Environmental Biology of Fishes

, Volume 101, Issue 5, pp 775–789 | Cite as

Age-specific environmental differences on the otolith shape of the bastard grunt (Pomadasys incisus) in the north-western Mediterranean

  • H. Villegas-Hernández
  • J. Lloret
  • M. Muñoz
  • G. R. Poot-López
  • S. Guillén-Hernández
  • C. González-Salas
Article

Abstract

The effects of sex, age, and environment on the shape of the bastard grunt (Pomadasys incisus) otoliths from the north-western Mediterranean were investigated. Specimens of this species were collected from two separate sampling areas in the north-western Mediterranean with different thermal regimes. Sex, growth rates, and age of P. incisus were determined by using gonad histology techniques, biometric analyses, and otolith microstructure analyses, respectively. The shape was described using normalized Elliptic Fourier descriptors (EFDs), and studied by means of multivariate statistics as predictive variables with age-specific discriminant analyses. There were no consistent differences found between sexes, but otolith shapes varied significantly between environments within different age classes. Total classification success varied between 87.3% and 89.2% between environments for the different age classes and provided a phenotypic basis for P. incisus population separation within an environmental gradient in determining its otolith shape. In addition, significant differences were observed between sampling areas in von Bertalanffy’s growth parameters, as well as in the fish length-weight (LWR) and fish length-otolith radius (TL-Ro) relationships. Data was discussed considering that the physical habitat variability could underlie a marked change in otolith shape during the animals’ growth. In this matter, we discussed the relative importance of both ontogenetic and environmental conditions (such as water temperature) on otolith shape.

Keywords

Pomadasys incises Age Otolith shape Fourier analysis Spatial variation 

Notes

Acknowledgements

The authors would like to thank the Abertis Foundation for the financial support given to this research (Ref. 1018-100305-00) and the University of Girona for further financial support (R + D ASING2011, Ref. SING11/10). Our sincere thanks to the IRTA research centre (particularly to Guiomar Rotllant and Rosa Trobajo) for their assistance during sampling. Finally, Harold Villegas-Hernandez would like to thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) in Mexico for the scholarship (Ref. 215050) that has enabled him to pursue his PhD studies at the University of Girona.

References

  1. Agüera A, Brophy D (2011) Use of saggital otolith shape analysis to discriminate Northeast Atlantic and Western Mediterranean stocks of Atlantic saury, Scomberesox saurus saurus (Walbaum). Fish Res 110(3):465–471.  https://doi.org/10.1016/j.fishres.2011.06.003 CrossRefGoogle Scholar
  2. Anderson MJ (2005) Permanova: a fortran computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, AucklandGoogle Scholar
  3. Annabi A, Said K, Reichenbacher B (2013) Inter-population differences in otolith morphology are genetically encoded in the killifish Aphanius fasciatus (Cyprinodontiformes). Sci Mar 77(2):269–279.  https://doi.org/10.3989/scimar.03763.02A CrossRefGoogle Scholar
  4. Ballagh AC, Welch D, Williams AJ et al (2011) Integrating methods for determining length-at-age to improve growth estimates for two large scombrids. Fish Bull 109:90–100Google Scholar
  5. Bănaru D, Mellon-Duval C, Roos D, Bigot JL, Souplet A, Jadaud A, Beaubrun P, Fromentin JM (2013) Trophic structure in the Gulf of Lions marine ecosystem (north-western Mediterranean Sea) and fishing impacts. J Mar Syst 111–112:45–68.  https://doi.org/10.1016/j.jmarsys.2012.09.010 CrossRefGoogle Scholar
  6. Beamish RJ, Fournier DA (1981) A method for comparing the precision of a set of age determinations. Can J Fish Aquat Sci 38(8):982–983.  https://doi.org/10.1139/f81-132 CrossRefGoogle Scholar
  7. Begg GA, Brown R (2000) Stock identification of haddock Melanogramus aeglefinus on Georges Bank based on otolith shape analysis. Trans Am Fish Soc 129(4):935–945.  https://doi.org/10.1577/1548-8659(2000)129<0935:SIOHMA>2.3.CO;2 CrossRefGoogle Scholar
  8. Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43(1-3):35–44.  https://doi.org/10.1016/S0165-7836(99)00065-X CrossRefGoogle Scholar
  9. Begg GA, Friedland KD, Pearce JB (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fish Res 43(1-3):1–8.  https://doi.org/10.1016/S0165-7836(99)00062-4 CrossRefGoogle Scholar
  10. Begg GA, Overholtz WJ, Munroe NJ (2000) The use of internal otolith morphometrics for identification of haddock (Melanogramus aeglefinus) stocks on Georges Bank. Fish Bull 99:1–14Google Scholar
  11. Beyer SG, Szedlmayer ST (2010) The use of otolith shape analysis for ageing juvenile red snapper, Lutjanus campechanus. Environ Biol Fish 89(3-4):333–340.  https://doi.org/10.1007/s10641-010-9684-z CrossRefGoogle Scholar
  12. Bodilis P, Crocetta F, Langeneck J, Francour P (2013) The spread of an Atlantic fish species, Pomadasys incisus (Bowdich, 1825) (Osteichthyes: Haemulidae), within the Mediterranean Sea with new additional records from the French Mediterranean coast. Ital J Zool 80(2):273–278.  https://doi.org/10.1080/11250003.2012.730555 CrossRefGoogle Scholar
  13. Bolle LJ, Begg GA (2000) Distinctions between silver hake (Merluccius bilinearis) stocks in U.S. waters of the northwest Atlantic based on whole otolith morphometric. Fish Bull 98:451–462Google Scholar
  14. Bosc E, Bricaoud A, Antoine D (2004) Seasonal and interannual variability in algal biomass and primary production in the Mediterranean Sea, as derived from 4 years of SeaWiFS observations. Glob Biogeochem Cycles 18(1):1–17.  https://doi.org/10.1029/2003GB002034 CrossRefGoogle Scholar
  15. Bowdich SL (1825) Fishes of Madeira. p. 121-125, 233-238. In: Bowdich TE (ed) Excursions in Madeira and Porto Santo during the autumn of 1823, while on his third voyage to Africa, London, p 278Google Scholar
  16. Cadrin SX, Friedland KD (1999) The utility of image processing techniques for morphometric analysis and stock identification. Fish Res 43(1-3):129–139.  https://doi.org/10.1016/S0165-7836(99)00070-3 CrossRefGoogle Scholar
  17. Campana SE, Casselman JM (1993) Stock discrimination using otolith shape analysis. Can J Fish Aquat Sci 50(5):1062–1083.  https://doi.org/10.1139/f93-123 CrossRefGoogle Scholar
  18. Capoccioni F, Costa C, Aguzzi J et al (2011) Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. J Exp Mar Bio Ecol 397(1):1–7.  https://doi.org/10.1016/j.jembe.2010.11.011 CrossRefGoogle Scholar
  19. Cardinale M, Doering-Arjes P, Kastowsky M, Mosegaard H (2004) Effects of sex, stock, and environment on the shape of known-age Atlantic cod (Gadus morhua) otoliths. Can J Fish Aquat Sci 61(2):158–167.  https://doi.org/10.1139/f03-151 CrossRefGoogle Scholar
  20. Castonguay M, Simard P, Gagnon P (1991) Usefulness of Fourier analysis of otolith shape for Atlantic mackerel (Scomber scombrus) stock discrimination. Can J Fish Aquat Sci 48:296–302CrossRefGoogle Scholar
  21. Chakroun-Marzouk N, Ktari MH (2006) Caractéristiques de la reproduction et de la croissance pondérale relative de Pomadasys incisus (Haemulidae) du golfe de Tunis. Cybium 30:333–342Google Scholar
  22. Chater I, Romdhani A, Dufour JL et al (2015) Otolith growth and age estimation of bastard grunt, Pomadasys incisus (Actinopterygii: Perciformes: Haemulidae), in the Gulf of tunis (central mediterranean). Acta Ichthyol Piscat 45(1):57–64.  https://doi.org/10.3750/AIP2015.45.1.06 CrossRefGoogle Scholar
  23. Coll M, Palomera I, Tudela S, Sardà F (2006) Trophic flows, ecosystem structure and fishing impacts in the South Catalan Sea, Northwestern Mediterranean. J Mar Syst 59(1-2):63–96.  https://doi.org/10.1016/j.jmarsys.2005.09.001 CrossRefGoogle Scholar
  24. Doering-Arjes P, Cardinale M, Mosegaard H (2008) Estimating population age structure using otolith morphometrics: a test with known-age Atlantic cod (Gadus morhua) individuals. Can J Fish Aquat Sci 65:2342–2350CrossRefGoogle Scholar
  25. FAO (2013) Fisheries and aquaculture software. FISAT II - FAO-ICLARM Stock Assessment Tool. In: FAO Fisheries and Aquaculture Department [online]. Rome. Updated 28 November 2013. [Cited 30 January 2018]. http://www.fao.org/fishery/
  26. Francour P, Boudouresque CF, Harmelin JG, Harmelin-Vivien ML, Quignard JP (1994) Are the Mediterranean waters becoming warmer? Information from biological indicators. Mar Pollut Bull 28(9):523–526.  https://doi.org/10.1016/0025-326X(94)90071-X CrossRefGoogle Scholar
  27. Friedland KD, Reddin DG (1994) Use of otolith morphology in stock discriminations of Atlantic salmon (Salmon salar). Can J Fish Aquat Sci 51(1):91–98.  https://doi.org/10.1139/f94-011 CrossRefGoogle Scholar
  28. Gagliano M, McCormick MI (2004) Feeding history influences otolith shape in tropical fish. Mar Ecol Prog Ser 278:291–296.  https://doi.org/10.3354/meps278291 CrossRefGoogle Scholar
  29. Galley EA, Wright PJ, Gibb FM (2006) Combined methods of otolith shape analysis improve identification of spawning areas of Atlantic cod. ICES J Mar Sci 63(9):1710–1717.  https://doi.org/10.1016/j.icesjms.2006.06.014 CrossRefGoogle Scholar
  30. Gauldie RW (1990) A measure of metabolisms in fish otoliths. Comp Biochem Physiol 97(4):475–480.  https://doi.org/10.1016/0300-9629(90)90113-7 CrossRefGoogle Scholar
  31. Gauldie RW, Nelson DGA (1990) Otolith growth in fishes. Comp Biochem Physiol 97(2):119–135.  https://doi.org/10.1016/0300-9629(90)90159-P CrossRefGoogle Scholar
  32. Gayanilo FC Jr, Sparre P, Pauly D (2005) FAO-ICLARM stock assessment tools II (FiSAT II). User’s guide. FAO Computerized Information Series (Fisheries). No. 8, Revised version. FAO, Rome, p 168Google Scholar
  33. Hüssy K (2008) Otolith shape in juvenile cod (Gadus morhua): ontogenetic and environmental effects. J Exp Mar Bio Ecol 364(1):35–41.  https://doi.org/10.1016/j.jembe.2008.06.026 CrossRefGoogle Scholar
  34. Hüssy K, Mosegaard H, Albertsen CM et al (2016) Evaluation of otolith shape as a tool for stock discrimination in marine fishes using Baltic Sea cod as a case study. Fish Res 174:210–218.  https://doi.org/10.1016/j.fishres.2015.10.010 CrossRefGoogle Scholar
  35. Iwata H, Ukai Y (2002) Shape: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. J Hered 93(5):384–385.  https://doi.org/10.1093/jhered/93.5.384 CrossRefPubMedGoogle Scholar
  36. Jónsdóttir IG, Campana SE, Marteinsdottir G (2006) Otolith shape and temporal stability of spawning groups of Icelandic cod (Gadus morhua L.) ICES J Mar Sci 63(8):1501–1512.  https://doi.org/10.1016/j.icesjms.2006.05.006 CrossRefGoogle Scholar
  37. Kimura DK (1980) Likelihood methods for the von Bertalanffy growth curve. Fish Bull:765–776Google Scholar
  38. Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comput Graph Image Process 18(3):236–258.  https://doi.org/10.1016/0146-664X(82)90034-X CrossRefGoogle Scholar
  39. Libungan LA, Slotte A, Husebø Å et al (2015) Latitudinal gradient in otolith shape among local populations of Atlantic herring (Clupea harengus L.) in Norway. PLoS One 10(6):1–15.  https://doi.org/10.1371/journal.pone.0130847 CrossRefGoogle Scholar
  40. Lombarte A, Lleonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fish 37(3):297–306.  https://doi.org/10.1007/BF00004637 CrossRefGoogle Scholar
  41. Mardia KV (1970) Measures of multivariate skewness and kurtosis with applications. Biometrika 36:519–530CrossRefGoogle Scholar
  42. Mosegaard H, Svedang H, Taberman K (1988) Uncoupling of somatic and otolith growth rates in Arctic char (Salvelinus alpinus) as an effect of differences in temperature response. Can J Fish Aquat Sci 45:1514–1524CrossRefGoogle Scholar
  43. Munro JL, Pauly D (1983) A simple method for comparing growth of fishes and invertebrates. Fishbyte 1:5–6Google Scholar
  44. Pajuelo JG, Lorenzo JM, Gregoire M (2003) Age and growth of the bastard grunt (Pomadasys incisus Haemulidae) inhabiting the Canarian archipelago, Northwest Africa. Fish Bull 101:851–859Google Scholar
  45. Pastor J, Astruch P, Prats E et al (2008) Premières observations en plongée de Pomadasys incisus (Haemulidae) sur la côte catalane française. Cybium 32:185–186Google Scholar
  46. Pothin K, Gonzalez-Salas C, Chabanet P, Lecomte-Finiger R (2006) Distinction between Mulloidichthys flavolineatus juveniles from Reunion Island and Mauritius Island (south-west Indian Ocean) based on otolith morphometrics. J Fish Biol 69(1):38–53.  https://doi.org/10.1111/j.1095-8649.2006.01047.x CrossRefGoogle Scholar
  47. Psomadakis PN, Giustino S, Vacchi M (2012) Mediterranean fish biodiversity: an updated inventory with focus on the Ligurian and Tyrrhenian seas. Zootaxa 3263:1–46Google Scholar
  48. Reichenbacher B, Kamrani E, Esmaeili HR, Teimori A (2009) The endangered cyprinodont Aphanius Ginaonis (Holly, 1929) from southern Iran is a valid species: evidence from otolith morphology. Environ Biol Fish 86(4):507–521.  https://doi.org/10.1007/s10641-009-9549-5 CrossRefGoogle Scholar
  49. Renaud S, Michaux J, Jeager JJ, Auffray JC (1996) Fourier analysis applied to Stephanomys (Rodentia: Muridae) molars: nonprogresive evolutionary pattern in a gradual lineage. Paleobiology 22(02):255–265.  https://doi.org/10.1017/S0094837300016201 CrossRefGoogle Scholar
  50. Reznick D, Lindbeck E, Bryga H (1989) Slower growth results in larger otoliths: an experimental test with guppies (Poecilia reticulata). Can J Fish Aquat Sci 46:108–112CrossRefGoogle Scholar
  51. Ricker WE (1973) Linear regressions in fishery research. J Fish Res Board Canada 30(3):409–434.  https://doi.org/10.1139/f73-072 CrossRefGoogle Scholar
  52. Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bulletin 191 of the Fisheries Research Board of Canada, p 400Google Scholar
  53. Salat J, Garcia MA, Cruzado A, Palanques A, Arı́n L, Gomis D, Guillén J, de León A, Puigdefàbregas J, Sospedra J, Velásquez ZR (2002) Seasonal changes of water mass structure and shelf slope exchanges at the Ebro shelf (NW Mediterranean). Cont Shelf Res 22(2):327–348.  https://doi.org/10.1016/S0278-4343(01)00031-0 CrossRefGoogle Scholar
  54. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675.  https://doi.org/10.1038/nmeth.2089 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Secor DH, Dean JM (1989) Somatic growth effects on the otolith—fish size relationship in young pond-reared striped bass, Morone saxatilis. Can J Fish Aquat Sci 46(1):113–121.  https://doi.org/10.1139/f89-015 CrossRefGoogle Scholar
  56. Simoneau M, Casselman JM, Fortin R (2000) Determining the effect of negative allometry (length/height relationship) on variation in otolith shape in lake trout (Salvelinus namaycush), using Fourier-series analysis. Can J Zool 78(9):1597–1603.  https://doi.org/10.1139/cjz-78-9-1597 CrossRefGoogle Scholar
  57. Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman and Company. 887 p., New YorkGoogle Scholar
  58. Stransky C, Murta AG, Schlickeisen J, Zimmermann C (2008) Otolith shape analysis as a tool for stock separation of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean. Fish Res 89(2):159–166.  https://doi.org/10.1016/j.fishres.2007.09.017 CrossRefGoogle Scholar
  59. Suyama S, Oshima K, Nakagami M, Ueno Y (2009) Seasonal change in the relationship between otolith radius and body length in age-zero Pacific saury Cololabis saira. Fish Sci 75(2):325–333.  https://doi.org/10.1007/s12562-008-0039-z CrossRefGoogle Scholar
  60. Titus K, Mosher JA, Williams BK (1984) Chance-corrected classification for use in discriminate analysis: ecological applications. Am Midl Nat 111:1–7, 1, 1, DOI:  https://doi.org/10.2307/2425535
  61. Vignon M, Morat F (2010) Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Mar Ecol Prog Ser 411:231–241.  https://doi.org/10.3354/meps08651 CrossRefGoogle Scholar
  62. Villegas-Hernández H, Lloret J, Muñoz M (2015) Climate-driven changes in life-history traits of the bastard grunt Pomadasys incisus (Teleostei: Haemulidae) in the north-western Mediterranean. Mediterr Mar Sci 16(1):21–30.  https://doi.org/10.12681/mms.951 CrossRefGoogle Scholar
  63. Wilson DT, Mccormick MI (1997) Spatial and temporal validation of settlement marks in the otoliths of tropical reef fishes. Mar Ecol Prog Ser 153:259–271.  https://doi.org/10.3354/meps153259 CrossRefGoogle Scholar
  64. Zar JH (1996) Biostatistical analysis. Prentice-Hall, Inc. 662 p., Upper Saddle RiverGoogle Scholar

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Authors and Affiliations

  1. 1.Departamento de Biología MarinaUniversidad Autónoma de YucatánMéridaMexico
  2. 2.Faculty of Sciences, Institute of Aquatic EcologyUniversity of GironaGironaSpain

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