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Journal ArticleDOI

Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae) from North-East Atlantic coastal waters and connected rivers

07 Jun 2017-Parasitology Research (Springer Berlin Heidelberg)-Vol. 116, Iss: 8, pp 2211-2230

TL;DR: Metazoan parasites were studied in 96 Alosa alosa and 78 Alosa fallax from North-East Atlantic coastal waters and connected rivers in order to increase knowledge on these anadromous endangered fish and measure the parasitic impact on host condition.
Abstract: Metazoan parasites were studied in 96 Alosa alosa and 78 Alosa fallax from North-East Atlantic coastal waters and connected rivers (among them three sympatric sites) in order to increase knowledge on these anadromous endangered fish and measure the parasitic impact on host condition. All shads were infected by one to six metazoan parasite taxa among the 12 identified in the whole sampling, with a mean abundance of parasites higher for A. alosa (167 ± 10) than for A. fallax (112 ± 11). Helminths, mostly trophically transmitted, were the best represented (eight taxa, prevalence up to 99%) in contrast with crustaceans and Petromyzontidae that rarely occurred (four taxa, prevalence <6%). Despite some quantitative differences, metazoan parasite communities of A. alosa and A. fallax remained stable in composition whatever the host developmental stage, sex, sample site, and salinity. Among the nine parasite taxa harbored by each Alosa species, six were shared with some differences in distribution patterns including in sympatric conditions, suggesting increasing dissimilarities between A. alosa and A. fallax with the age. Information on feeding ecology provided by trophically transmitted helminths confirmed euryphagous opportunistic diet of immatures and adults of both shad species, and assessed feeding of adults during spawning migrations. Our study also revealed the significant negative impact of Hemiurus appendiculatus on A. alosa and Pronoprymna ventricosa on A. fallax. Because helminth parasites are omnipresent in the shads and decrease their fitness, parasitological data must be included in further investigations and management programs on A. alosa and A. fallax.
Topics: Alosa (64%)

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Metazoan parasite communities in Alosa alosa
(Linnaeus, 1758) and Alosa fallax (Lac,pSde, 1803)
(Clupeidae) from North-East Atlantic coastal waters
and connected rivers
Claudia Gérard, Maxime Hervé, Mélanie Gay, Odile Bourgau, Eric Feunteun,
Anthony Acou, Elodie Réveillac
To cite this version:
Claudia Gérard, Maxime Hervé, Mélanie Gay, Odile Bourgau, Eric Feunteun, et al.. Metazoan parasite
communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lac,pSde, 1803) (Clupeidae) from
North-East Atlantic coastal waters and connected rivers. Parasitology Research, Springer Verlag
(Germany), 2017, 116 (8), pp.2211-2230. �10.1007/s00436-017-5525-8�. �hal-01577992�

Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803)
(Clupeidae) from North-East Atlantic coastal waters and connected rivers
Claudia Gérard
1*
, Maxime Hervé
2
, Mélanie Gay
3
, Odile Bourgau
3
, Eric Feunteun
4
, Anthony Acou
4
and Elodie
Réveillac
5
1
UMR ECOBIO 6553, CNRS, Université de Rennes 1, Avenue du Général Leclerc 35042 Rennes, France
2
IGEPP, Université de Rennes 1, Avenue du Général Leclerc 35042 Rennes, France
3
French Agency for Food, Environmental and Occupational Health and Safety (Anses), Laboratory for Food
Safety, F-62200 Boulogne-sur-Mer, France
4
UMR 7208 BOREA, Service des Stations Marines, Muséum National d’Histoire Naturelle, 38 rue du Port
Blanc, 35800 Dinard, France
5
ESE Agrocampus-Ouest INRA, Ecologie Halieutique, Rue de Saint Brieuc 35042 Rennes, France
*Corresponding author, Email address: claudia.gerard@univ-rennes1.fr
Phone: (+33) 2-23-23-50-37

Abstract
Metazoan parasites were studied in 96 Alosa alosa and 78 Alosa fallax from North-East Atlantic coastal waters
and connected rivers (among them three sympatric sites) in order to increase knowledge on these anadromous
endangered fish and measure the parasitic impact on host condition.
All shads were infected by one to six metazoan parasite taxa among the 12 identified in the whole sampling, with
a mean abundance of parasites higher for A. alosa (167 ± 10) than for A. fallax (112 ± 11). Helminths, mostly
trophically-transmitted, were the best represented (eight taxa, prevalence up to 99%) in contrast with crustaceans
and Petromyzontidae that rarely occurred (four taxa, prevalence < 6%). Despite some quantitative differences,
metazoan parasite communities of A. alosa and A. fallax remained stable in composition whatever host
developmental stage, sex, sample site and salinity. Among the nine parasite taxa harbored by each Alosa species,
six were shared with some differences in distribution patterns including in sympatric conditions, suggesting
increasing dissimilarities between A. alosa and A. fallax with the age. Information on feeding ecology provided
by trophically-transmitted helminths confirmed euryphagous opportunistic diet of immatures and adults of both
shad species, and assessed feeding of adults during spawning migrations. Our study also revealed the significant
negative impact of Hemiurus appendiculatus on A. alosa and Pronoprymna ventricosa on A. fallax.
Because helminth parasites are omnipresent in the shads and decrease their fitness, parasitological data must be
included in further investigations and management programs on A. alosa and A. fallax.
Key-words
Alosa spp.; metazoan parasites; host developmental stage; marine vs freshwater phases; fitness loss.

Introduction
Although cryptic, parasites are ubiquitous members of ecological communities, representing high
biomass, and are recognized as key players in broader interactions and ecosystem dynamics, such as food web
structure and energy flow (e.g. Price et al. 1986; Marcogliese 2004; Kuris et al. 2008; Johnson et al. 2010;
Hatcher et al. 2012; Lambden and Johnson 2013; Sekalovic et al. 2014). Parasites increase vulnerability of their
host and decrease their fitness; the host mortality risk of infected individuals being almost thrice higher
compared to hosts uninfected or with reduced parasite burdens (Combes 1995; Thomas et al. 2007; Robar et al.
2010; McElroy and De Buron 2014 for reviews). Furthermore, parasites such as helminths are increasingly used
as biological tags to provide information on host populations (e.g. feeding habits, habitat use, stock
discrimination, and migration) and on free-living biodiversity and changes in ecosystem structure and
functioning (MacKenzie 2002; Marcogliese 2005 for reviews).
The anadromous allis shad Alosa alosa (Linnaeus, 1758) and twaite shad Alosa fallax (Lacépède, 1803)
spend most of their life along the European Atlantic coast before returning in fresh waters to spawn generally in
their natal rivers, with one spawning migration for A. alosa but several for A. fallax (for reviews: Baglinière and
Elie 2000; Aprahamian et al. 2003a; Jolly et al. 2012). During the last decades, these closely related clupeids
greatly declined in abundance throughout their geographic range, probably due to anthropogenic impact (e.g.
overfishing, pollution, dam constructions, gravel extraction) (Baglinière and Elie 2000; Aprahamian et al.
2003a). Therefore, they are considered a vulnerable species (listed in Annex II of the EU Habitats Directive and
Annex III of the Bern Convention) and are classified as of « least concern » by IUCN (Freyhof and Kottelat
2008ab). Up to now, respectively 23 (19 helminths and four crustaceans) and 20 (17 helminths and three
crustaceans) taxa of metazoan parasites have been recorded in A. alosa and A. fallax, among them 11 shared by
the two host species (Aprahamian 1985; Doherty and McCarthy 2002; Aprahamian et al. 2003a; Nunn et al.
2008; Bao et al. 2015ab). Numerous studies have been conducted in order to increase knowledge on shads for
conservation purposes (e.g. Baglinière and Elie 2000; Aprahamian et al. 2003ab; Baglinière et al. 2003; Jolly et
al. 2012; Acou et al. 2013; Martin et al. 2015; Mota et al. 2015), but the significance of parasites has rarely been
considered and never included in management and conservation programs.
Parasite communities tend to be similar in hosts that are geographically, phylogenetically, ecologically and
developmentally close from one another (Locke et al. 2013). A. alosa and A. fallax are closely related species
between which extensive hybridization can occur despite assessment of independent lineages (Alexandrino et al.

2006) and some ecological and biological differences (Baglinière and Elie 2000; Taverny and Elie 2001ab;
Aprahamian et al. 2003ab). Therefore, similarities and dissimilarities of the parasite communities are expected
between A. alosa and A. fallax, depending on developmental stage, geographical site, and marine or freshwater
phase. The analysis of metazoan parasite communities is thus undoubtedly an interesting and attractive way of
getting knowledge on the spatial ecology of both shad species throughout their anadromous life-cycle as well as
on their health status.
In this context, our objectives are:
(1) To describe and compare communities of metazoan parasites in A. alosa and A. fallax sampled in European
Atlantic coastal-estuarine waters and rivers during their oceanic growth and anadromous breeding phases, and
thus to determine how the parasitofauna of shads is influenced by environmental (salinity, site) and host
physiological parameters (developmental stage, sex);
(2) to evaluate the impact of metazoan parasites on A. alosa and A. fallax using four condition indices (total
weight, girth, fat content, and Fulton’s K) as a proxy of fitness (Jakob et al. 1996);
(3) to determine if some parasite taxa could be used as biological tags to discriminate shad individuals (at a
specific and/or population level) and/or to provide information on feeding habits and displacements.
Materials and Methods
Study-sites and fish samplings
The European “Natura 2000” networking program (Acou et al. 2013), which aims to increase
knowledge on shad species for conversation purposes, provided a total of 96 A. alosa and 78 A. fallax. These
were caught between May 2010 and March 2012 by professional fishermen in four French freshwater river
systems (Vire, Vilaine, Loire, and Dordogne) and four estuarine and coastal waters from North-East Atlantic
including Bay of Biscay and North Sea (Fig. 1, Table 1). Three sampling sites were found to harbor A. alosa and
A. fallax in sympatric conditions (i.e. Loire, North Biscay Bay, and Adour).
Fish measurements
Total weight (TW, g), fork length (FL, mm) and girth (G, mm) of each fish were measured. Then,
gonads were extracted and weighted (GW, g) in order to calculate the gonado-somatic ratio (= GW / TW) as a
proxy of maturity stage and reproductive potential. The fat content in fish was proximately determined through
the elemental bulk tissue carbon to nitrogen ratio (C/N) in muscles, calculated through stable isotope ratio

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