Explorative analysis on red mullet (<em>Mullus barbatus</em>) ageing data variability in the Mediterranean

Pierluigi Carbonara; Walter Zupa; Aikaterini Anastasopoulou; Andrea Bellodi; Isabella Bitetto; Charis Charilaou; Archontia Chatzispyrou; Romain Elleboode; Antonio Esteban; Maria Cristina Follesa; Igor Isajlovic; Angélique Jadaud; Cristina García-Ruiz; Amalia Giannakaki; Beatriz Guijarro; Sotiris Elias Kiparissis; Alessandro Ligas; Kelig Mahé; Andrea Massaro; Damir Medvesek; Chryssi Mytilineou; Francesc Ordines; Paola Pesci; Cristina Porcu; Panagiota Peristeraki; Ioannis Thasitis; Pedro Torres; Maria Teresa Spedicato; Angelo Tursi; Letizia Sion

doi:10.3989/scimar.04999.19A

Authors

Pierluigi Carbonara COISPA Tecnologia and Ricerca, Stazione Sperimentale per lo Studio delle Risorse del Mare https://orcid.org/0000-0002-2529-2535
Walter Zupa COISPA Tecnologia and Ricerca, Stazione Sperimentale per lo Studio delle Risorse del Mare https://orcid.org/0000-0002-2058-8652
Aikaterini Anastasopoulou Hellenic Centre for Marine Research https://orcid.org/0000-0003-0872-6984
Andrea Bellodi Department of Life and Environmental Sciences, University of Cagliari https://orcid.org/0000-0002-9017-1692
Isabella Bitetto COISPA Tecnologia and Ricerca, Stazione Sperimentale per lo Studio delle Risorse del Mare https://orcid.org/0000-0002-8497-1642
Charis Charilaou Department of Fisheries and Marine Research, Ministry of Agriculture, Rural Development and Environment https://orcid.org/0000-0002-5510-7265
Archontia Chatzispyrou Hellenic Centre for Marine Research https://orcid.org/0000-0003-1603-8524
Romain Elleboode French Research Institute for Exploitation of the Sea (Ifremer) https://orcid.org/0000-0001-9084-0895
Antonio Esteban Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Murcia https://orcid.org/0000-0002-2896-7972
Maria Cristina Follesa Department of Life and Environmental Sciences, University of Cagliari https://orcid.org/0000-0001-8320-9974
Igor Isajlovic Institute of Oceanography and Fisheries Split https://orcid.org/0000-0001-7101-9575
Angélique Jadaud MARBEC, Ifremer, Univ Montpellier, CNRS https://orcid.org/0000-0001-6858-3570
Cristina García-Ruiz Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Málaga https://orcid.org/0000-0003-2767-4200
Amalia Giannakaki Hellenic Center for Marine Research, Institute of Marine Biological Resources and Inland Waters https://orcid.org/0000-0001-5436-991X
Beatriz Guijarro Intituto Español de Oceanografía, Centre Oceanogràfic de les Balears https://orcid.org/0000-0002-2083-4681
Sotiris Elias Kiparissis Hellenic Agricultural Organization-DEMETER, Fisheries Research Institute of Kavala https://orcid.org/0000-0002-0587-8889
Alessandro Ligas Centro Interuniversitario di Biologia Marina ed Ecologia Applicata https://orcid.org/0000-0003-1036-3553
Kelig Mahé French Research Institute for Exploitation of the Sea (Ifremer) https://orcid.org/0000-0002-6506-211X
Andrea Massaro APLYSIA https://orcid.org/0000-0001-9224-3883
Damir Medvesek Institute of Oceanography and Fisheries Split https://orcid.org/0000-0002-3869-8550
Chryssi Mytilineou Hellenic Centre for Marine Research https://orcid.org/0000-0002-9326-1650
Francesc Ordines Intituto Español de Oceanografía, Centre Oceanogràfic de les Balears https://orcid.org/0000-0002-2456-2214
Paola Pesci Department of Life and Environmental Sciences, University of Cagliari https://orcid.org/0000-0002-9066-8076
Cristina Porcu Department of Life and Environmental Sciences, University of Cagliari https://orcid.org/0000-0003-2649-6502
Panagiota Peristeraki Hellenic Center for Marine Research - University of Crete, Biology Department https://orcid.org/0000-0002-8608-078X
Ioannis Thasitis Department of Fisheries and Marine Research, Ministry of Agriculture, Rural Development and Environment https://orcid.org/0000-0002-0940-2212
Pedro Torres Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Málaga https://orcid.org/0000-0002-7076-6023
Maria Teresa Spedicato COISPA Tecnologia and Ricerca, Stazione Sperimentale per lo Studio delle Risorse del Mare https://orcid.org/0000-0001-9939-9426
Angelo Tursi University of Bari Aldo Moro (UNIBA), Department of Biology https://orcid.org/0000-0002-7776-2738
Letizia Sion University of Bari Aldo Moro (UNIBA), Department of Biology https://orcid.org/0000-0002-0308-1841

DOI:

https://doi.org/10.3989/scimar.04999.19A

Keywords:

Mullus barbatus, age variability, MEDITS, Mediterranean, reader effect, false rings, date of birth

Abstract

The uncertainty in age estimation by otolith reading may be at the root of the large variability in red mullet (Mullus barbatus) growth models in the Mediterranean. In the MEDITS survey, red mullet age data are produced following the same sampling protocol and otolith reading methodology. However, ageing is assigned using different interpretation schemes, including variations in theoretical birthdate and number of false rings considered, in addition to differences in the experience level of readers. The present work analysed the influence of these variations and the geographical location of sampling on red mullet ageing using a multivariate approach (principal component analysis). Reader experience was the most important parameter correlated with the variability. The number of rings considered false showed a significant effect on the variability in the first age groups but had less influence on the older ones. The effect of the theoretical birthdate was low in all age groups. Geographical location had a significant influence, with longitude showing greater effects than latitude. In light of these results, workshops, exchanges and the adoption of a common ageing protocol based on age validation studies are considered fundamental tools for improving precision in red mullet ageing.

Downloads

Download data is not yet available.

References

Abdi H., Williams L.J. 2010. Principal component analysis. WIREs Computational Statistics 2: 433-459. https://doi.org/10.1002/wics.101

Anonymous. 2017. MEDITS-Handbook. Version nº 9. MEDITS Working Group, 106 pp. http://www.sibm.it/MEDITS%202011/principaledownload. htm

Appelberg M., Formigo N., Geffen A.J., et al. 2005. A cooperative effort to exchange age reading experience and protocols between European fish institutes. Fish. Res. 76: 167-173. https://doi.org/10.1016/j.fishres.2005.06.001

Beamish R.J., McFarlane G.A. 1995. A discussion of the importance of ageing error, and an application to walleye Pollock: the world's largest fishery. In: Secor D.H., Dean J.M. et al. (eds), Recent developments in fish otolith research. Univ. South Carolina Press, Columbia, pp. 545-565.

Bianchini M.L., Ragonese S. 2011. Establishing length-at-age references in the red mullet, Mullus barbatus L. 1758 (Pisces, Mullidae), a case study for growth assessments in the Mediterranean geographical sub-areas (GSA). Mediterr. Mar. Sci. 12: 316-332. https://doi.org/10.12681/mms.35

Campana S.E. 2001. Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J. Fish Biol. 59: 197-242. https://doi.org/10.1111/j.1095-8649.2001.tb00127.x

Carbonara P., Intini S., Modugno E., et al. 2015. Reproductive biology characteristics of red mullet (Mullus barbatus L., 1758) in Southern Adriatic Sea and management implications. Aquat. Living Resour. 28: 21-31. https://doi.org/10.1051/alr/2015005

Carbonara P., Intini S., Kolitari J., et al. 2018. A holistic approach to the age validation of Mullus barbatus L., 1758 in the Southern Adriatic Sea (Central Mediterranean). Sci. Rep. 8: 13219. https://doi.org/10.1038/s41598-018-30872-1 PMid:30185811 PMCid:PMC6125484

Coggins L.G., Gwinn D.C., Allen M.S. 2013. Evaluation of Age- Length Key Sample Sizes Required to Estimate Fish Total Mortality and Growth. Trans. Am. Fish. Soc. 142: 832-840. https://doi.org/10.1080/00028487.2013.768550

Corrales X., Ofir E., Coll M., et al. 2017. Modeling the role and impact of alien species and fisheries on the Israeli marine continental shelf ecosystem. J. Mar. Syst. 170: 88-102. https://doi.org/10.1016/j.jmarsys.2017.02.004

Düzbastilar F.O., Laleli T., Özgül A., et al. 2015. Determining the severity of skin injuries of red mullet, Mullus barbatus (Actinopterygii: Perciformes: Mullidae), inflicted during escape from trawl codend. Acta Ichthyol. Piscat. 45: 75-83. https://doi.org/10.3750/AIP2015.45.1.08

Edelist D., Golani D., Spanier E. 2014. First implementation of the Large Fish Index (LFI) in the eastern Mediterranean. Sci. Mar. 78: 185-192. https://doi.org/10.3989/scimar.03936.26A

Eero M., Hjelm J., Behrens J., et al. 2015. Eastern Baltic cod in distress: biological changes and challenges for stock assessment. ICES J. Mar. Sci. 72: 2180-2186. https://doi.org/10.1093/icesjms/fsv109

Fiorentino F., Zamboni A., Rossi M., et al. 1998. The growth of the Red Mullet (Mullus barbatus, L. 1758) during the first years of life in the Ligurian Sea (Mediterranean). CHIEAM-Options Mediterr. 35: 65-78.

Fiorentino F., Gancitano V., Gancitano S., et al. 2013. An updated two phase growth model for demersal fish with an application to red mullet (Mullus barbatus L., 1758) (Perciformes Mullidae) of the Mediterranean. Naturalista Sicil. S. IV, XXXVII: 529-542.

Fishstat. 2016. Fisheries and aquaculture software. FishStat Plus - Universal software for fishery statistical time series. FAO Fisher. Aquac. Dep. Rome. Updated 14 September 2017. [Cited 10 October 2019]. http://www.fao.org/fishery/statistics/software/fishstat/en

Hüssy K., Radtke K., Plikshs M., et al. 2016. Challenging ICES age estimation protocols: lessons learned from the eastern Baltic cod stock. ICES J. Mar. Sci. 73: 2138-2149. https://doi.org/10.1093/icesjms/fsw107

ICES. 2009. Report of the Workshop on Age Reading of Red mullet Mullus barbatus and Striped mullet Mullus surmuletus (WKACM), 30 March - 3 April 2009, Boulogne sur Mer, France. ICES CM 2009ACOM:44, 42 pp.

ICES. 2011a. Report of the Workshop of National Age Readings Coordinators (WKNARC), 5-9 September 2011, Boulogne-sur- Mer, France. ICES CM 2011/ACOM:45, 175 pp.

ICES. 2011b. Report of the Planning Group on Commercial Catches, Discards and Biological Sampling (PGCCDBS), 7 - 11 February 2011, Vienna, Austria. ICES CM 2011/ACOM:40, 174 pp.

ICES. 2012 Report of the Workshop on Age Reading of Red Mullet and Striped Red Mullet (WKACM), 2-6 July 2012, Boulogne sur Mer, France. ICES CM 2012ACOM: 60, 52 pp.

ICES. 2013. Report of the Second Workshop of National Age Readings Coordinators (WKNARC2), 13 - 17 May 2013, Horta, Azores. ICES CM 2013/ACOM:52, 65 pp.

ICES. 2017a. Workshop on Ageing Validation methodology of Mullus species (WKVALMU), 15-19 May 2017, Conversano, Italy. ICES CM 2017/ SSGIEOM:31, 74 pp.

ICES. 2017b. Report of the Workshop on Age estimation of European anchovy (Engraulis encrasicolus). WKARA2 2016 Report 28 November - 2 December 2016. Pasaia, Spain. ICES CM 2016/SSGIEOM:17, 223 pp.

ICES. 2018. Working Group on Biological Parameters (WGBIOP), 1-5 October 2018. Ghent, Belgium. ICES CM 2018/EOSG:07, 186 pp.

Jolliffe I.T. 2002. Principal Component Analysis. Second Edition, Springer Series in Statistics, 487 pp.

Kassambara A. 2017. Practical Guide To Principal Component Methods in R: PCA, M (CA), FAMD, MFA, HCPC, factoextra (Vol. 2). Statistical tools for high-throughput data analysis - STHDA, 169 pp.

Kaiser H.F. 1960. The Application of Electronic Computers to Factor Analysis. Educ. Psichol. Meas. 20: 141-151. https://doi.org/10.1177/001316446002000116

Kimura D.K., Anderl D.M. 2005 Quality control of age data at Alaska Science Center. Mar. Freshwater Res. 56: 783-789. https://doi.org/10.1071/MF04141

Kimura D.K., Lyons J.J. 1991. Between-Reader Bias and Variability in the Age-Determination Process. Fish. Bull. 89: 53-60.

Lê S., Josse J., Husson F. 2008. FactoMineR: An R Package for Multivariate Analysis. J. Stat. Softw. 25. https://doi.org/10.18637/jss.v025.i01

Liao H., Sharov A.F., Jones C.M., et al. 2013. Quantifying the Effects of Aging Bias in Atlantic Striped Bass Stock Assessment. Trans. Am. Fish. Soc. 142: 193-207. https://doi.org/10.1080/00028487.2012.705255

Mahé K., Elleboode R., Charilaou C., et al. 2012. Striped red mullet (Mullus surmuletus) and red mullet (M. barbatus) otolith and scale exchange 2011. Ifremer 30 pp.

Mahé K., Anastasopoulou A., Bekas P., et al. 2016. Report of the Striped red mullet (Mullus surmuletus) and Red mullet (Mullus barbatus) Exchange 2016. Ifremer 21 pp. https://archimer.ifremer.fr/doc/00348/45922/45615.pdf

Mati?-Skoko S., ?egvi?-Bubi? T., Mandi? I., et al. 2018. Evidence of subtle genetic structure in the sympatric species Mullus barbatus and Mullus surmuletus (Linnaeus, 1758) in the Mediterranean Sea. Sci. Rep. 8: 676. https://doi.org/10.1038/s41598-017-18503-7 PMid:29330368 PMCid:PMC5766513

Morales-Nin B., Panfili J. 2002. Specific age estimation. In: Panfili J., Troadec H., et al. (eds), Manual of fish sclerochronology. Ifremer-IRD coedition, Brest, France.

Moutin T., Raimbault P. 2002. Primary production, carbon export and nutrients availability in western and eastern Mediterranean Sea in early summer 1996 (MINOS cruise). J. Mar. Syst. 33-34: 273-288. https://doi.org/10.1016/S0924-7963(02)00062-3

Punt A.E., Smith D.C., KrusicGolub K., et al. 2008. Quantifying age-reading error for use in fisheries stock assessments, with application to species in Australia's southern and eastern scalefish and shark fishery. Can. J. Fish. Aquat. Sci. 65: 1991-2005. https://doi.org/10.1139/F08-111

R Development Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

Reeves S.A. 2003. A simulation study of the implications of age-reading errors for stock assessment and management advice. ICES J. Mar. Sci. 60: 314-328. https://doi.org/10.1016/S1054-3139(03)00011-0

Rude N.P., Hintz W.D., Norman J.D., et al. 2013. Using pectoral fin rays as a non lethal aging structure for smallmouth bass: precision with otolith age estimates and the importance of reader experience. J. Freshwater Ecol. 28: 2-199. https://doi.org/10.1080/02705060.2012.738253

Saborido-Rey F., Kjesbu O.S. 2005. Growth and maturation dynamics. 26 pp.

Sieli G., Badalucco C., Di Stefano G., et al. 2011, Biology of red mullet, Mullus barbatus (L. 1758), in the Gulf of Castellammare (NW Sicily, Mediterranean Sea) subject to a trawling ban. J. Appl. Ichthyol. 27: 1218-1225. https://doi.org/10.1111/j.1439-0426.2011.01784.x

Smith B.J., Dembkowski D.J., James D.A., et al. 2016. A Simple Method to Reduce Interpretation Error of Ages Estimated from Otoliths. Open Fish Sci. J. 9: 1-7. https://doi.org/10.2174/1874401X01609010001

Sonin O., Spanier E., Levi D., et al. 2007. Nanism (dwarfism) in fish: a comparison between red mullet Mullus barbatus from the southeastern and the central Mediterranean. Mar. Ecol. Prog. Ser. 343: 221-228. https://doi.org/10.3354/meps06917

Scientific Technical and Economic Committee for Fisheries (STECF). 2017. 54th Plenary Meeting Report (PLEN-17-01). Publ. Offi. Europ. Union, Luxembourg; EUR 28569 EN

Tursi A., Matarrese A., D'Onghia G., et al. 1994. Population biology of red mullet (Mullus barbatus L.) from the Ionian Sea. Mar. Life 4: 33-43.

Vrantzas N., Kalagia M., Karlou C. 1992. Age, growth and state of stock of red mullet (Mullus barbatus L. 1758) in the Saronikos Gulf of Greece. FAO Fish. Rep. 477: 51-67.