Effects of habitat conditions at hatching time on growth history of offspring European anchovy, Engraulis encrasicolus, in the Central Mediterranean Sea

The knowledge of the growth history in young fishes represents an important aspect of fishery ecology. This is especially relevant in short-living species like European anchovy, since they suffer a high mortality rate in their early life stages until recruitment. Although it is well known that habitat condition significantly affects spawning dynamics of fishes, it is not yet clear if these conditions affect growth trajectories during the early life stage’s critical period. Otolith microstructure analysis has been proven a useful tool to back-calculate growth history of young fishes. Thus, we analysed the effect of habitat variability on their growth history using otolith microstructures and environmental variables obtained from satellite imagery. Growth trajectories in juvenile anchovies, collected in two recruitment surveys carried out in 2004 and 2005 in the Strait of Sicily, were characterized by means of three indices within the fast growing period: the maximum increment width, the mean value of increment width, and the time extension of the fast growing period. Obtained results evidenced a clear effect of environmental conditions, particularly of sea surface temperature and chlorophyll-a concentration, on the growth histories of juveniles of anchovy. Furthermore, delayed effects of environmental conditions at hatching time on the forthcoming growth dynamics were discussed.

[1]  A. Bonanno,et al.  Influence of environmental variability on anchovy early life stages (Engraulis encrasicolus) in two different areas of the Central Mediterranean Sea , 2012, Hydrobiologia.

[2]  F. Alemany,et al.  Postflexion larvae and juvenile daily growth patterns of the Alborán Sea sardine (Sardina pilchardus Walb.): influence of wind , 2006 .

[3]  G. Champalbert,et al.  Feeding Behaviour and Trophic Environment of Engraulis encrasicolus (L.) in the Bay of Biscay , 1999 .

[4]  P. Blanchfield,et al.  Growth and feeding efficiency of wild and aquaculture genotypes of rainbow trout (Oncorhynchus mykiss) common to Lake Huron, Canada , 2014 .

[5]  E.,et al.  Chemistry and composition of fish otoliths : pathways , mechanisms and applications , 2006 .

[6]  R. Francis,et al.  Back‐calculation of fish length: a critical review , 1990 .

[7]  P. Grønkjær.  Otoliths as individual indicators: a reappraisal of the link between fish physiology and otolith characteristics , 2016 .

[8]  Otolith microstructure examination and analysis , 1993 .

[9]  W. E. Ricker,et al.  11 – Growth Rates and Models , 1979 .

[10]  I. Aoki,et al.  Environmental determinants of growth rates for larval Japanese anchovy Engraulis japonicus in different waters , 2006 .

[11]  M. Bradford,et al.  Interannual variability in stage-specific survival rates and the causes of recruitment variation , 1997 .

[12]  J. Hjort,et al.  Fluctuations in the Great Fisheries of Northern Europe: Viewed in the Light of Biological Research , 1914 .

[13]  E. Tjørve,et al.  The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family , 2017, PloS one.

[14]  R. Voss,et al.  Variability of larval Baltic sprat (Sprattus sprattus L.) otolith growth: a modeling approach combining spatially and temporally resolved biotic and abiotic environmental key variables , 2010 .

[15]  M. Mesa,et al.  Growth and mortality rates of European anchovy (Engraulis encrasicolus) in the Adriatic Sea during the transition from larval to juvenile stages , 2009 .

[16]  Yoshirô Watanabe,et al.  Growth of larval and early juvenile Japanese anchovy, Engraulis japonicus, in the Kuroshio‐Oyashio transition region , 2001 .

[17]  D. Jerry,et al.  Candidate growth genes in finfish — Where should we be looking? , 2007 .

[18]  J. Anderson.  A Review of Size Dependant Survival During Pre-recruit Stages of Fishes in Relation to Recruitment , 1988 .

[19]  S. Somarakis,et al.  Trophodynamics of anchovy in a non-upwelling system: direct comparison with sardine , 2014 .

[20]  Bernardo Spagnolo,et al.  PICOPHYTOPLANKTON DYNAMICS IN NOISY MARINE ENVIRONMENT , 2012 .

[21]  B. Morales-Nin,et al.  Setting up interpretation criteria for ageing juvenile european anchovy otoliths , 2008 .

[22]  I. Palomera,et al.  Seasonal comparison of the diets of juvenile European anchovy Engraulis encrasicolus and sardine Sardina pilchardus in the Gulf of Lions , 2014 .

[23]  X. Irigoien,et al.  Validation of daily increments deposition in the otoliths of European anchovy larvae (Engraulis encrasicolus L.) reared under different temperature conditions , 2008 .

[24]  K. Able,et al.  Relationships between otolith microstructure, otolith growth, somatic growth and ontogenetic transitions in two cohorts of windowpane , 2001 .

[25]  A. Cuttitta,et al.  Effect of habitat conditions on reproduction of the European anchovy (Engraulis encrasicolus) in the Strait of Sicily , 2006 .

[26]  P. Álvarez,et al.  Validation of daily increments in the otolith microstructure of Northeast Atlantic mackerel fish larvae , 2008 .

[27]  J. Dulčić.  Growth of anchovy, Engraulis encrasicolus (L.), larvae in the Northern Adriatic Sea , 1997 .

[28]  S. Campana,et al.  Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods , 2001 .

[29]  A. Folkvord,et al.  Temperature dependent otolith growth of larval and early juvenile Atlantic cod (Gadus morhua) , 2002 .

[30]  U. Cotano,et al.  Validation of age determination using otoliths of the European anchovy (Engraulis encrasicolus L.) in the Bay of Biscay , 2016 .

[31]  Manuel O. Nevárez-Martínez,et al.  Growth and hatching dates of juvenile pacific sardine Sardinops caeruleus in the Gulf of California , 2000 .

[32]  Javier Delgado,et al.  Hydrographic phenomena influencing early life stages of the Sicilian Channel anchovy , 2002 .

[33]  Giuseppa Buscaino,et al.  Habitat Selection Response of Small Pelagic Fish in Different Environments. Two Examples from the Oligotrophic Mediterranean Sea , 2014, PloS one.

[34]  J. Zweifel,et al.  PREHATCH AND POSTHATCH GROWTH OF FISHES­ A GENERAL MODEL , 1976 .

[35]  A. Cuttitta,et al.  Linking habitat conditions and growth in the European anchovy (Engraulis encrasicolus) , 2004 .

[36]  U. Cotano,et al.  Validation of the first annual increment deposition in the otoliths of European anchovy in the Bay of Biscay based on otolith microstructure analysis , 2016 .

[37]  M. Kentouri,et al.  Temperature-induced ontogenetic plasticity in sea bass (Dicentrarchuslabrax) , 2001 .

[38]  B. Morales-Nin,et al.  Juvenile European anchovy otolith microstructure , 2006 .

[39]  A. Cuttitta,et al.  Spawning site selection by European anchovy (Engraulis encrasicolus) in relation to oceanographic conditions in the Strait of Sicily , 2013 .

[40]  Jordi Lleonart,et al.  Fish stock assessments in the Mediterranean: state of the art , 2003 .

[41]  E. Moksness,et al.  Temperature-dependent otolith growth in Norwegian spring-spawning herring (Clupea harengus L.) larvae , 2004 .

[42]  M. Begon,et al.  Ecology: From Individuals to Ecosystems , 2005 .

[43]  S. Campana.  Otolith science entering the 21st century , 2005 .

[44]  L. Fuiman,et al.  Quantifying Developmental Progress for Comparative Studies of Larval Fishes , 1998 .

[45]  P. Petitgas,et al.  The selection process from larval to juvenile stages of anchovy (Engraulis encrasicolus) in the Bay of Biscay investigated by Lagrangian simulations and comparative otolith growth , 2003 .

[46]  J. Miquel,et al.  Characterizing the potential habitat of European anchovy Engraulis encrasicolus in the Mediterranean Sea, at different life stages , 2013 .

[47]  W. C. Leggett,et al.  Experimental evidence for selection against fish larvae with high metabolic rates in a food limited environment , 2005 .

[48]  Hui-Lun Chen,et al.  Effects of water temperature, salinity and feeding regimes on metamorphosis, growth and otolith Sr:Ca ratios of Megalops cyprinoides leptocephali , 2008 .

[49]  K. Able,et al.  Patterns of metamorphosis in summer flounder, Paralichthys dentatus , 1993 .

[50]  J. G. Field,et al.  Impact of environmental factors on survival of larval and juvenile Cape anchovy Engraulis encrasicolus (G.) in the southern Benguela upwelling region, determined from hatchdate distributions: implications for recruitment , 2005 .

[51]  G. Triantafyllou,et al.  Seasonal changes in growth and condition of anchovy late larvae explained with a hydrodynamic-biogeochemical model simulation , 2013 .

[52]  D. P. Fey.  The effect of temperature and somatic growth on otolith growth : the discrepancy between two clupeid species from a similar environment , 2006 .

[53]  C. Fulton,et al.  All in the ears: unlocking the early life history biology and spatial ecology of fishes , 2016, Biological reviews of the Cambridge Philosophical Society.

[54]  G. Triantafyllou,et al.  Disentangling the effects of inherent otolith growth and model-simulated ecosystem parameters on the daily growth rate of young anchovies , 2014 .

[55]  J. Herrmann,et al.  A novel length back-calculation approach accounting for ontogenetic changes in the fish length – otolith size relationship during the early life of sprat (Sprattus sprattus) , 2012 .

[56]  S. Mazzola,et al.  Application of GAMs and multinomial models to assess the spawning pattern of fishes with daily spawning synchronicity: A case study in the European anchovy (Engraulis encrasicolus) in the central Mediterranean Sea , 2015 .

[57]  E. Fanelli,et al.  Spatial variations in feeding habits and trophic levels of two small pelagic fish species in the central Mediterranean Sea. , 2016, Marine environmental research.

[58]  Astrid Jarre,et al.  Small pelagics in upwelling systems: patterns of interaction and structural changes in "wasp-waist" ecosystems , 2000 .

[59]  S. C. Weeker.  HABITAT SELECTION. , 1964, Scientific American.

[60]  S. Somarakis,et al.  Oceanographic habitat, growth and mortality of larval anchovy (Engraulis encrasicolus) in the northern Aegean Sea (eastern Mediterranean) , 2007 .

[61]  Motomitsu Takahashi,et al.  Growth rate-dependent recruitment of Japanese anchovy Engraulis japonicus in the Kuroshio-Oyashio transitional waters , 2004 .

[62]  M. Peck,et al.  Calibrating and comparing somatic-, nucleic acid-, and otolith-based indicators of growth and condition in young juvenile European sprat (Sprattus sprattus) , 2015 .

[63]  J. S. Rogers,et al.  Otolith record of age, growth, and ontogeny in larval and pelagic juvenile Stephanolepishispidus (Pisces: Monacanthidae) , 2001 .

[64]  R. Lough,et al.  Ontogenetic and seasonal trends in recent growth rates of Atlantic cod and haddock larvae on Georges Bank: effects of photoperiod and temperature , 2006 .

[65]  S. Campana.  How Reliable are Growth Back-Calculations Based on Otoliths? , 1990 .

[66]  A. Temming,et al.  Temperature-induced regional and temporal growth differences in Baltic young-of-the-year sprat Sprattus sprattus , 2006 .

[67]  M. Waldron.  Evidence of reduced growth rates of anchovy recruits off South Africa in 1989 and 1991 , 1995 .

[68]  A. Cuttitta,et al.  Factors structuring reproductive habitat suitability of Engraulis encrasicolus in the south coast of Sicily , 2006 .

[69]  G. Tserpes,et al.  The Alarming Decline of Mediterranean Fish Stocks , 2014, Current Biology.

[70]  X. Irigoien,et al.  Growth and movement patterns of early juvenile European anchovy (Engraulis encrasicolus L.) in the Bay of Biscay based on otolith microstructure and chemistry , 2010 .

[71]  B. Morales-Nin,et al.  Larval growth of anchovy, Engraulis encrasicolus, in the Western Mediterranean Sea , 1988 .

[72]  S. Campana,et al.  Microstructure of Fish Otoliths , 1985 .

[73]  G. Triantafyllou,et al.  Seasonal changes in otolith increment width trajectories and the effect of temperature on the daily growth rate of young sardines , 2016 .

[74]  Bruno Buongiorno Nardelli,et al.  Environmental processes driving anchovy and sardine distribution in a highly variable environment: the role of the coastal structure and riverine input , 2016 .

[75]  F. Alemany,et al.  Birthdate analysis and its application to the study of recruitment of the Atlanta­ Iberian sardine Sardina pilchardus , 1997 .

[76]  Giuseppa Buscaino,et al.  Space utilization by key species of the pelagic fish community in an upwelling ecosystem of the Mediterranean Sea , 2017, Hydrobiologia.

[77]  Salvatore Aronica,et al.  European anchovy (Engraulis encrasicolus) age structure and growth rate in two contrasted areas of the Mediterranean Sea: the paradox of faster growth in oligotrophic seas , 2017 .