Abstract
Although zebrafish (Danio rerio) is a highly studied organism on many fields of research, many aspects of its basic biology still elude the scientific community. Its response to temperature - especially developmental one - has been very scarcely studied and this is an important lack of knowledge since the species is considered quite eurythermal in nature. In the present study, zebrafish was subjected to four different developmental temperatures (22, 25, 28 and 31°C) from the half-epiboly stage until after metamorphosis in order to examine whether the temperature can influence the juvenile’s phenotype. Morphometric and meristic characters were explored. Body shape and almost all of the meristic characters studied were significantly affected by the temperature applied during the first stages of development. Most meristic characters of the study, presented a significant differentiation in the extreme temperatures used (22 and/or 31°C), whereas lower temperatures seemed to produce higher meristic counts in the majority of the characters. Zebrafish juveniles, as shown in this study, exhibit highly variable phenotypes (phenotypic plasticity) induced by diverse thermal conditions during their early ontogenetic stages possibly in order to successfully adjust to different environments.
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Abdel I, Abellán E, López-Albors O, Valdés P, Nortes M, García-Alcázar A (2005) Abnormalities in the juvenile stage of sea bass (Dicentrarchus labrax L.) reared at different temperatures: types, prevalence and effect on growth. Aquac Int 12(6):523–538
Alami-Durante H, Bergot P, Rouel M, Goldspink G (2000) Effects of environmental temperature on the development of the myotomal white muscle in larval carp (Cyprinus carpio L.). J Exp Biol 203(24):3675
Amsterdam A, Hopkins N (2006) Mutagenesis strategies in zebrafish for identifying genes involved in development and disease. Trends Genet 22:473–478
Axelrod H, Schultz L (1990) Handbook of tropical aquarium fishes. McGraw-Hill, New York, p 718
Ayala M, López-Albors O, Gil F, García-Alcázar A, Abellán E, Alarcón J, Álvarez M, Ramírez-Zarzosa G, Moreno F (2001) Temperature effects on muscle growth in two populations (Atlantic and Mediterranean) of sea bass, Dicentrarchus labrax L. Aquaculture 202(3–4):359–370
Bird N, Mabee P (2003) Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (Ostariophysi: Cyprinidae). Dev Dyn 228(3):337–357
Blaxter J (1991) The effect of temperature on larval fishes. Neth J Zool 42(3):336–357
Cabral HN, Marques JF, Rego AL, Catarino AI, Figueiredo J, Garcia J (2003) Genetic and morphological variation of Synaptura lusitanica Capello, 1868, along the Portuguese coast. J Sea Res 50(2–3):167–175
Corti M, Loy A, Cataudella S (1996) Form changes in the sea bass, Dicentrarchus labrax (Moronidae: Teleostei), after acclimation to freshwater: an analysis using shape coordinates. Environ Biol Fish 47(2):165–175
Dentry W, Lindsey C (1978) Vertebral variation in zebrafish (Brachydanio rerio) related to the prefertilization temperature history of their parents. Can J Zool 56(2):280–283
Ellis T, Howell B, Hayes J (1997) Morphological differences between wild and hatchery reared turbot. J Fish Biol 50(5):1124–1128
Engeszer RE, Patterson LB, Rao AA, Parichy DM (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4(1):21–40
Ferreri F, Nicolais C, Boglione C, Bmertoline B (2000) Skeletal characterization of wild and reared zebrafish: anomalies and meristic characters. J Fish Biol 56(5):1115–1128
Fowler J (1970) Control of vertebral number in teleosts-an embryological problem. Q Rev Biol 45(2):148–167
Froese R, Pauly D (2009) FishBase website, http://www.fishbase.org/Summary/SpeciesSummary.php?ID=4653. Accessed at 7 June 2010
Fuiman L, Batty R (1997) What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. J Exp Biol 200(12):1745
Georgakopoulou E, Sfakianakis DG, Kouttouki S, Divanach P, Kentouri M, Koumoundouros G (2007) The influence of temperature during early life on phenotypic expression at later ontogenetic stages in sea bass. J Fish Biol 70(1):278–291
Hard J, Berejikian B, Tezak E, Schroder S, Knudsen C, Parker L (2000) Evidence for morphometric differentiation of wild and captively reared adult coho salmon: a geometric analysis. Environ Biol Fish 58(1):61–73
Harder W (1975) Anatomy of fishes. Schweizerbart, Stuttgart
Ibañez-Aguirre AL, Lleonart J (1996) Relative growth and comparative morphometrics of Mugil cephalus L. and M. curema V. in the Gulf of Mexico. Sci Mar 60(2–3):361–368
Imre I, McLaughlin R, Noakes D (2002) Phenotypic plasticity in brook charr: changes in caudal fin induced by water flow. J Fish Biol 61(5):1171–1181
Johnston IA (1993) Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Mar Biol 116(3):363–379
Johnston IA (2006) Environment and plasticity of myogenesis in teleost fish. J Exp Biol 209(12):2249
Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T (2009) Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 212(12):1781
Junquera S, Perez-Gandaras G (1993) Population diversity in Bay of Biscay anchovy (Engraulis encrasicolus L. 1758) as revealed by multivariate analysis of morphometric and meristic characters. ICES J Mar Sci 50(4):383
Koumoundouros G, Ashton C, Sfakianakis DG, Divanach P, Kentouri M, Anthwal N, Stickland N (2009) Thermally induced phenotypic plasticity of swimming performance in European sea bass Dicentrarchus labrax juveniles. J Fish Biol 74(6):1309–1322
Koumoundouros G, Divanach P, Kentouri M (2001) The effect of rearing conditions on development of saddleback syndrome and caudal fin deformities in Dentex dentex (L.). Aquaculture 200(3–4):285–304
Koumoundouros G, Gagliardi F, Divanach P, Boglione C, Cataudella S, Kentouri M (1997) Normal and abnormal osteological development of caudal fin in Sparus aurata L. fry. Aquaculture 149(3–4):215–226
Koumoundouros G, Sfakianakis DG, Divanach P, Kentouri M (2002) Effect of temperature on swimming performance of sea bass juveniles. J Fish Biol 60(4):923–932
Lawrence C (2007) The husbandry of zebrafish (Danio rerio): a review. Aquaculture 269(1–4):1–20
Lein I, Holmefjord I, Rye M (1997) Effects of temperature on yolk sac larvae of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 157(1–2):123–135
Lindsey C, Ali M (1965) The effect of alternating temperature on vertebral count in the medaka (Oryzias latipes). Can J Zool 43(1):99–104
Lindsey CC (1988) Factors controlling meristic variation. Fish Physiol 11(part B):197–274
Mamuris Z, Apostolidis P, Panagiotaki P, Theodorou A, Triantaphyllidis C (1998) Morphological variation between red mullet populations in Greece. J Fish Biol 52(1):107–117
Matsuoka M (1987) Development of the skeletal tissues and skeletal muscles in the red sea bream (Pagrus major). Bull Seikai Reg Fish Res Lab 65:1–114
Murray C, Beacham T (1989) Responses of meristic characters in chum salmon (Oncorhynchus keta) to temperature changes during development. Can J Zool 67(3):596–600
Nathanailides C, Stickland N, Lopez-Albors O (1995) Influence of prehatch temperature on the development of muscle cellularity in posthatch Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 52(4):675–680
O'Reilly K, Horn M (2004) Phenotypic variation among populations of Atherinops affinis (Atherinopsidae) with insights from a geometric morphometric analysis. J Fish Biol 64(4):1117–1135
Pakkasmaa S, Piironen J (2001) Morphological differentiation among local trout (Salmo trutta) populations. Biol J Linn Soc 72(2):231–239
Parichy D, Elizondo M, Mills M, Gordon T, Engeszer R (2009) Normal table of postembryonic zebrafish development: Staging by externally visible anatomy of the living fish. Dev Dyn 238(12):2975–3015
Park E, Kim D (1984) A procedure for staining cartilage and bone of whole vertebrate larvae while rendering all other tissues transparent. Biotech Histochem 59(5):269–272
Plaut I, Gordon M (1994) Swimming metabolism of wild-type and cloned zebrafish Brachydanio rerio. J Exp Biol 194(1):209
Polo A, Yufera M, Pascual E (1991) Effects of temperature on egg and larval development of Sparus aurata L. Aquaculture 92:367–375
Salini J, Milton D, Rahman M, Hussain M (2004) Allozyme and morphological variation throughout the geographic range of the tropical shad, hilsa Tenualosa ilisha. Fish Res 66(1):53–69
Sfakianakis DG, Georgakopoulou E, Papadakis I, Divanach P, Kentouri M, Koumoundouros G (2006) Environmental determinants of haemal lordosis in European sea bass, Dicentrarchus labrax (Linnaeus, 1758). Aquaculture 254(1–4):54–64
Sfakianakis DG, Koumoundouros G, Anezaki L, Divanach P, Kentouri M (2003) Development of a saddleback-like syndrome in reared white seabream Diplodus sargus (Linnaeus, 1758). Aquaculture 217(1–4):673–676
Sfakianakis DG, Koumoundouros G, Divanach P, Kentouri M (2004) Osteological development of the vertebral column and of the fins in Pagellus erythrinus (L. 1758). Temperature effect on the developmental plasticity and morpho-anatomical abnormalities. Aquaculture 232(1–4):407–424
Sfakianakis DG, Leris I, Kentouri M (2011) Effect of developmental temperature on swimming performance of zebrafish (Danio rerio) juveniles. Environ Biol Fish 90(4):421–427. doi:10.1007/s10641-010-9751-5
Sokal R, Rohlf F (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, New York
Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc 83(1):13–34
Taning AV (1952) Experimental study of meristic characters in fishes. Biol Rev 27(2):169–193
Taylor WR, van Dyke GC (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium 9(2):107–119
Tudela S (1999) Morphological variability in a Mediterranean, genetically homogeneous population of the European anchovy, Engraulis encrasicolus. Fish Res 42(3):229–243
Turan C (2004) Stock identification of Mediterranean horse mackerel (Trachurus mediterraneus) using morphometric and meristic characters. ICES J Mar Sci 61(5):774
Turan C, Oral M, Öztürk B, Düzgüneş E (2006) Morphometric and meristic variation between stocks of Bluefish (Pomatomus saltatrix) in the Black, Marmara, Aegean and northeastern Mediterranean Seas. Fish Res 79(1–2):139–147
Vågsholm I, Djupvik HO (1998) Risk factors for spinal deformities in Atlantic salmon, Salmo salar L. J Fish Dis 21(1):47–53
Wang L, Tsai C (2000) Effects of temperature on the deformity and sex differentiation of tilapia, Oreochromis mossambicus. J Exp Zool 286(5):534–537
Westerfield M (1995) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene
Wiegand M, Hataley J, Kitchen C, Buchanan L (1989) Induction of developmental abnormalities in larval goldfish, Carassius auratus L., under cool incubation conditions. J Fish Biol 35(1):85–95
Wilkes D, Xie SQ, Stickland NC, Alami-Durante H, Kentouri M, Sterioti A, Koumoundouros G, Fauconneau B, Goldspink G (2001) Temperature and myogenic factor transcript levels during early development determines muscle growth potential in rainbow trout (Oncorhynchus mykiss) and sea bass (Dicentrarchus labrax). J Exp Biol 204(16):2763–2771
Wimberger PH (1992) Plasticity of fish body shape. The effects of diet, development, family and age in two species of Geophagus (Pisces; Cichlidae). Biol J Linn Soc 45(3):197–218
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The authors thank two anonymous reviewers for their helpful comments in producing the final manuscript. The present study was financed by the European Social Fund and National Resources (EPEAEK II–PYTHAGORAS I) to M.K.
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Sfakianakis, D.G., Leris, I., Laggis, A. et al. The effect of rearing temperature on body shape and meristic characters in zebrafish (Danio rerio) juveniles. Environ Biol Fish 92, 197–205 (2011). https://doi.org/10.1007/s10641-011-9833-z
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DOI: https://doi.org/10.1007/s10641-011-9833-z