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Defining length-at-metamorphosis in fishes: a multi-character approach

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Abstract

The present study attempts to highlight the value of multi-character approaches for defining thresholds in fish ontogeny, like the onset of the juvenile period. We developed techniques to objectively define the transition from larval to juvenile development using morphometric as well as morphological characters and exemplify the multi-character approach on newly settled white sea-breams (Diplodus sargus sargus) collected from the eastern Mediterranean. The morphometric analysis was based on principles of multivariate allometry whereas the analysis of morphology, on assigning a suite of selected characters (here related to external morphology and osteological development) into larval, transforming and juvenile states. The size-at-change in multivariate allometric growth (L m) is considered here to denote mean length-at-metamorphosis. An almost perfect match is demonstrated between L m (‘multivariate morphometry’) and mean size-at-morphological change (‘multivariate morphology’) in white sea-bream.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton 11:36–42

    Google Scholar 

  • Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25:19–22. doi:10.1007/s00338-005-0044-y

    Article  Google Scholar 

  • Balon EK (1999) Alternative ways to become a juvenile or a definitive phenotype (and on some persisting linguistic offenses). Environ Biol Fish 56:17–38. doi:10.1023/A:1007502209082

    Article  Google Scholar 

  • Boglione C, Giganti M, Selmo C, Cataudella S (2003) Morphoecology in larval fin-fish: a new candidate species for aquaculture, Diplodus puntazzo (Sparidae). Aquacult Int 11:17–41. doi:10.1023/A:1024119032359

    Article  CAS  Google Scholar 

  • Bradford MJ (1992) Precision of recruitment predictions from early life stages of marine fishes. Fish Bull 90:439–453

    Google Scholar 

  • Bryan PG, Madraisau BB (1977) Larval rearing and development of Siganus lineatus (Pisces: Siganidae) from hatching through metamorphosis. Aquaculture 10:243–252. doi:10.1016/0044-8486(77)90005-9

    Article  Google Scholar 

  • Cadrin SX (2000) Advances in morphometric identification of fishery stocks. Rev Fish Biol Fisher 10:91–112. doi:10.1023/A:1008939104413

    Article  Google Scholar 

  • Carr MH, Hixon MA (1995) Predation effects on early post-settlement survivorship of coral-reef fishes. Mar Ecol Prog Ser 124:31–42. doi:10.3354/meps124031

    Article  Google Scholar 

  • Copp GH, Kováč V (1996) When do fish with indirect development become juveniles? Can J Fish Aquat Sci 53:746–752. doi:10.1139/cjfas-53-4-74

    Article  Google Scholar 

  • Ditty JG, Fuiman LA, Shaw RF (2003) Characterizing natural intervals of development in fishes: an example using blennies (Teleostei: Blenniidae). In: The big fish bang: proceedings of the 26th annual larval fish conference, Bergen, pp 405–418

  • Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statist Sci 1:54–75. doi:10.1214/ss/1177013815

    Article  Google Scholar 

  • Elbal MT, Hernandez MPG, Lozano MT, Agulleiro B (2004) Development of the digestive tract of gilthead sea bream (Sparus aurata L.). Light and electron microscopic studies. Aquaculture 234:215–238. doi:10.1016/j.aquaculture.2003.11.028

    Article  Google Scholar 

  • Fryer RJ (1991) A model of between-haul variation in selectivity. ICES J Mar Sci 48:281–290. doi:10.1093/icesjms/48.3.281

    Article  Google Scholar 

  • Fuiman LA (1983) Growth gradients in fish larvae. J Fish Biol 23:117–123. doi:10.1111/j.1095-8649.1983.tb02886.x

    Article  Google Scholar 

  • Fuiman LA (1994) The interplay of ontogeny and scaling in the interactions of fish larvae and their predators. J Fish Biol 45((Suppl A)):55–79. doi:10.1006/jfbi.1994.1214

    Article  Google Scholar 

  • Fuiman LA (2002) Special considerations of fish eggs and larvae. In: Fuiman LA, Werger RG (eds) Fishery science: the unique contributions of early life stages. Blackwell Science, Oxford, pp 1–32

    Google Scholar 

  • Fuiman LA, Higgs DM (1997) Ontogeny, growth, and the recruitment process. In: Chambers RC, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman and Hall, London, pp 225–249

    Google Scholar 

  • Fuiman LA, Poling KR, Higgs DM (1998) Quantifying developmental progress for comparative studies of larval fishes. Copeia 3:602–611. doi:10.2307/1447790

    Article  Google Scholar 

  • Gisbert E, Merino G, Muguet JB, Bush D, Piedrahita RH, Conklin DE (2002) Morphological development and allometric growth patterns in hatchery-reared California halibut larvae. J Fish Biol 61:1217–1229. doi:10.1111/j.1095-8649.2002.tb02466.x

    Article  Google Scholar 

  • Gozlan RE, Copp GH, Tourenq JN (1999) Comparison of growth plasticity in the laboratory and field, and implications for the onset of juvenile development in sofie, Chondrostoma toxostoma. Environ Biol Fish 56:153–165. doi:10.1023/A:1007577321999

    Article  Google Scholar 

  • Higgs DM, Fuiman LA (1998) Associations between sensory development and ecology in three species of clupeoid fish. Copeia 1:133–144. doi:10.2307/1447709

    Article  Google Scholar 

  • Houde ED (1987) Fish early life dynamics and recruitment variability. In: 10th annual larval fish conference, Am Fish Soc Symp 2:17–29

  • Huxley J (1932) Problems of relative growth. New York Dial Press, New York

    Google Scholar 

  • Jolicoeur P (1963a) The multivariate generalization of the allometry equation. Biometrics 19:497–499. doi:10.2307/2527939

    Article  Google Scholar 

  • Jolicoeur P (1963b) The degree of generality of robustness in Martes americana. Growth 27:1–27

    Google Scholar 

  • Juanes F, Conover DO (1994) Rapid growth, high feeding rates, and early piscivory in young-of-the-year bluefish (Pomatomus saltatrix). Can J Fish Aquat Sci 51:1752–1761. doi:10.1139/f94-176

    Article  Google Scholar 

  • Kanou K, Kohno H, Sano M (2004) Morphological and functional development of characters associated with settlement in the yellowfin goby, Acanthogobius flavimanus. Ichthyol Res 51:213–221. doi:10.1007/s10228-004-0217-7

    Google Scholar 

  • Keefe M, Able KW (1993) Patterns of metamorphosis in summer flounder, Paralichthys dentatus. J Fish Biol 42:713–728. doi:10.1111/j.1095-8649.1993.tb00380.x

    Article  Google Scholar 

  • Klingenberg CP, Froese R (1991) A multivariate comparison of allometric growth patterns. Syst Zool 40:410–419. doi:10.2307/2992236

    Article  Google Scholar 

  • Koumoundouros G, Divanach P, Kentouri M (1999) Ontogeny and allometric plasticity of Dentex dentex (Osteichthyes: Sparidae) in rearing conditions. Mar Biol 135:561–572. doi:10.1007/s002270050657

    Article  Google Scholar 

  • Koumoundouros G, Divanach P, Anezaki L, Kentouri M (2001) Temperature-induced ontogenetic plasticity in sea bass (Dicentrarchus labrax). Mar Biol 139:817–830. doi:10.1007/s002270100635

    Article  Google Scholar 

  • Koumoundouros G, Ashton C, Giopanou I, Ksenikoudakis G, Georgakopoulou E, Stickland NC (2009) Ontogenetic differentiation of swimming performance in gilthead sea bream (Sparus aurata, Linnaeus 1758) during metamorphosis. J Exp Mar Biol Ecol 370:75–81. doi:10.1016/j.jembe.2008.12.001

    Article  Google Scholar 

  • Kováč V (2002) Synchrony and heterochrony in ontogeny (of fish). J Theor Biol 217:499–507. doi:10.1006/jtbi.2002.3043

    Article  PubMed  Google Scholar 

  • Kováč V, Copp GH (1999) Prelude: looking at early development in fishes. Environ Biol Fish 56:7–14. doi:10.1023/A:1007546711019

    Article  Google Scholar 

  • Kováč V, Copp GH, Francis MP (1999) Morphometry of the stone loach, Barbatula barbatula: do mensural characters reflect the species’ life history thresholds? Environ Biol Fish 56:105–115. doi:10.1023/A:1007570716690

    Article  Google Scholar 

  • Kováč V, Katina S, Copp GH, Siryova S (2006) Ontogenetic variability in external morphology and microhabitat use of spirlin Alburnoides bipunctatus from the River Rudava (Danube catchment). J Fish Biol 68:1257–1270. doi:10.1111/j.1095-8649.2006.01007.x

    Article  Google Scholar 

  • Leis JM (2006) Are larvae of demersal fishes plankton or nekton? Adv Mar Biol 51:57–141. doi:10.1016/S0065-2881(06)51002-8

    Article  PubMed  Google Scholar 

  • Loy A, Bertelletti M, Costa C, Ferlin L, Cataudella S (2001) Shape changes and growth trajectories in the early stages of three species of the genus Diplodus (Perciformes, Sparidae). J Morphol 250:24–33. doi:10.1002/jmor.1056

    Article  CAS  PubMed  Google Scholar 

  • Macpherson E, Biagi F, Francour P, Garcia-Rubies A, Harmelin J, Harmelin-Vivien M, Jouvenel JY, Planes S, Vigliola L, Tunesi L (1997) Mortality of juvenile fishes of the genus Diplodus in protected and unprotected areas in the western Mediterranean Sea. Mar Ecol Prog Ser 160:135–147. doi:10.3354/meps160135

    Article  Google Scholar 

  • McCormick MI, Makey L, Dufour V (2002) Comparative study of metamorphosis in tropical reef fishes. Mar Biol 141(5):841–853. doi:10.1007/s00227-002-0883-9

    Article  Google Scholar 

  • Nikolioudakis N, Kiparissis S, Koumoundouros G, Somarakis S (2007) Allometric somatic growth patterns and otolith shape changes in Diplodus sargus (Linnaeus, 1758) during metamorphosis. Rapp Comm Int Mer Medit 38:554

    Google Scholar 

  • Osse JWM, van den Boogaart JGM (1995) Fish larvae, development, allometric growth and the aquatic environment. ICES Mar Sci 201:21–34

    Google Scholar 

  • Park EH, Kim DS (1984) A procedure for staining cartilage and bone of whole vertebrate larvae while rendering all other tissues transparent. Stain Technol 59:269–272. doi:10.3109/10520298409113869

    CAS  PubMed  Google Scholar 

  • Petrakis G, Stergiou KI (1997) Size selectivity of diamond and square mesh codends for four commercial Mediterranean fish species. ICES J Mar Sci 54:13–23. doi:10.1006/jmsc.1996.0172

    Article  Google Scholar 

  • Russo T, Pulcini D, Bruner E, Cataudella S (2009) Shape and size variation: growth and development of the dusky grouper (Epinephelus marginatus Lowe, 1834). J Morphol 270:83–96. doi:10.1002/jmor.10674

    Article  PubMed  Google Scholar 

  • Sagnes P, Gaudin P, Statzner B (1997) Shifts in morphometrics and their relation to hydrodynamic potential and habitat use during grayling ontogenesis. J Fish Biol 50:846–858. doi:10.1006/jfbi.1996.0353

    Article  Google Scholar 

  • Sediva A, Kováč V, Copp GH (2000) Growth variability of morphometric characters in perch Perca fluviatilis and its relation to microhabitat use. Folia Zool 49:123–132

    Google Scholar 

  • 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 232:407–424. doi:10.1016/j.aquaculture.2003.08.014

    Article  Google Scholar 

  • Shea BT (1985) Bivariate and multivariate growth allometry: statistical and biological considerations. J Zool 206:367–390. doi:10.1111/j.1469-7998.1985.tb05665.x

    Article  Google Scholar 

  • Simonovič PD, Garner P, Eastwood EA, Kováč V, Copp GH (1999) Correspondence between ontogenetic shifts in morphology and habitat use in minnow Phoxinus phoxinus. Environ Biol Fish 56:117–128. doi:10.1023/A:1007541915307

    Article  Google Scholar 

  • Sissenwine MP (1984) Why do fish populations vary? In: May RM (ed) Exploitation of marine communities. Dahlem Konferenzen, New York, pp 59–94

    Google Scholar 

  • Smith PE (1985) Year class strength and survival of 0-group clupeoids. Can J Fish Aquat Sci 42:69–82. doi:10.1139/f85-263

    Article  Google Scholar 

  • Thorisson K (1994) Is metamorphosis a critical interval in the early life of marine fishes? Environ Biol Fish 40:23–36. doi:10.1007/BF00002180

    Article  Google Scholar 

  • Urho L (2002) Characters of larvae—what are they? Folia Zool 51:161–186

    Google Scholar 

  • van der Veer HW, Bergman MJN (1987) Predation by crustaceans on a newly settled 0-group plaice Pleuronectes platessa populations in the western Wadden Sea. Mar Ecol Prog Ser 35:203–215. doi:10.3354/meps035203

    Article  Google Scholar 

  • van Snik GMJ, van den Boogaart JGM, Osse JWM (1997) Larval growth patterns in Cyprinus caprio and Clarias gariepinus with the attention to the finfold. J Fish Biol 50:1339–1352. doi:10.1111/j.1095-8649.1997.tb01657.x

    Article  Google Scholar 

  • Vigliola L, Harmelin-Vivien M (2001) Post-settlement ontogeny in three Mediterranean reef fish species of the genus Diplodus. Bull Mar Sci 68:271–286

    Google Scholar 

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Acknowledgments

We thank the European Social Fund (ESF), Operational Program for Educational and Vocational Training II (EPEAEK II), and particularly the Program PYTHAGORAS II, for funding this work. The authors thank E. Schismenou, Dr. S. Isari and Dr. A. Ramfos for their assistance in field sampling and laboratory analysis, and E. Georgakopoulou for her help with fish staining. Acknowledgements are also given to Dr. U. Sommer and two other anonymous referees for valuable comments regarding this manuscript. This study fully complies with the current laws of Greece.

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Correspondence to Stylianos Somarakis.

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Communicated by D. Goulet.

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Nikolioudakis, N., Koumoundouros, G., Kiparissis, S. et al. Defining length-at-metamorphosis in fishes: a multi-character approach. Mar Biol 157, 991–1001 (2010). https://doi.org/10.1007/s00227-009-1379-7

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