Skip to main content
Log in

Linking growth patterns to sea temperature and oxygen levels across European sardine (Sardina pilchardus) populations

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The previously studied geographic variability in the growth patterns of different European sardine or European pilchard (Sardina pilchardus) populations has been attributed to the trophic status and productivity of the various ecosystems, as well as the genetic distance among populations. However, in the face of ocean warming and its multifaceted effects on marine populations and fisheries, it is interesting to explore growth patterns through the prism of sea temperature and dissolved oxygen. Here, data on the asymptotic length, growth coefficient, and maximum reported age of 47 Atlantic and Mediterranean sardine populations, covering the entire geographical range of its distribution, were extracted from published sources and were correlated with regional sea surface temperature and dissolved oxygen. Asymptotic length was negatively related to sea temperature and more strongly positively related to oxygen levels, indicating that sardines grow to larger body size in cooler waters that are more oxygenated. Within the context of climate change, the link of intraspecific growth variability with temperature and oxygen draws attention to the adverse effects this might have on many fish biological characteristics in a warming future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated and/or analysed during the current study are available by the authors upon reasonable request.

References

  • Akyol O, Tokac A, Unsal S (1996) An investigation on the growth and reproduction characteristics of the sardine (Sardina pilchardus Walbaum, 1792) in the Bay of Izmir (Aegean Sea). Su Urunleri Dergisi 13(3–4):383–394

    Google Scholar 

  • Alemany F, Álvarez F (1993) Growth differences among sardine (Sardina pilchardus Walb.) populations in Western Mediterranean. Sci Mar 57(2–3): 229–234.

  • Alheit J, Licandro P, Coombs S, Garcia A, Giraldez A, Santamaria MTG, Slotte A, Tsikliras AC (2014) Atlantic Multi-decadal Oscillation (AMO) modulates dynamics of small pelagic fishes and ecosystem regime shifts in the eastern North and Central Atlantic. J Mar Syst 131:21–35

    Article  Google Scholar 

  • Andreu B, Rodriguea-Roda J, Larrañeta MG (1950) Contribución al estudio de la talla, edad y crecimiento de la sardina (Sardina pilchardus Walb.) de las costas españolas de Lovante (Noviembre 1949-Mayo 1950). Publ Inst Biol Apl Barc 7:159–189

    Google Scholar 

  • Antonakakis K, Giannoulaki M, Machias A, Somarakis S, Sanchez S, Ibaibarriaga L, Uriarte A (2011) Assessment of the sardine (Sardina pilchardus Walbaum, 1792) fishery in the eastern Mediterranean basin (North Aegean Sea). Medit Mar Sci 12:333–357

    Article  Google Scholar 

  • Apostolidis C, Stergiou KI (2014) Estimation of growth parameters from published data for several Mediterranean fishes. J Appl Ichthyol 30:189–194

    Article  Google Scholar 

  • Arendt J (2007) Ecological correlates of body size in relation to cell size and cell number: patterns in flies, fish, fruits and foliage. Biol Rev Camb Philos Soc 82:241–256

    Article  PubMed  Google Scholar 

  • Assis J, Tyberghein L, Bosh S, Verbruggen H, Serrão EA, De Clerck O (2017) Bio-ORACLE v2.0: Extending marine data layers for bioclimatic modelling. Glob Ecol Biogeogr 27(3): 277–284.

  • Audzijonyte A, Barneche DR, Baudron AR, Belmaker J, Clark TD, Marshall CT, Morrongiello JR, van Rijn I (2019) Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Glob Ecol Biogeogr 28:64–77

    Article  Google Scholar 

  • Barraca I, Pestana G (1985) Growth studies, using scales of Sardina pilchardus (Walb.) in Portuguese waters (1979–1984). ICES C.M. /H:22.

  • Baudron AR, Needle CL, Rijndorp AD, Marshall CT (2014) Warming temperatures and smaller body sizes: synchronous changes in growth of North Sea fishes. Glob Change Biol 20:1023–1031

    Article  Google Scholar 

  • Bianchi CN, Morri C (2003) Global sea warming and “tropicalization” of the Mediterranean Sea: biogeographic and ecological aspects. Biogeographia 24:319–328

    Google Scholar 

  • Bouchereau JL, Djabali F, Do Chi T, Mouhoub R, Pastor X, Tomasini JA (1985) Essais d’évaluation de l’état d’exploitation des stocks de sardines dans les divisions statistiques Baléares et golfe du Lion, par quelques méthodes analytiques simples. FAO Fish Rep 347:163–185

    Google Scholar 

  • Bougis P (1952) La croissance des poissons méditerranéens. Vie Milieu Suppl 2:118–146

    Google Scholar 

  • Brahmi B, Bennoui A, Oualiken A (1998) Estimation de la croissance de la sardine (Sardina pilchardus, Walbaum, 1792) dans la région centre de la côte algerienne. Cah Opt Méd 35:57–64

    Google Scholar 

  • Brosset P, Fromentin JM, Van Beveren E, Lloret J, Marques V, Basilone G, Bonanno A, Carpi P, Donato F, Čikeš Keč V, De Felice A, Ferreri R, Gašparević D, Giráldez A, Gücü A, Iglesias M, Leonori I, Palomera I, Somarakis S, Tičina V, Torres P, Ventero A, Zorica B, Ménard F, Saraux C (2017) Spatio-temporal patterns and environmental controls of small pelagic fish body condition from contrasted Mediterranean areas. Prog Oceanogr 151:149–162

    Article  Google Scholar 

  • Butzin M, Pörtner H-O (2016) Thermal growth potential of Atlantic cod by the end of the 21st century. Glob Change Biol 22:4162–4168

    Article  Google Scholar 

  • Campillo A (1992) Les pêcheries françaises de Méditerranée: synthèse des connaissances. Institut Français de Recherche pour l'Exploitation de la Mer, France. 206

  • Cheung WWL, Lam VWY, Sarmiento JL, Kearney K, Watson R, Pauly D (2009) Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish 10:235–251

    Article  Google Scholar 

  • Cheung WWL, Lam VWY, Sarmiento JL, Kearney K, Watson R, Zeller D, Pauly D (2010) Large-scale redistribution of maximum fisheries catch potential in the global ocean under climate change. Glob Change Biol 16:24–35

    Article  Google Scholar 

  • Cheung WWL, Sarmiento JL, Dunne J, Fröhlicher TL, Lam VWY, Palomares MLD, Watson R, Pauly D (2013a) Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat Clim Chang 3:254–258

    Article  Google Scholar 

  • Cheung WWL, Watson R, Pauly D (2013b) Signature of ocean warming in global fisheries catch. Nature 497:365–368

    Article  CAS  PubMed  Google Scholar 

  • Colloca F, Cardinale M, Maynou F, Giannoulaki M, Scarcella G, Jenko K, Bellido JM, Fiorentino F (2013) Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability. Fish Fish 14:89–109

    Article  Google Scholar 

  • Coro G, Gonzalez Vilas L, Magliozzi C, Ellenbroek A, Scarponi P, Pagano P (2018) Forecasting the ongoing invasion of Lagocephalus sceleratus in the Mediterranean Sea. Ecol Model 371:37–49

    Article  Google Scholar 

  • Cury P, Pauly D (2000) Patterns and propensities in reproduction and growth of marine fishes. Ecol Res 15:101–106

    Article  Google Scholar 

  • D’Ancona U (1937) La croissance chez les animaux méditerranéens. Rapp P-V Réun CIEM 10:162–224

    Google Scholar 

  • Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci 106:12788–12793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado A, Fernandez MAR, Goni R (1981) Contribución al estudio de la sardina (Sardina pilchardus Walb.) en aguas de Africa Occidental. III. Estudio del crecimiento por lectura directa de otolitos y por retrocalculo mediante escalimetria de escamas. Bol Inst Esp Oceanogr 6:139–164

    Google Scholar 

  • Dimarchopoulou D, Makino M, Prayoga MR, Zeller D, Vianna GM, Humphries AT (2021) Responses in fisheries catch data to a warming ocean along a latitudinal gradient in the western Pacific Ocean. Environ Biol Fishes. https://doi.org/10.1007/s10641-021-01162-z

    Article  Google Scholar 

  • Djabali F, Boudraa S, Bouhdid A, Bousbia H, Bouchelaghem EH, Brahmi B, Dob M, Derdiche O, Djekrir F, Kadri L, Mammasse M, Stambouli A, Tehami B (1990) Travaux réalisés sur les stocks pélagiques et démersaux de la région de Béni-saf. FAO Fish Rep 447:160–165

    Google Scholar 

  • Fage L (1920) Engraulidae, Clupeidae. Report on the Danish Oceanographical Expeditions 1908–1919 to the Mediterranean and adjacent seas, vol. 2, no. 6. 140

  • Froese R, Pauly D (2021) FishBase. In: R. Froese & D. Pauly (Editors). World Wide Web electronic publication. www.fishbase.org, 15 July, 2021

  • Galil BS, Marchini A, Occhipinti-Ambrogi A (2018) East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea. Estuar Coast Shelf Sci 201:7–16

    Article  Google Scholar 

  • Gattuso J-P, Magnan A, Billee R, Cheung WWL, Howes EL, Joos F, Allemand D, Bopp L, Cooley SR, Eakin CM, Hoegh-Guldberg O, Kelly RP, Pörtner H-O, Rogers AD, Baxter JM, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila UR, Treyer S, Turley C (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:6243

    Article  Google Scholar 

  • GFCM (1981) Working party on resource appraisal and fishery statistics report of technical consultation on stock assessment in the Balearic and Gulf of Lions statistical divisions, Palma de Mallorca, Spain. FAO Fish Rep 227:1–151

    Google Scholar 

  • Golani D, Azzuro E, Dulčić J, Massuti E, Orsi-Relini L (2021) Atlas of exotic fishes in the Mediterranean Sea, 2ed edn. CIEM Publishers, Paris/Monaco, p 365

    Google Scholar 

  • Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9(2):228–241

    Article  PubMed  Google Scholar 

  • Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15:56–61

    Article  CAS  PubMed  Google Scholar 

  • Idrissi M (1987) Note sur la pêcherie des espèces pélagiques en Méditerranée. FAO Fish Rep 395:133–139

    Google Scholar 

  • James F (1970) Geographic size variation in birds and its relationship to climate. Ecology 51:365–390

    Article  Google Scholar 

  • Kartas F (1981) Les clupéidés de Tunisie. Caractéristiques biométriques et biologiques. Etude comparée des populations de l'Atlantique est et de la Méditerranée. Thèse de Doctorat d'Etat, Université de Tunis, Faculté des sciences, 608

  • Larrañeta G (1965) Les constantes de la croissance de la sardine de Castellón. Proc Gen Fish Coun Médit 8:273–276

    Google Scholar 

  • Larrañeta MG, Lopez J (1958) El crecimiento de la sardina (Sardina pilchardus Walb.) de las costas de Castellón. Invest Pesq 6:53–82

    Google Scholar 

  • Laskaridis K (1948) Study of the biology of the sardine (Clupea pilchardus Walb.) in Greek waters. Prakt Hellen Hydrobiol Inst 2:11–88

    Google Scholar 

  • Lee JY (1961) Le sardine du golfe du Lion (Sardina pilchardus sardina Regan). Rev Trav Inst Pêches Marit 25:417–512

    Google Scholar 

  • Lenoir J, Svenning J-C (2015) Climate-related range shifts – a global multidimensional synthesis and new research directions. Ecography 38:15–28

    Article  Google Scholar 

  • Levangie PEL, Blanchfield PJ, Hutchings JA (2021) The influence of ocean warming on the natural mortality of marine fishes. Environ Biol Fishes. https://doi.org/10.1007/s10641-021-01161-0

    Article  Google Scholar 

  • Lopez J (1963) Age de la sardine (Sardina pilchardus Wald.) de Barcelone. Proc Gen Fish Coun Mèdit 7:299–308

    Google Scholar 

  • Meyer KA, Schill DJ (2021) The Gill-Oxygen Limitation Theory and size at maturity/ maximum size relationships for salmonid populations occupying flowing waters. J Fish Biol 98:44–49

    Article  CAS  PubMed  Google Scholar 

  • Mouhoub R (1986) Contribution à l'étude de la dynamique de la population exploitée de la sardine (Sardina pilchardus, Walbaum, 1792) des côtes algéroises. USTHB. Alger. 163 p. Thèse de Magister.

  • Mozzi C, Duo A (1958) Croissance et âge des sardines de la Haute Adriatique débarquées à Chioggia. Tech Pap Gen Fish Coun Médit 5(10):1–15

    Google Scholar 

  • Muzinic R (1957) Sur la croissance de la jeune sardine (Sardina pilchardus Wald.) dans les eaux de Split. Biljeske, Split (12).

  • Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935

    Article  CAS  PubMed  Google Scholar 

  • Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026

    Article  CAS  Google Scholar 

  • Pauly D (1994) On the Sex of the Fish and the Gender of Scientists. Chapman and Hall, London, p 250

    Google Scholar 

  • Pauly D (1998) Tropical fishes: patterns and propensities. J Fish Biol 53(Suppl A):1–17

    Google Scholar 

  • Pauly D (2010) Gasping Fish and Panting Squids: Oxygen, Temperature and the Growth of Water-Breathing Animals. Excellence in Ecology (22), International Ecology Institute, Oldendorf/Luhe, Germany

  • Pauly D (2019) A précis of Gill-Oxygen Limitation Theory (GOLT), with some Emphasis on the Eastern Mediterranean. Medit Mar Sci 20 Special Issue: 660–668

  • Pauly D (2021) The gill-oxygen limitation theory (GOLT) and its critics. Sci Adv 7: eabc6050

  • Penas Lado E (1978) Estudio sobre la dinámica y la estrategia de explotacion del “stock” de sardina (Sardina pilchardus, Walbaum) de la costas de Castellón. Bol Inst Esp Oceanogr 4(3):143–160

    Google Scholar 

  • Perez N, Proteiro C, Alvarez F (1985) Contribucion al conocimiento de la biologia de la sardina de Galicia. Bol Inst Esp Oceanog 2:27–37

    Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate Change and Distribution Shifts in Marine Fishes. Science 308:1912–1915

    Article  CAS  PubMed  Google Scholar 

  • Porteiro C, Alvarez F (1985) Determinacion del crecimiento de la sardina, Sardina pilchardus, en aguas gallegas, mediante lectura directa de otolitos. Inst Esp Oceanog Informes Tecnicos, No. 14

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Article  PubMed  Google Scholar 

  • Rodriguez-Roda J, Larrañeta MG (1955) El crecimiento de la sardina (Sardina pilchardus Wald.) de mento de las costas de Alicante. Invest Pesq 2:9–20

    Google Scholar 

  • Sabatés A, Martín P, Lloret J, Raya V (2006) Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Glob Change Biol 12:2209–2219

    Article  Google Scholar 

  • Saraux C, Van Beveren E, Brosset P, Queiros Q Bourdeix J-H, Dutto G, Gasset E, Jac C, Bonhommeau S, Fromentin J-M (2019) Small pelagic fish dynamics: a review of mechanisms in the Gulf of Lions. Deep-Sea Res II 159: 52-61

  • Scientific, Technical and Economic Committee for Fisheries (STECF) (2013) 2012 Assessment of Mediterranean Sea stocks part II (STECF 13–05). Publications Office of the European Union, Luxembourg, EUR 25309 EN, JRC 81592, 618

  • Silva A, Carrera P, Masse J, Uriarte A, Santos MB, Oliveira PB, Soares E, Porteiro C, Stratoudakis Y (2008) Geographic variability of sardine growth across the northeastern Atlantic and the Mediterranean Sea. Fish Res 90:56–69

    Article  Google Scholar 

  • Sinovcic G (1983) Summary of biological parameters of sardine (Sardina pilchardus Walb.) from the central Adriatic. FAO Fish Rep 290:147–148

    Google Scholar 

  • Stergiou KI, Tsikliras AC, Pauly D (2009) Farming up the Mediterranean food webs. Conserv Biol 23:230–232

    Article  PubMed  Google Scholar 

  • Sumaila UR, Cheung WWL, Lam VWY, Pauly D, Herrick S (2011) Climate change impacts on the biophysics and economics of world fisheries. Nat Clim Chang 1:449–456

    Article  Google Scholar 

  • Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Chang 2:686–690

    Article  Google Scholar 

  • Tserpes G, Tsimenides N (1991) Evaluation of growth rate differences in populations of Sardina pilchardus (Walbaum 1792) (Clupeidae) from the Aegean and Ionian Seas. Cybium 15:15–22

    Google Scholar 

  • Tsikliras AC (2008) Climate-related geographic shift and sudden population increase of a small pelagic fish (Sardinella aurita) in the eastern Mediterranean Sea. Mar Biol Res 4:477–481

    Article  Google Scholar 

  • Tsikliras AC, Koutrakis ET (2013) Growth and reproduction of European sardine, Sardina pilchardus (Pisces: Clupeidae), in northeastern Mediterranean. Cah Biol Mar 54: 365–374

  • Tsikliras AC, Polymeros K (2014) Fish market prices drive overfishing of the 'big ones’. Peer J 2: e638

  • Tsikliras AC, Stergiou KI (2014) Mean temperature of the catch increases quickly in the Mediterranean Sea. Mar Ecol Progr Ser 515:281–284

    Article  Google Scholar 

  • Tsikliras AC, Peristeraki P, Tserpes G, Stergiou KI (2015) Mean temperature of the catch (MTC) in the Greek Seas based on landings and survey data. Front Mar Sci 2:23

    Article  Google Scholar 

  • Tsikliras AC, Licandro P, Pardalou A, McQuinn IH, Gröger JP, Alheit J (2019) Synchronization of Mediterranean pelagic fish populations with the North Atlantic climate variability. Deep-Sea Res II 159:143–151

    Article  Google Scholar 

  • Tyberghein L, Verbruggen H, Pauly K, Troupin C, Mineur F, De Clerck O (2012) Bio-ORACLE: A global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr 21:272–281

    Article  Google Scholar 

  • Ulman A, Yildiz T, Demirel N, Canak O, Yemişkend E, Pauly D (2021) The biology and ecology of the invasive silver-cheeked toadfish (Lagocephalus sceleratus), with emphasis on the Eastern Mediterranean. NeoBiota 68:145–175. https://doi.org/10.3897/neobiota.68.71767

    Article  Google Scholar 

  • Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH et al (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc r Soc b: Biol Sci 281:20140846

    Article  Google Scholar 

  • Voulgaridou P, Stergiou KI (2003) Trends in various biological parameters of the European sardine, Sardina pilchardus (Walbaum, 1792), in the Eastern Mediterranean Sea. Sci Mar 67: 269–280

Download references

Acknowledgements

We would like to thank Daniel Pauly for the useful suggestions he provided on the draft of this manuscript and two anonymous reviewers for their helpful comments and suggestions that improved our work.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Donna Dimarchopoulou or Athanassios C. Tsikliras.

Ethics declarations

Ethics approval

No approval of research ethics committees was required to accomplish the goals of this study because no experimental work was conducted.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dimarchopoulou, D., Tsikliras, A.C. Linking growth patterns to sea temperature and oxygen levels across European sardine (Sardina pilchardus) populations. Environ Biol Fish 105, 1335–1345 (2022). https://doi.org/10.1007/s10641-022-01229-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-022-01229-5

Keywords

Navigation