Assessment of the body indices and Anguillicola crassus infection status in European eel (Anguilla anguilla) in estuarine systems in Greece

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Δημοσιευμένα: Apr 19, 2025
DOI: https://doi.org/10.12681/jhvms.38045
V Kantzoura
1Veterinary Research Institute, Hellenic Agricultural Organization - DEMETER, 57001 Thermi, Thessaloniki, Greece
A Sapounidis
Fisheries Research Institution, Hellenic Agricultural Organization - DEMETER, 64007 Nea Peramos, Kavala, Greece
MK Kouam
Faculty of Agronomy and Agricultural Sciences, Cameroon
E Koutrakis
Fisheries Research Institution, Hellenic Agricultural Organization - DEMETER
Περίληψη

The European eel (Anguilla anguilla, Linnaeus 1758) is a catadromous, benthic carnivorous predator species that spends most of its life in freshwater, brackish and coastal habitats. Τhe aims of the present study were to examine the morphometric features of European eel population in five estuarine systems in Northern and Western Greece, to investigate the prevalence of Anguillicola crassus and to identify the risk factors associated with an effect to parasitism. The total length of the examined eels (1,343) ranged from 320 mm to 991 mm and the total weight ranged from 46 g to 2,760 g. Condition factor (K) ranged from 0.02 (Mazoma lagoon) to 0.44 (Vistonis and Evros estuarine systems). From the regression results on Lt-Wt relationship, the coefficient of determination (r2) was found to have a strong relationship between Lt-Wt (p<0.01). The overall prevalence of the parasitism was 27.1% (CI: 26.0-31.0). Among the different sampling sites, the eels collected from Vistonis estuarine system had the highest prevalence (63.5%) (CI: 57.8-68.8) following the two lagoons from Mesolonghi lagoon complex: Kleisova lagoon (36.6%) and Tholi lagoon (35.6%). The multivariate binary logistic model analysis demonstrated that the significant factors associated with the infection of A. crassus into the Greek eel population, were the Condition factor K, gender, life stage and eels originate from Vistonis estuarine system. A high level of A. crassus parasitism in various habitats in the study area was located and the nematode is abundant in all A. anguilla habitats in Greece.

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Βιογραφικό Συγγραφέα
MK Kouam, Faculty of Agronomy and Agricultural Sciences, Cameroon

Department of Animal Science, Faculty of Agronomy and Agricultural Sciences, P.O. Box 188, Dschang, Cameroon

 

Αναφορές
Abdallah, L.G.B., Maamouri, F., 2006. Spatio-temporal dymanics of the
Nematoda Anguillicola crassus in Northeast Tunisian lagoons. C. R.
Biol. 329, 785-789.
Andrew, J. H. D., & Jellyman, D. J., 2005. Sex determination in freshwater
eels and management options for manipulation of sex. Reviews
in Fish Biology and Fisheries 15, 37-52. DOI:10.1007/s11160-005-
-x
Algers, B., Blokhuis, H.J., Botner, A., Broom, D.M., Costa, P., Domingo,
M., Greiner, M., Hartung, J., Koenen, F., Müller-Graf, C. et al.
& Wierup M., 2009. Species—specific welfare aspects of the main
systems of stunning and killing of farmed eels (Anguilla anguilla).
European Food Safety Authority Journal 1014, 1-42
Alexakis, D., 2011. Assessment of water quality in the Messolonghi-Etoliko
and Neochorio region (West Greece) using hydrochemical and
statistical analysis methods. Environ Monit Assess 182, 397-413.
https://doi.org/10.1007/s10661-011-1884-2
Amin, S. M. N., Arshad, A., Haldar, G. C., Shohaimi, Ara, R., 2005. Estimation
of Size Frequency Distribution, Sex Ratio and Length-Weight
Relationship of Hilsa (Tenualosailisha) in the Bangladesh Water. Research
Journal of Agriculture and Biological Sciences, 1(1), 61-66.
Aprahamian, M. W., Evans, D. W., Briand, C., Walker, A. M., McElarney,
Y., Allen, M. (2021). The changing times of Europe’s largest remaining
commercially harvested population of eel Anguilla anguilla L.
Journal of Fish Biology, 99(4), 1201- 1221. https://doi.org/10.1111/
jfb.14820
Arai, T., Chino, N., 2012. Diverse migration strategy between freshwater
and seawater habitats in the freshwater eel genus Anguilla. J Fish
Biol., 81(2), 442-455. doi: 10.1111/j.1095-8649.2012.03353.x.
Aschonitis, V., Castaldelli, G., Lanzoni, M., Rossi, R., Kennedy, C., Fano,
E.Α., 2017. Long‐term records (1781-2013) of European eel (Anguilla
anguilla L.) production in the Comacchio Lagoon (Italy): evaluation
of local and global factors as causes of the population collapse.
Aquatic Conservation Marine and Freshwater Ecosystems, 27(2),
-520. https://doi.org/10.1002/aqc.2701
Ayala, D. J., Munk, P., Lundgreen, R. B. C., Traving, S. J., Jaspers, C.,
Jørgensen, T. S., Hansen, L. H., Riemann, L., 2018. Gelatinous plankton
is important in the diet of European eel (Anguilla anguilla) larvae
in the Sargasso Sea. Sci Rep., 8(1), 6156. doi: 10.1038/s41598-018-
-x.
Bagenal, T., Tesch, F.W., 1978. Age and growth. In: Methods for assessment
of fish production in fresh water. T. Bagenal (Ed.), Blackwell
Scientific Publications, Oxford, UK, pp. 118-130.
Barry, J., Newton, M., Dodd, J. A., Evans, D., Newton, J., Adams, C.E.,
The effect of foraging and ontogeny on the prevalence and intensity
of the invasive parasite Anguillicola crassus in the European
eel Anguilla anguilla. J Fish Dis., 40(9), 1213-1222. doi: 10.1111/
jfd.12596.
Becerra-Jurado, G., Cruikshanks, R., O’Leary, C., Kelly, F., Poole, R.,
Gargan, P., 2014. Distribution, prevalence and intensity of Anguillicola
crassus (Nematoda) infection in Anguilla anguilla in the Republic
of Ireland. J. Fish Biol. 84, 1046-1062.
Bernotas, P., Vetemaa, M., Saks, L., Eschbaum, R., Verliin, A., Järvalt, A.,
Dynamics of European eel landings and stocks in the coastal
waters of Estonia. ICES Journal of Marine Science, 73(1), 84-90, doi.
org/10.1093/icesjms/fsv245
Beullens, K., Eding, E. H., Gilson, P., Ollevier, F., Komen, J., Richter,
C.J.J., 1997. Gonadal differentiation, intersexuality and sex ratios of
European eel (Anguilla anguilla L.) maintained in captivity. Aquaculture,
, 135-150.
Bevacqua, D., Andrello, Μ., Paco, A., Paco, M., Crivelli, A., 2011. Density-
dependent and inter-specific interactions affecting European eel
settlement in freshwater habitats. Hydrobiologia, 671(1), 259-265.
DOI: 10.1007/s10750-011-0725-1
Bevacqua, D., Melià, P., Gatto, M., & De Leo, G.A., 2015. A global viability
assessment of the European eel. Glob Chang Biol., 21(9), 3323-
doi: 10.1111/gcb.12972.
Bond, C.E., 1996. Biology of fishes. Harcort Brace, New York, 750 pp.
Capoccioni, F., Costa, C., Canali, E., Aguzzi, J., Antonucci, F., Ragonese,
S., Bianchini, M.L., 2014. The potential reproductive contribution of
Mediterranean migrating eels to the Anguilla anguilla stock. Scientific
Reports 4 7188.
Clains, D. K., Chaput, G., Poirier, L. A., Avery, T. S., Castanguary, M.,
Mathers, A., Casselman, J. M., Bradford, R. G., Pratt, T., Verreault,
G. et al., 2014. Recovery potential assessment for American eel (Anguilla
rostata) for eastern Canada: life history, distribution, reported
landings, status indicators, and demographic parameters. DFO Canadian
Science Advisory Secretariat Research Document 2013/134 xiv
p. http://www.dfo-mpo.gc.ca/csas-sccs/index-eng.htm
Costa-Dias, S., 2010. Infection by Anguillicoloides crassus in a riverine
stock of European eel, Anguilla anguilla. Fisheries Fish Manag. Ecol. 17, 485-492. https://doi.org/10.1111/j.1365-2400.2010.00746.x
Dekker, W., Casselman, J.M., 2014. The 2003 Quebec Declaration of concern
about Eel declines-11 years later: are eels climbing back up the
slippery slope? Fisheries 39, 613-614.
De Meyer, J., Christiaens, J., Adriaens, D., 2016. Diet-induced phenotypic
plasticity in European eel (Anguilla anguilla). J Exp Biol., 219(3),
-363. doi: 10.1242/jeb.131714.
De Meyer, J., Verhelst, P., Adriaens, D., 2020. Saving the European Eel:
How Morphological Research Can Help in Effective Conservation
Management. Integr Comp Biol.;60(2):467-475. doi:10.1093/icb/
icaa004
Dezfuli, B. S., Maestri, C., Lorenzoni, M., Carosi, A., Maynard, B. J.,
Bosi, G., 2021. The impact of Anguillicoloides crassus (Nematoda)
on European eel swimbladder: histopathology and relationship between
neuroendocrine and immune cells. Parasitology, 148(5), 612-
https://doi.org/10.1017/S0031182021000032
Genc, E., Sangun, M. K., Dural, M., Can, M. F., Altunhan, C., 2007. Element
concentrations in the swimbladder parasite Anguillicola crassus
(nematoda) and its host the European eel, Anguilla anguilla from Asi
River (Hatay-Turkey). Environmental Monitoring and Assessment
(1-3), 59-65. doi:10.1007/s10661-007-9878-9
Genç, T. O., Yilmaz, F., 2017. Metal Accumulations in Water, Sediment,
Crab (Callinectessapidus) and Two Fish Species (Mugilcephalus
and Anguilla anguilla) from the Köyceğiz Lagoon System-Turkey:
An Index Analysis Approach. Bull Environ Contam Toxicol, 99, 173.
https://doi.org/10.1007/s00128-017-2121-7
Gérard, C., Trancart, T., Amilhat, E., Faliex, E., Virag, L., Feunteun, E.,
Acou, A., 2013. Influence of introduced vs. native parasites on the
body condition of migrant silver eels. Parasite, 20, 38. https://doi.
org/10.1051/parasite/2013040
Gkanasos, A., Somarakis, S., Tsiaras, K., Kleftogiannis, D., Giannoulaki,
M., Schismenou, E., Sofianos, S., Triantafyllou, G., 2019. Development,
application and evaluation of a 1-D full life cycle anchovy and
sardine model for the North Aegean Sea (Eastern Mediterranean).
PLoS One, 14(8):e0219671. doi: 10.1371/journal.pone.0219671
Golani, D, Shefler, D, Gelman, A., 1988. Aspects of growth and feeding
habits of the adult European eel (Anguilla anguilla) in Lake
Kinneret (Lake Tiberias), Israel. Aquaculture, 74(3-4), 349-354.
doi:10.1016/0044-8486(88)90378-x
Henderson, A. P., Plenty, J. S., Lyn, C., Newton, C. L., Bird, J.D., 2012.
Evidence for a population collapse of European eel (Anguilla anguilla)
in the Bristol Channel. Coral Reefs, the Aquarium Trade and the
Maritime Industry, 92(4), 843-851. DOI: https://doi.org/10.1017/
S002531541100124X
ICES, 2021. Report of the Working Group on Eels (WGEEL), ICES Scientific
Reports. 3:85. 205 pp. https://doi.org/10.17895/ices.pub.8143
ICES, 2018. European eel (Anguilla anguilla) throughout its natural
range. ICES advice on fishing opportunities. DOI/URI 10.17895/ices.
pub.4601
Jacoby, D., Gollock, M., 2014. Anguilla anguilla. The IUCN Red List
of Threatened Species 2014: e.T60344A45833138. http://dx.doi.
org/10.2305/IUCN.UK.2014-1.RLTS.T60344A45833138.en.
Jobling, M., 1995. Environmental biology of fishes: Chapman & Hall,
London, Fish & Fisheries, 16, 455.
Kantzoura, V., Sapounidis, A., Kouam, M.K., Kolygas, M.Ν., Krey, G.,
Koutrakis, E., 2021. Anguillicola (Anguillicoides) crassus: Morphometric
characteristics and pathogenicity in eels (Anguilla anguilla)
in Greece. Vet. Parasitol. Reg. Stud. 25, 100586. https://doi.
org/10.1016/j.vprsr.2021.100586
Katselis, G., Koutsikopoulos, C.. Dimitriou, E., Rogdakis, I., (2003). Spatial
and temporal trends in the composition of the fish barriers fisheries
production of the Μesolonghi-Εtoliko lagoon (western Greek
coast). Scientia Marina 67 (4), 501-511.
Kitada, S., Nakajima, K., Hamasaki, K., Shishidou, H., Waples, R. S.,
Kishino, H., 2019. Rigorous monitoring of a large-scale marine stock
enhancement program demonstrates the need for comprehensive
management of fisheries and nursery habitat. Sci Rep., 9(1), 5290.
doi: 10.1038/s41598-019-39050-3.
Koutrakis, E.T., Tsikliras, A.C., 2003. Length - weight relationships of
fishes from three northern Aegean estuarine systems (Greece). J Appl
Ichthyology, 19, 258-260.
Koutrakis, E.T., Conides, A., Parpoura, A.C., van Ham, E.H., Katselis,
G., Koutsikopoulos, C., 2007. Lagoon Fisheries’ Resources in Hellas.
Chapter 6, pp. 223-234. In. Papaconstantinou C., Zenetos A., Vassilopoulou
V., Tserpes G. (eds), State of Hellenic Fisheries. Hellenic
Centre for Marine Research, Athens, Greece.
Koutrakis E.T, Tsikliras A.C., 2003. Length-weight relationships of fishes
from three northern Aegean estuarine systems (Greece). J. Appl. Ichthyol.
: 258-260.
Knights, B., 2003. A review of the possible impacts of long-term oceanic
and climate changes and fishing mortality on recruitment of anguillid
eels of the Northern hemisphere. Sci Total Environ, 310, 237-244.
Le Cren, C.D., 1951. The Length-Weight Relationship and Seasonal Cycle
in Gonad Weight and Condition in Perch, Perca fluviatilis. Journal
of Animal Ecology, 20, 201-219.
Lefebvre, F., Crivelli AJ., 2012. Salinity effects on anguillicolosis in
Atlantic eels: a natural tool for disease control. Mar Ecol Prog Ser
,193-202. https://doi.org/10.3354/meps10032
Lefebvre, F., Fazio, G., Mounaix, B., Crivelli, A.J., 2013. Is the continental
life of the European eel Anguilla anguilla affected by the parasitic
invader Anguillicoidescrassus? Proceedings of the Royal Society B:
Biological Sciences, 208, 20122916.
Lortholarie, M., Poirier, L., Kamari, A., Herrenknecht, C., Zalouk-
Vergnoux, A., 2021. Rare earth element organotropism in European
eel (Anguilla anguilla). Sci. Total Environ., 766, https://doi.
org/10.1016/j.scitotenv.2020.142513
MacNamara, R., Koutrakis, E. T., Sapounidis, A., Lachouvaris, D., Arapoglou,
F., Panora, D., Mccarthy, T.K., 2014. Reproductive potential
of silver European eels (Anguilla anguilla) migrating from Vistonis
Lake (Northern Aegean Sea, Greece). Medit. Mar. Sci., 15, 539-544.
DOI: http://dx.doi.org/10.12681/mms.614
Marcogliese, J. D., 2002. Food webs and the transmission of parasites
to marine fish. Parasitology, 124(07), S83-99. DOI: 10.1017/
S003118200200149X
Markou, D., Sylaios, G., Tsihrintzis, V., Gikas, G., Haralambidou, K.,
Water quality of Vistonis Lagoon, Northern Greece: seasonal
variation and impact of bottom sediments. Desalination 210(1-3),
-97.
Martinez-Carrasco, C., Ruiz de Ybanez, R., Penalver, J., Mayo-Hernandez,
E., Garcia-Ayala, A., Munoz, P., 2011. Prevalence of Anguillicoides
crassus (Nematoda, Dracunculoidea) in wild European eels
(Anguilla anguilla L.) from Mar Menor lagoon (Western Mediterranean,
Spain). Revue Med Vet, 162, 154-158.
McConville, J., Fringuelli, E., Evans, D., Savage, P., 2018. First examination
of the Lough Neagh European eel (Anguilla anguilla) population
for eel virus European, eel virus European X and Anguillid Herpesvirus-
infection by employing novel molecular techniques. J Fish Dis.,
(12), 1783-1791. doi: 10.1111/jfd.12885.
Moravec, F., Skorikova, B., 1998. Amphibians and larvae of aquatic
insects as new paratenic hosts of Anguillicolacrassus (Nematode:
Dracunculoidea), a swimbladder parasite of eels. Dis Aquat Org, 34,
-222.
Newbold, L.R., Hockley, F.A., Williams, C.F., Cable, J., Reading, A.J.,
Auchterlonie, N., Kemp, P.S., 2015. Relationship between European
eel Anguilla anguilla infection with non-native parasites and swimming
behavior on encountering accelerating flow. J Fish Biol. 86(5),
-1533. doi: 10.1111/jfb.12659.
Nzau Matondo, B., Delrez, N., Bardonnet, A., Vanderplasschen, A.,
Joaquim-Justo, C., Rives, J., Benitez, J. P., Dierckx, A., Séleck,
E., Rollin, X., Ovidio, M., 2022. A complete check-up of European
eel after eight years of restocking in an upland river: Trends in
growth, lipid content, sex ratio and health status. The Science of the
total environment, 807 (Pt 3), 151020. https://doi.org/10.1016/j.scitotenv.
151020
Pankurst, N.W., 1982. Relation of visual changes to the onset of sexual
maturation in the European eel Anguilla anguilla. J. Fish Biol. 21,
-140.
Palstra, A. P., Heppener, D. F. M., van Ginneken, V. T. J., Szekely, C., van
den Thillart, J.M., 2007. Swimmbladder performance of silver eels is
severely impaired by the swim bladder parasite Anguillicolacrassus.
Journal of Experimental Marine Biology and Ecology, 352, 244-256
Poole, W.R., Diserud, O.H., Thorstad, E.B., Durif, M.C., Dolan, C., Sand lund, O.T., Bergesen, K., Rogan, G., Kelly, S., Vollestad, L.A., 2018.
Long-term variation in numbers and biomass of silver eels being
produced in two European river systems. ICES Journal of Marine
Science, 75(5). DOI: 10.1093/icesjms/fsy053
Pujolar, J.M., Bevacqua, D., Capoccioni, F., Ciccotti, E., De Leo, G. A.,
Zane, L., 2011. No apparent genetic bottleneck in the demographically
declining European eel using molecular genetics and forward-time
simulations. Conserv Genet 12, 813-825.
Rahel, F.J., McLaughlin, R.L., 2018. Selective fragmentation and the
management of fish movement across anthropogenic barriers. Ecol
Appl. 28(8), 2066-2081doi: 10.1002/eap.1795
Reid, M. K., Spencer, K.L., 2009. Use of principal components analysis
(PCA) on estuarine sediment datasets: the effect of data pre-treatment.
Environ Pollut. 157(8-9), 2275-2281 doi: 10.1016/j.envpol.
03.033.
Ricker, W.E. (1975). Computation and interpretation of biological statistics
of fish populations. Bulletin of the Fisheries Research Board of
Canada 191, 382.
Rubin, A., de Coulon, P., Bailey, C., Segner, H., Wahli, T., Rubin, J.F.,
Keeping an eye on wild brown trout (Salmo trutta) populations:
Correlation between temperature, environmental parameters, and
proliferative kidney disease. Front Vet Sci. 22(6), 281. doi: 10.3389/
fvets.2019.00281
Schneebauer, G., Hanel, R., Pelster, B., 2016. Anguillicola crassus impairs
the silvering-related enhancements of the ROS defense capacity
in swimbladder tissue of the European eel (Anguilla anguilla).
Journal of comparative physiology. B, Biochemical, systemic, and
environmental physiology, 186(7), 867-877. https://doi.org/10.1007/
s00360-016-0994-0
Silva, A.T., Midwood, J.D., Aarestrup, K., Pottinger, T.G., Madsen, S.S.,
Cooke, S.J., 2018. The influence of sex, parasitism, and ontogeny on
the physiological response of European eels (Anguilla anguilla) to
an abiotic stressor. Physiological and Biochemical Zoology, 91, 976-
Simon. J., Ubl, C., Lewin, W.C., Dorow, M., 2023. Infection with swim
bladder nematode Anguillicola crassus in relation to European eel
growth, age, and habitat along the German Baltic coast. Dis Aquat
Org 155:21-33. https://doi.org/10.3354/dao03739
Smith, J.A., Handley, J.C., Dietl, G.P., 2018. Effects of dams on downstream
molluscan predator-prey interactions in the Colorado River
estuary. Proc Biol Sci. 30, 285(1879). pii: 20180724. doi: 10.1098/
rspb.2018.0724.
Tech, F.W., 1971. Age and Growth. In: Richer W.E. (ed.). Methods for
assessment of fish production in fresh water, Blackwell Scientific
Publications, Oxford & Edinburgh, p. 98-130
Unger, P., Schmidt, J., Dorow, M., Möller, S., Palm, H.W., 2024. Reaching
the steady state: 30 years of Anguillicola crassus infection of European
eel, Anguilla anguilla L., in Northern Germany. Parasitology.
(3):300-308. doi: 10.1017/S0031182024000039
Wootton, R.J., 1990. Ecology of Teleost Fishes. Springer, p. 1-14.
Würtz, J., Taraschewski, H., Pelster, B., 1996. Changes in gas composition
in the swimbladder of the European eel (Anguilla anguilla) infected
with Anguillicola crassus (Nematoda). Parasitology, 11(2), 233-238.