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Analysis of potential drivers of spatial and temporal changes in anisakid larvae infection levels in European hake, Merluccius merluccius (L.), from the North-East Atlantic fishing grounds

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Abstract

We analysed the spatial and temporal variability of Anisakis larvae infection in hake (Merluccius merluccius) from the North-East Atlantic from 1998 to 2020 and the potential drivers (i.e., environmental and host abundance) of such variation. The results showed that hake from separate sea areas in the North Atlantic have marked differences in temporal abundance levels. Hake larger than 60 cm were all parasitized in all ICES (International Council for the Exploration of the Sea) subareas 6, 7, and 8. The belly flaps were the most parasitized parts of the flesh, accounting for 92% of the total. Individuals of Anisakis simplex, Anisakis pegreffii, Anisakis spp. and a hybrid of Anisakis simplex × pegreffii were genetically identified, and Anisakis simplex as the most abundant (88–100%). An ecological niche model of Anisakis occurrence in fishes in the NE Atlantic was built to define the thermal optimum and environmental ranges for salinity, depth, chlorophyll concentration, and diffuse attenuation. The temporal variability of anisakid infection in fishes in the last two decades indicated an increase in the NE Atlantic at an annual rate of 31.7 nematodes per total number of specimens examined per year. This rise in infection levels could be triggered by the increase in intermediate host fish stocks, especially hake in the area.

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Data availability

The data underlying this article were provided by the Directorate of Fisheries and Aquaculture under licence / by permission. Data will be shared on request to the corresponding author with permission of the Directorate of Fisheries and Aquaculture of the Basque Government.

References

  • Abaunza P, Villamor B, Pérez JR (1995) Infestation by larvae of Anisakis simplex (Nematoda: Ascaridata) in horse mackerel, Trachurus trachurus, and Atlantic mackerel, Scomber scombrus, in ICES Divisions VIIIb, VIIIc and IXa (N-NW of Spain). Sci Mar 59(3–4):223–233

    Google Scholar 

  • Abollo E, Gestal C, Pascual S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499. https://doi.org/10.1007/s004360100389

    Article  PubMed  CAS  Google Scholar 

  • Aksnes DL (2007) Evidence for visual constraints in large marine fish stocks. Limnol Oceanogr 52:198–203

    Article  Google Scholar 

  • Arthur JR (1983) A preliminary analysis of the discreteness of stocks of walleye pollock (Theragra chalcogramma) from the Northeastern Pacific Ocean off Canada based on their parasites. Canadian Technical Report of Fisheries and Aquatic Sciences nº 1184:15 pp.

  • Assis J, Tyberghein L, Bosch S, Verbruggen H, Serrão EA, De Clerck O (2018) Bio-ORACLE v2.0: extending marine data layers for bioclimatic modelling. Glob Ecol Biogeogr 27:277–284

    Article  Google Scholar 

  • Bao M, Pierce GJ, Strachan NJC, Martínez C, Fernández R, Theodossiou I (2018) Consumers’ attitudes and willingness to pay for Anisakis -free fish in Spain. Fisheries Research 202(June ). https://doi.org/10.1016/j.fishres.2017.06.018

  • Barbet-Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: how, where and how many? Methods Ecol Evol 3(2):327–338. https://doi.org/10.1111/j.2041-210X.2011.00172.x

    Article  Google Scholar 

  • Berland B (1989). Identification of larval nematodes from fish. Nematode problems in North Atlantic fish. Report from a workshop in Kiel 3-4 April, C. M. 1989/F: 6. pp: 16-22

  • Brattey J, Bishop CA (1992) Larval Anisakis simplex (Nematoda: Ascaroidea) infection in the musculature of Atlantic cod, Gadus morhua, from Newfoundland and Labrador. Can J Fish Aquat Sci 49(12):2635–2647

    Article  Google Scholar 

  • Buchmann K, Mehrdana F (2016) Effects of anisakid nematodes Anisakis simplex (s.l.), Pseudoterranova decipiens (s.l.) and Contracaecum osculatum (s.l.) on fish and consumer health. Food and Waterborne Parasitology 4:13–22

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer

    Google Scholar 

  • Bush AO, Lafferty KH, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms Margolis et al. revisited. J Parasitol 83(4):575–583

    Article  PubMed  CAS  Google Scholar 

  • Carvajal J, Cattan PE (1985) A study of the anisakid infection in the chilean hake, Merluccius gayi (Guichenot, 1848). Fish Res 3:245–250

    Article  Google Scholar 

  • Cipriani P et al (2018) Anisakispegreffii (Nematoda: Anisakidae) in European anchovy Engraulis encrasicolus from the Mediterranean Sea: fishing ground as a predictor of parasite distribution. Fish Res 202:59–68

    Article  Google Scholar 

  • Cipriani P et al (2018) The Mediterranean European hake, Merluccius merluccius: detecting drivers influencing the Anisakis spp. larvae distribution. Fish Res 202:79–89

    Article  Google Scholar 

  • Cipriani P et al (2015) Genetic identification and distribution of the parasitic larvae of Anisakis pegreffii and Anisakis simplex (s.s.) in European hake Merluccius merluccius from the Tyrrhenian Sea and Spanish Atlantic coast: Implications for food safety. Int J Food Microbiol 198:1–8

    Article  PubMed  Google Scholar 

  • Community Reference Laboratory for Parasites (2010). Identification of anisakidae larvae at the species level by PCR/RFLP. 12 pp.

  • Chenowett JF, McGladdery E, Sindermann CJ, Sawyer TK, Bier JW (1986) An investigation into the usefulness of parasites as tags for herring (Clupea harengus) stocks in the Western North Atlantic, with emphasis on use the larval nematode Anisakis simplex. J Northwest Atlantic Fish Sci 7:25–33

    Article  Google Scholar 

  • Debenedetti AL et al (2019) Prevalence and risk of anisakid larvae in fresh fish frequently consumed in spain: an Overview. Fishes 4(13):16. https://doi.org/10.3390/fishes4010013

    Article  Google Scholar 

  • Diez G, Artetxe I (2000). Estudio de la parasitación por nemátodos de las especies de peces de mayor interés comercial. Informe Interno de AZTI para DAPA, 45 pp.

  • Dominici F, McDermott A, Zeger SL, M. SJ, (2002) On the use of generalized additive models in time-series studies of air pollution and health. Am J Epidemiol 156(3):193–203. https://doi.org/10.1093/aje/kwf062

    Article  PubMed  Google Scholar 

  • EEA (2017). Climate change, impacts and vulnerability in Europe 2016. An indicator-based report. EEA Report No 1. 424

  • Evans PGH, Waggitt JJ (2020) Impacts of climate change on marine mammals, relevant to the coastal and marine environment around the UK. MCCIP Science Review 2020:421–455

    Google Scholar 

  • Farjallah S et al (2008) Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitoly Research 102:371–379. https://doi.org/10.1007/s00436-007-0771-9

    Article  Google Scholar 

  • Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49

    Article  Google Scholar 

  • Fiorenza EA et al (2020) It’s a wormy world: meta-analysis reveals several decades of change in the global abundance of the parasitic nematodes Anisakis spp. and Pseudoterranova spp. in marine fishes and invertebrates. Glob Change Biol 00:1–13. https://doi.org/10.1111/gcb.15048

    Article  Google Scholar 

  • Gay M et al (2018) Infection levels and species diversity of ascaridoid nematodes in Atlantic cod, Gadus morhua, are correlated with geographic area and fish size. Fish Res 202:90–102

    Article  Google Scholar 

  • George-Nascimento M, Arancibia H (1992) Stocks ecológicos del jurel (Trachurus symmetricus murphyi Nichols) en tres zonas de pesca frente a Chile, detectados mediante comparación de su fauna parasitaria y morfometría. Rev Chil Hist Nat 65:453–470

    Google Scholar 

  • Gómez-Mateos M, Valero A, Morales-Yuste M, Martín-Sánchez J (2016) Molecular epidemiology and risk factors for Anisakis simplex s.l. infection in blue whiting (Micromesistius poutassou) in a confluence zone of the Atlantic and Mediterranean: Differences between A. simplex s.s. and A. pegreffii. Int J Food Microbiol 232:111–116

    Article  PubMed  Google Scholar 

  • Gregori M, Roura A, Pascual S, Abollo E, González AIF, Abaunza P (2014) Anisakis simplex complex (Nematoda Anisakidae) in zooplankton communities from temperate NE Atlantic waters. Journal of Natural History. https://doi.org/10.1080/00222933.2014.979260

    Article  Google Scholar 

  • Hastie T, Tibshirani R (1990) Generalized additive models, volume 43 of Monographs on Statistics and Applied Probability. Chapman & Hall, London

  • Hays R, Measures LN, Huo J (1998) Euphausiids as intermediate hosts of Anisakis simplex in the St. Lawrence Estuary. Can J Zool 76:1226–1235

    Article  Google Scholar 

  • Herreras MV, Aznar FJ, Balbuena JA, Raga JA (2000) Anisakid larvae in the musculature of the argentinean hake, Merluccius hubbsi. J Food Prot 63(8):1141–1143

    Article  PubMed  CAS  Google Scholar 

  • Hijmans RJ, Phillips S, Leathwick J, Elith J (2012) dismo Species distribution modeling. R package version 0:7–17

    Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22(2):415–427

    Article  Google Scholar 

  • ICES (2020) Working Group on Southern Horse Mackerel, Anchovy and Sardine (WGHANSA). ICES Scientific Reports 2(41):655. https://doi.org/10.17895/ices.pub.5977

    Article  Google Scholar 

  • ICES (2020b). Working Group on Widely Distributed Stocks (WGWIDE). ICES Scientific Reports, 2:82. 1019 pp. https://doi.org/10.17895/ices.pub.7475

  • ICES (2021a). ICES Stock Assessment Database. Copenhagen, Denmark. ICES. [accessed date: 26/02/2021]. https://standardgraphs.ices.dk.

  • ICES (2021) Working Group for the Bay of Biscay and the Iberian Waters Ecoregion (WGBIE). ICES Scientific Reports 3(48):1101. https://doi.org/10.17895/ices.pub.8212

    Article  Google Scholar 

  • Jimenez-Valverde A, Lobo JM (2007) Threshold criteria for conversion of probability of species presence to either-or presence-absence. Acta Oecologica 31(3):361–369

    Article  Google Scholar 

  • Khan RA, Tuck C (1995) Parasites as biological indicators of stocks of Atlantic cod (Gadus morhua) off Newfoundland, Canada. Can J Fish Aquat Sci 52(supp. 1):195–201

    Article  Google Scholar 

  • Klimpel S, Palm HW (2011) Anisakid nematode (Ascaridoidea) life cycles and distribution: increasing zoonotic potential in the time of climate change? in H. Mehlhorn, editor.Progress in Parasitology. Springer Berlin Heidelberg, 201-222

  • Kuhn T, Cunze S, Kochmann J, Klimpel S (2016) Environmental variables and definitive host distribution: a habitat suitability modelling for endohelminth parasites in the marine realm. Sci Rep 6:30246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuhn T, GarcíaMárquez J, Klimpel S (2011) Adaptive radiation within marine anisakid nematodes a zoogeographical modeling of cosmopolitan zoonotic parasites. PLoS ONE 8(10):e77908 6-e28642

    Google Scholar 

  • Kuhn T, Hailer F, Palm HW, Klimpel S (2013) Global assessment of molecularly identified Anisakis Dujardin, 1845 (Nematoda: Anisakidae) in their teleost intermediate hosts. Folia Parasitol 60(2):123–134

    Article  CAS  Google Scholar 

  • Levsen A et al (2018) Anisakis species composition and infection characteristics in Atlantic mackerel, Scomber scombrus, from major European fishing grounds —reflecting changing fish host distribution and migration pattern. Fish Res 202:112–121

    Article  Google Scholar 

  • Levsen A et al (2018) A survey of zoonotic nematodes of commercial key fish species from major European fishing grounds—Introducing the FP7 PARASITE exposure assessment study. Fish Res 202:4–21

    Article  Google Scholar 

  • Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3(1):704

    Article  PubMed  CAS  Google Scholar 

  • Lotze HK, Coll M, Magera AM, Ward-Paige C, Airoldi L (2011) Recovery of marine animal populations and ecosystems. Trends Ecol Evol 26(11):595–605

    Article  PubMed  Google Scholar 

  • MacKenzie K (1987) Parasites as indicators of host populations. Int J Parasitol 17:345–352

    Article  PubMed  CAS  Google Scholar 

  • MacKenzie K, Abaunza P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38:45–56

    Article  Google Scholar 

  • Magera AM, Mills Flemming JE, Kaschner K, Christensen LB, Lotze HK (2013) Recovery Trends in Marine Mammal Populations. PLoS ONE 8(10):e77908. https://doi.org/10.1371/journal.pone.0077908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marcogliese DJ (2008) Effects of climate change on animal and zoonotic helminthiases. Rev Revue Scientifique Et Technique-Office International Des Epizooties 27:443–452

    Google Scholar 

  • Margolis L, Esch GW, Holmes JC, Kurie AM, Schad GA (1982) The use of ecological terms in parasitology Report of an ad hoc committe of the American Society of Parasitologists. J Parasitol 68(1):131–133

    Article  Google Scholar 

  • Mattiucci S, Abaunza P, Damiano S, Garcia A, Santos MN, Nascetti G (2007) Distribution of Anisakis larvae, identified by genetic markers, and their use for stock characterization of demersal and pelagic fish from European waters: an update. J Helminthol 81:117–127. https://doi.org/10.1017/S0022149X07754718

    Article  PubMed  CAS  Google Scholar 

  • Mattiucci S, Abaunza P, Ramadori L, Nascetti G (2004) Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. J Fish Biol 65:495–510

    Article  Google Scholar 

  • McGladdery SE (1986) Anisakis simplex (Nematoda: Anisakidae) infection of the musculature and body cavity of Atlantic herring (Clupea harengus harengus). CanJ Fish Aquat Sci 43(7):1312–1317

    Article  Google Scholar 

  • McGladdery SE, Burt MDB (1985) Potential of parasites for use as biological indicators of migration, feeding, and spawning behavior of Northwest Atlantic Herring (Clupea harengus). CanJ Fish Aquat Sci 42:1957–1968

    Article  Google Scholar 

  • Mclelland G, Misra RK, Martell DJ (1990) Larval anisakine nematodes in various fish species from sable island bank and vicinity. Can J Fish Aquat Sci 222:83–118

    Google Scholar 

  • Measures LN (1996) Effect of temperature and salinity on development and survival of eggs and free-living larvae of sealworm (Pseudoterranova decipiens). Can J Fish Aquat Sci 53:2804–2807

    Article  Google Scholar 

  • Molina-Fernández D, Rubio-Calvo D, Adroher FJ, Benítez R (2018) Molecular epidemiology of Anisakis spp. in blue whiting Micromesistius poutassou in eastern waters of Spain, western Mediterranean Sea. Int J Food Microbiol 282:49–56

    Article  PubMed  Google Scholar 

  • Moser M, Hsieh J (1992) Biological tags for stock separation in pacific herring Clupea harengus pallasi in California. J Parasitol 78(1):54–60

    Article  PubMed  CAS  Google Scholar 

  • Myjak P, Szostakowska B, Wojciechowski J, Pietkiewicz M, Rockiki J (1994) Anisakid larvae in cod from the southern Baltic Sea. Arch Fish Mar Res 42(2):149–161

    Google Scholar 

  • Pascual S, Rodríguez H, Pierce GJ, Hastie LC, González AF (2018) The NE Atlantic European hake: a neglected high exposure risk for zoonotic parasites in European fish markets. Fish Res 202:69–78

    Article  Google Scholar 

  • Pierce GJ et al (2018) Ascaridoid nematode infection in haddock (Melanogrammus aeglefinus) and whiting (Merlangius merlangus) in Northeast Atlantic waters. Fish Res 202:122–133

    Article  Google Scholar 

  • Planque B, Loots C, Petitgas P, Lindstrom U, Vaz S (2011) Understanding what controls the spatial distribution of fish populations using a multi-model approach. Fish Oceanogr 20(1):1–17. https://doi.org/10.1111/j.1365-2419.2010.00546.x

    Article  Google Scholar 

  • Rodríguez H, Abollo E, González ÁF, Pascual S, Abaunza P (2018) Scoring the parasite risk in highly-valuable fish species from southern ICES areas. Fish Res 202:134–139

    Article  Google Scholar 

  • Rokicki J (2009) Effects of climatic changes on anisakid nematodes in polar regions. Polar Sci 3:197–201

    Article  Google Scholar 

  • Rose GA (2018) The fish nematode problem in major European fish stocks. Fish Res 202:1–3

    Article  Google Scholar 

  • Serrat A, Lloret J, Frigola-Tepe X, Muñoz M (2019) Trade-offs between life-history traits in a coldwater fish in the Mediterranean Sea: the case of blue whiting Micromesistius poutassou. Journal of Fish Biology:1-16

  • Smith JW (1984) Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878): length distribution and viability of L3 of known minimum age from herring Clupeaharengus. J Helminthot 58:337–340

    Article  Google Scholar 

  • Smith JW, Wootten R (1984) Fiche nº 8 Anisakis larvae (“herringworm”) (Nematoda) in fish Parasitose des poissons par les larves du nématode Anisakis Fiches d’identification des maladies et parasites des poissons crustacés et mollusques. NOAA Northeast fisheries center Sandy Hook laboratory Highlands New Jersey 07732:5

    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 

  • Unger P, Klimpel S, Lang T, Palm H (2014) Metazoan parasites from herring (Clupea harengus L.) as biological indicators in the Baltic Sea. Acta Parasitol 59:518–528

    Article  PubMed  Google Scholar 

  • Valero A, López-Cuello M, Benítez R, Adroher FJ (2006) Anisakis spp in European hake Merluccius merluccius (L) from the Atlantic off north-west Africa and the Mediterranean off southern Spain. Acta Parasitologica 51(3):209–212

    Article  Google Scholar 

  • Williams HH, MacKenzie K, McCarthy AM (1992) Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev Fish Biol Fisheries 2:144–176

    Article  Google Scholar 

  • Zuur AF, Leno EN, Walker NJ (2009) Mixed effects models and extensions in ecology with R. , Springer Science NY, Springer Science NY,

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Acknowledgements

We are very grateful to Sergio López from OPP 07 and Miguel Neira from ABSA for supplying hake samples in the last two years of the study. We also acknowledge the contribution of Amaia Astarloa to the discussions about cetacean abundance trends in the North-East Atlantic.

Funding

This work was supported by the Directorate of Fisheries and Aquaculture of the Basque Government (Department of Economic Development, Infrastructures and Environment – Vice Dept. of Agriculture, Fisheries and Food Policies) project ANIFEMP (grant number 00001-IRB2018-33) and by the European Union project (Urban Klima 2050) from the LIFE programme (grant number LIFE 18 IPC 000001).

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  1. Marine Research, AZTI- Basque Research and Technology Alliance (BRTA), Txatxarramendi s/n, 48395, Sukarrieta-Bizkaia, Spain

    Guzmán Diez, Guillem Chust, Eider Andonegi, Marina Santurtún, Carmen Abaroa, Elisabette Bilbao, Arantza Maceira & Iñaki Mendibil

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  1. Guzmán Diez
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Contributions

GD, GC, EA, and MS contributed to the conception and design of the study. GD, AM, and CA collected and analysed the samples and EB and IM performed the genetic analysis. GD, GC, and EA analysed the data and wrote the manuscript and carried out substantial revisions of the manuscript. All the authors revised and approved the submitted version.

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Correspondence to Guzmán Diez.

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Diez, G., Chust, G., Andonegi, E. et al. Analysis of potential drivers of spatial and temporal changes in anisakid larvae infection levels in European hake, Merluccius merluccius (L.), from the North-East Atlantic fishing grounds. Parasitol Res 121, 1903–1920 (2022). https://doi.org/10.1007/s00436-022-07446-2

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