Advertisement

Marine Biology

, 163:240 | Cite as

Can pathogens alter the population dynamics of sardine in the NW Mediterranean?

  • Elisabeth Van Beveren
  • Nicolas Keck
  • Jean-Marc Fromentin
  • Stéphanie Laurence
  • Hélène Boulet
  • Sophie Labrut
  • Marine Baud
  • Laurent Bigarré
  • Pablo Brosset
  • Claire SarauxEmail author
Original paper

Abstract

Sardine populations worldwide can fluctuate drastically over short time periods, in terms of both biomass and biological characteristics. Fluctuations might be amplified by pathogens, but such hypotheses have never been considered in the absence of clear macroscopic symptoms. In the Gulf of Lions (NW Mediterranean), an enduring severe decrease in sardine (Sardina pilchardus) size, condition and age has been observed since 2008, resulting in a strong decline in landings. This situation might have been caused or aggravated by diseases, especially as other drivers such as fisheries are not expected to be important. Therefore, we developed and performed a general veterinary study, aimed at detecting a wide range of potential pathogens, including parasites, viruses and bacteria. We explored which infectious agents are most likely to produce a causal relationship with sardine health, important information for future infection experiments. Among about 1300 sardines sampled during June 2014–July 2015, microscopic parasites (often trematodes and coccidians) and bacteria Tenacibaculum and Vibrio spp. were found. However, no clear damage to tissue was observed and there was generally no link between the agents’ presence and host size or condition, so that no strong indications of pathogenicity were present. Nonetheless, 54 % of the sardines analysed in 2015 had elevated quantities of melano-macrophage centres (macrophage aggregates), indicating stress on the fish that might potentially be related to starvation and/or pollution.

Keywords

Vibrio Fish Condition Sardina Pilchardus Sardine Population Lean Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to acknowledge J.-F. Bernardet (Institut National de la Recherche Agronomique) for the characterisation of Tenacibaculum, J.-C. Raymond (Comité National des Pêches Maritimes et des Elevages Marins) for his useful comments on the results and the manuscript and D. Duplisea (Fisheries and Oceans Canada) for the thorough language editing. We also thank the captain and the crew of the RV “L’Europe” as well as all the scientists on board for their assistance during the PELMED surveys. PELMED surveys are cofinanced by Europe through the Data Collection Framework. Our gratitude is extended as well to the MEDITS team and the fishermen who provided us with sardine samples. We would also like to thank the two anonymous reviewers, whose suggestions greatly improved the manuscript. This work is a part of the programme EcoPelGol (Study of the Pelagic ecosystem in the Gulf of Lions), financed by France Filière Pêche (FFP).

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests or conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2016_3015_MOESM1_ESM.pdf (311 kb)
Supplementary material 1 (PDF 311 kb)

References

  1. Abollo E, Calvo M, Pascual S (2001) Hepatic coccidiosis of the blue whiting, Micromesistius poutassou (Risso), and horse mackerel, Trachurus trachurus (L.), from Galician waters. J Fish Dis 24:335–343. doi: 10.1046/j.1365-2761.2001.00298.x CrossRefGoogle Scholar
  2. Agius C (1979) The role of melano-macrophage centres in iron storage in normal and diseased fish. J Fish Dis 2:337–343. doi: 10.1111/j.1365-2761.1979.tb00175.x CrossRefGoogle Scholar
  3. Agius C, Roberts RJ (1981) Effects of starvation on the melano-macrophage centres of fish. J Fish Biol 19:161–169. doi: 10.1111/j.1095-8649.1981.tb05820.x CrossRefGoogle Scholar
  4. Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509CrossRefGoogle Scholar
  5. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178. doi: 10.1111/j.1937-2817.2010.tb01236.x CrossRefGoogle Scholar
  6. Bakke TA, Harris PD (1998) Diseases and parasites in wild Atlantic salmon (Salmo salar) populations. Can J Fish Aquat Sci 55:247–266. doi: 10.1139/cjfas-55-S1-247 CrossRefGoogle Scholar
  7. Baldwin RE, Banks MA, Jacobson KC (2011) Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax). Rev Fish Biol Fish 22:137–156. doi: 10.1007/s11160-011-9227-5 CrossRefGoogle Scholar
  8. Balebona MC, Zorrilla I, Moriñigo MA, Borrego JJ (1998) Survey of bacterial pathologies affecting farmed gilt-head sea bream (Sparus aurata L.) in southwestern Spain from 1990 to 1996. Aquaculture 166:19–35. doi: 10.1016/S0044-8486(98)00282-8 CrossRefGoogle Scholar
  9. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-10. http://CRAN.Rproject.org/package=lme4
  10. Baud M, Cabon J, Salomoni A et al (2015) First generic one step real-time Taqman RT-PCR targeting the RNA1 of betanodaviruses. J Virol Methods 211:1–7. doi: 10.1016/j.jviromet.2014.09.016 CrossRefGoogle Scholar
  11. Baumgartner TR, Soutar A, Ferreira-Bartrina V (1992) Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep 33:24–40Google Scholar
  12. Brosset P, Fromentin J-M, Ménard F et al (2014) Measurement and analysis of small pelagic fish condition: a suitable method for rapid evaluation in the field. J Exp Mar Biol Ecol 462:90–97. doi: 10.1016/j.jembe.2014.10.016 CrossRefGoogle Scholar
  13. Brosset P, Ménard F, Fromentin J-M et al (2015) Influence of environmental variability and age on the body condition of small pelagic fish in the Gulf of Lions. Mar Ecol Prog Ser 529:219–231. doi: 10.3354/meps11275 CrossRefGoogle Scholar
  14. Brosset P, Le Bourg B, Costalago D et al (2016) Linking small pelagic dietary shifts with ecosystem changes in the Gulf of Lions. Mar Ecol Prog Ser 554:157–171. doi: 10.3354/meps11796 CrossRefGoogle Scholar
  15. Brown CL, George CT (1985) Age-dependent accumulation of macrophage aggregates in the yellow perch Perca flavescens (Mitchell). J Fish Dis 8:135–138CrossRefGoogle Scholar
  16. Carli A, Pane L, Casareto L et al (1993) Occurrence of Vibrio alginolyticus in Ligurian coast rock pools (Tyrrhenian Sea, Italy) and its association with the copepod Tigriopus fulvus (Fisher 1860). Appl Environ Microbiol 59:1960–1962Google Scholar
  17. Cavallero S, Magnabosco C, Civettini M et al (2015) Survey of Anisakis sp and Hysterothylacium sp in sardines and anchovies from the North Adriatic Sea. Int J Food Microbiol 200:18–21. doi: 10.1016/j.ijfoodmicro.2015.01.017 CrossRefGoogle Scholar
  18. Checkley D, Alheit J, Oozeki Y, Roy C (2009) Climate change and small pelagic fish. Cambridge University Press, New YorkCrossRefGoogle Scholar
  19. Colorni A, Paperna I, Gordin H (1981) Bacterial infections in gilt-head sea bream Sparus aurata cultured at Elat. Aquaculture 23:257–267. doi: 10.1016/0044-8486(81)90019-3 CrossRefGoogle Scholar
  20. Costa G, MacKenzie K (1994) Histopathology of Goussia clupearum (Protozoa: Apicomplexa: Coccidia) in some marine fish from Scottish waters. Dis Aquat Organ 18:192–202CrossRefGoogle Scholar
  21. Crockford M, Jones JB, McColl K, Whittington RJ (2008) Comparison of three molecular methods for the detection of pilchard herpesvirus in archived paraffin-embedded tissue and frozen tissue. Dis Aquat Organ 82:37–44. doi: 10.3354/dao01965 CrossRefGoogle Scholar
  22. Cury P, Bakun A, Crawford RJM et al (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci 57:603–618. doi: 10.1006/jmsc.2000.0712 CrossRefGoogle Scholar
  23. Elotmani F, Assobhei O (2004) In vitro inhibition of microbial flora of fish by nisin and lactoperoxidase system. Lett Appl Microbiol 38:60–65. doi: 10.1046/j.1472-765X.2003.01441.x CrossRefGoogle Scholar
  24. Faílde LD, Losada AP, Bermúdez R et al (2013) Tenacibaculum maritimum infection: pathology and immunohistochemistry in experimentally challenged turbot (Psetta maxima L.). Microb Pathog 65:82–88. doi: 10.1016/j.micpath.2013.09.003 CrossRefGoogle Scholar
  25. Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (2006) The prokaryotes: Vol. 6: proteobacteria: Gamma Subclass, 3rd edn. Springer, SingaporeGoogle Scholar
  26. Ferrer-Maza D, Lloret J, Muñoz M et al (2016) Links between parasitism, energy reserves and fecundity of European anchovy, Engraulis encrasicolus, in the northwestern Mediterranean Sea. Conserv Physiol 4:cov069. doi: 10.1093/conphys/cov069 CrossRefGoogle Scholar
  27. Fournie JW, Summers KJ, Courtney LA, Virginia DE (2001) Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J Aquat Anim Health 13:105–116CrossRefGoogle Scholar
  28. González-Kother P, González MT (2014) The first report of liver coccidian Goussia cruciata in jack mackerel, Trachurus murphyi, from the South Pacific and its relationship with host variables. Parasitol Res 113:3903–3907. doi: 10.1007/s00436-014-4134-z CrossRefGoogle Scholar
  29. Harmelin MV, Mahe K, Bodiguel X, Mellon C (2012) Possible link between prey quality, condition and growth of juvenile hake (Merluccius merluccius) in the Gulf of Lions (NW Mediterranean). Cybium 36:323–328Google Scholar
  30. Jarre A, Hutchings L, Kirkman SP et al (2015) Synthesis: climate effects on biodiversity, abundance and distribution of marine organisms in the Benguela. Fish Oceanogr 24:122–149. doi: 10.1111/fog.12086 CrossRefGoogle Scholar
  31. Jones JB, Hyatt AD, Hine PM et al (1997) Australasian pilchard mortalities. World J Microbiol Biotechnol 13:383–392. doi: 10.1023/A:1018568031621 CrossRefGoogle Scholar
  32. Kent M (1990) Hand-held instrument for fat/water determination in whole fish. Food Control 1:47–53. doi: 10.1016/0956-7135(90)90121-R CrossRefGoogle Scholar
  33. Lafferty KD (2013) Parasites in Marine Food Webs. Bull Mar Sci 89:123–134. doi: 10.5343/bms.2011.1124 CrossRefGoogle Scholar
  34. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35:31–54. doi: 10.1146/annurev.ecolsys.35.021103.105704 CrossRefGoogle Scholar
  35. Lluch-Belda D, Schwartzlose RA, Serra R et al (1992) Sardine and anchovy regime fluctuations of abundance in four regions of the world oceans: a workshop report. Fish Oceanogr 1:339–347. doi: 10.1111/j.1365-2419.1992.tb00006.x CrossRefGoogle Scholar
  36. Míguez B, Combarro MP (2003) Bacteria associated with sardine (Sardina pilchardus) eggs in a natural environment (Ría de Vigo, Galicia, northwestern Spain). FEMS Microbiol Ecol 44:329–334. doi: 10.1016/S0168-6496(03)00070-9 CrossRefGoogle Scholar
  37. Miller KM, Teffer A, Tucker S et al (2014) Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evol Appl 7:812–855. doi: 10.1111/eva.12164 CrossRefGoogle Scholar
  38. Millot C (1990) The Gulf of Lions’ hydrodynamics. Cont Shelf Res 10:885–894. doi: 10.1016/0278-4343(90)90065-T CrossRefGoogle Scholar
  39. Ottersen G, Planque B, Belgrano A et al (2001) Ecological effects of the North Atlantic Oscillation. Oecologia 128:1–14. doi: 10.1007/s004420100655 CrossRefGoogle Scholar
  40. Panzarin V, Fusaro A, Monne I et al (2012) Molecular epidemiology and evolutionary dynamics of betanodavirus in southern Europe. Infect Genet Evol 12:63–70. doi: 10.1016/j.meegid.2011.10.007 CrossRefGoogle Scholar
  41. Pikitch EK, Rountos KJ, Essington TE et al (2014) The global contribution of forage fish to marine fisheries and ecosystems. Fish Fish 15:43–64. doi: 10.1111/faf.12004 CrossRefGoogle Scholar
  42. Piñeiro-Vidal M, Riaza A, Santos Y (2008) Tenacibaculum discolor sp. nov. and Tenacibaculum gallaicum sp. nov., isolated from sole (Solea senegalensis) and turbot (Psetta maxima) culture systems. Int J Syst Evol Microbiol 58:21–25. doi: 10.1099/ijs.0.65397-0 CrossRefGoogle Scholar
  43. Rice J (1995) Food web theory, marine food webs and what climate changes may do to northern marine fish populations. In: Beamish RJ (ed) Climate change and northern fish populations. Canadian Special Publications of Fisheries and Aquatic Sciences, Canada, pp 561–568Google Scholar
  44. Van Beveren E (2015) Population changes in small pelagic fish of the Gulf of Lions: a bottom-up control?. Université de Montpellier, MontpellierGoogle Scholar
  45. Van Beveren E, Bonhommeau S, Fromentin J-M et al (2014) Rapid changes in growth, condition, size and age of small pelagic fish in the Mediterranean. Mar Biol 161:1809–1822. doi: 10.1007/s00227-014-2463-1 CrossRefGoogle Scholar
  46. Van Beveren E, Fromentin J-M, Bonhommeau S et al (2016) The fisheries history of small pelagics in the Northern Mediterranean. ICES J Mar Sci. doi: 10.1093/icesjms/fsw023 Google Scholar
  47. Wang Y-D, Huang S-J, Chou H-N et al (2014) Transcriptome analysis of the effect of Vibrio alginolyticus infection on the innate immunity-related complement pathway in Epinephelus coioides. BMC Genomics 15:1102. doi: 10.1186/1471-2164-15-1102 CrossRefGoogle Scholar
  48. Whittington RJ, Crockford M, Jordan D, Jones B (2008) Herpesvirus that caused epizootic mortality in 1995 and 1998 in pilchard, Sardinops sagax neopilchardus (Steindachner), in Australia is now endemic. J Fish Dis 31:97–105CrossRefGoogle Scholar
  49. Xie Z-Y, Hu C-Q, Chen C et al (2005) Investigation of seven Vibrio virulence genes among Vibrio alginolyticus and Vibrio parahaemolyticus strains from the coastal mariculture systems in Guangdong, China. Lett Appl Microbiol 41:202–207. doi: 10.1111/j.1472-765X.2005.01688.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Elisabeth Van Beveren
    • 1
  • Nicolas Keck
    • 2
  • Jean-Marc Fromentin
    • 1
  • Stéphanie Laurence
    • 2
  • Hélène Boulet
    • 2
  • Sophie Labrut
    • 3
  • Marine Baud
    • 4
  • Laurent Bigarré
    • 4
  • Pablo Brosset
    • 1
    • 5
  • Claire Saraux
    • 1
    Email author
  1. 1.IFREMER (Institut Français de Recherche pour l’Exploitation de la MER)UMR MARBECSète CedexFrance
  2. 2.Conseil Départemental de l’HéraultLaboratoire Départemental VétérinaireMontpellier 2France
  3. 3.L’Université Nantes Angers Le Mans (LUNAM), Oniris, Nantes-Atlantic National College of Veterinary Medicine, Food Science and Engineering, Laboratoire d’Histopathologie AnimaleNantesFrance
  4. 4.ANSES, Laboratoire de Ploufragan-PlouzanéPlouzanéFrance
  5. 5.Université Montpellier, UMR MARBECSète CedexFrance

Personalised recommendations