. 1997;17:415–421. doi: 10.1023/A:1007795827112. DOI

Hou Y, Suzuki Y, Aida K. Changes in immunoglobulin producing cells in response to gonadal maturation in rainbow trout. Fisheries Sci. 1999;65:844–849.

Hou Y, Suzuki Y, Aida K. Effects of steroids on the antibody producing activity of lymphocytes in rainbow trout. Fisheries Sci. 1999;65:850–855.

Collazos ME, Barriga C, Ortega E. Seasonal changes in phagocytic capacity and superoxide anion production of blood phagocytes from tench (Tinca tinca, L.) J Comp Physiol B. 1995;165:71–76. doi: 10.1007/BF00264688. DOI

Collazos ME, Ortega E, Barriga C. Effect of temperature on the immune system of a cyprinid fish (Tinca tinca, L). Blood phagocyte function at low temperature. Fish Shellfish Immun. 1994;4:231–238. doi: 10.1006/fsim.1994.1021. DOI

Smyth JD, Halton DW. The Physiology of Trematodes. Cambridge: Cambridge University Press; 1983.

Sitja-Bobadilla A, Alvarez-Pellitero P. Experimental transmission of Sparicotyle chrysophrii (Monogenea: Polyopisthocotylea) to gilthead seabream (Sparus aurata) and histopathology of the infection. Folia Parasit. 2009;56:143–151. PubMed

Molnár K, Majoros G, Csaba G, Székely C. Pathology of Atractolytocestus huronensis Anthony, 1958 (Cestoda, Caryophyllaeidae) in Hungarian pond-farmed common carp. Acta Parasitol. 2003;48:222–228.

Scharsack JP, Kalbe M, Derner R, Kurtz J, Milinski M. Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Dis Aquat Organ. 2004;59:141–150. PubMed

Hakoyama H, Nishimura T, Matsubara N, Iguchi K. Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biol J Linn Soc. 2001;72:401–407. doi: 10.1111/j.1095-8312.2001.tb01326.x. DOI

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