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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.

Summary (4 min read)

Introduction

  • 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.
  • 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, 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.

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

  • 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 analyses by mass spectrometry.
  • The use of this index relies on the assumption that an increase in tissue total lipid concentration correlated with increases in C/N ratios since lipid contains mainly carbon and few-to-no nitrogen (Barnes et al. 2007).
  • The Fulton’s K was used as a condition index for A. alosa and A. fallax because of their quasi-isometric length-weight growth (Bolger and Connolly 1989; Taverny and Elie 2001a; Correia et al. 2001) and was calculated as K = 105 TW/FL3.
  • Immature shads of both Alosa species were mostly captured in coastal waters during their growth phase (80.0% for A. alosa and 96.0% for A. fallax) (Table 2).

Parasitological research

  • All the 174 fish were frozen before the search for metazoan parasites as in previous studies (Gérard et al.
  • The following organs and tissues: skin, gills, muscles, heart, digestive tract, gonads, and body cavity were meticulously dissected under a binocular stereomicroscope.
  • Molecular identification of nematodes via DNA sequencing A total of 54 Anisakis and 249 Hysterothylacium were analyzed by molecular identification tools.
  • Sequences were analyzed using BioEdit software to obtain consensus sequences from forward and reverse sequences.

Statistical analysis

  • Mean number of parasite taxa was compared between (i) all individuals, (ii) immatures and (iii) adults of the two host species using likelihood ratio tests applied on Generalized Linear Models (family: Poisson, link: log) (GLMs).
  • Mean total abundance of parasites was compared between (i) all individuals, (ii) immatures and (iii) adults of the two host species using a Student t-test.
  • In models focused on immatures and adults, the only explanatory variable was the host species.
  • The relationship between host size and parasite prevalence and abundance was tested using Wald tests (based on GLMs for prevalence, LMs for abundance), at the scale of the whole parasitofauna and for each of the major parasite taxa, separately for each host species.
  • Throughout the following sections, data are reported as means ± standard error (SE).

Results

  • Composition of metazoan parasite community in A. alosa and A. fallax Each of the 96 A. alosa and 78 A. fallax dissected was infected (total prevalence of 100%) by one to six metazoan parasite taxa among the 12 identified in the whole sampling (Table 3).
  • Some organs (i.e. muscles, heart and gonads) were not found infected.
  • Based on molecular identification, three nematode species were unambiguously identified, i.e., Anisakis simplex sensu stricto (Rudolphi, 1809), Anisakis pegreffii Campana-Rouget and Biocca, 1955, and Hysterothylacium aduncum (Rudolphi, 1802) (Table 4).
  • A. simplex s.s. and H. aduncum were recorded in both shad species and in most sampling sites, whereas A. pegreffi was only found in A. fallax from Loire and Pertuis Charentais (Table 4).

2. Is the metazoan parasite community influenced by host developmental stage (juvenile vs adult) and sex?

  • - Alosa alosa Differences occurred depending on the developmental stage of A. alosa (Table 5).
  • Both prevalences and abundances were higher in adults (vs immatures) for H. aduncum and Anisakis spp. (P ≤ 0.010), but not different whatever the developmental stage for M. alosae and H. appendiculatus (Table 5).
  • The mean number of parasite taxa per fish was not different among the sites as well as the mean total abundance of metazoan parasites per fish, but the distribution patterns of the nine parasite taxa differed between sites (CCA: pseudo-F = 10.196, df1 = 3, df2 = 91, P < 0.001) (Table 7).
  • P. laevis was only recorded in fresh waters whereas C. emarginata and A. foliaceus were only found in salt waters; these three species being rare in A. fallax (total prevalence ≤ 5%) (Table 6).
  • Between six and seven parasite taxa were recorded depending on the site with a mean value of 6.6 ± 0.2 (Table 8).

4. Are metazoan parasite communities different between host species in the whole sampling, in sympatric

  • Prevalences and abundances of shared parasite taxa were also significantly different between shad species (P < 0.001, Table 9), except for those of H. aduncum and the rare copepod C. emarginata, and also abundance of H. appendiculatus (Table 9).
  • These differences and similarities were not influenced by sympatric conditions except for prevalence and abundance of Anisakis spp. (P ≤ 0.005) and, in a lesser extent, abundance of E. fragile, a rare species in A. alosa (P = 0.050) (Table 9).
  • No differences occurred in the abundances of each of the six common parasite taxa between immatures of A. alosa and A. fallax (Tables 5, 6 and 10).

5. Relationship between parasite abundance and fish size and impact of parasitism on host body condition

  • Among the four major parasite taxa of A. alosa, prevalences and abundances of both H. aduncum and Anisakis spp. and abundance of M. alosae were positively correlated to the fork length of A. alosa (P ≤ 0.021); no relationship was detected for prevalence of M. alosae and both prevalence and abundance of H. appendiculatus.
  • No significant relationship was evident for M. alosae and Anisakis spp. whatever the body condition index considered.
  • Independently of fish size, the whole parasite abundance was negatively related to the girth (P = 0.034); no significant relationship was detected with the other body condition indices (total weight, C/N ratio, and Fulton’s K).
  • When considering each of the six main parasite taxa, some of them (H. aduncum, P. ventricosa, and E. fragile) were correlated to the body condition of A. fallax.
  • Indeed, a positive relationship was demonstrated between H. aduncum and both total weight and Fulton’s K (P ≤ 0.013), as well as between E. fragile and both girth and Fulton’s K (P ≤ 0.007).

Discussion

  • 1) High significance of metazoan parasites in A. alosa and A. fallax and comparison with previous parasitological studies.
  • The authors study highlights the importance of metazoan parasites in A. alosa and A. fallax in terms of their total prevalence of 100% and their high mean abundance (respectively 167 ± 10 and 112 ± 11 parasites per fish) and diversity (nine parasite taxa per host species).
  • The shads were mainly used as definitive hosts by helminths (except Anisakis using shads as paratenic hosts) and infected following ingestion of parasitized preys (except M. alosae actively infecting host gills) (Table 3).
  • Moreover, the absence of Anisakis spp. in English and Irish waters is questioning since A. simplex s.s. is widespread between 35°N and Arctic Polar Circle whereas the upper limit of A. pegreffii is the Iberian coast of North-East Atlantic (Mattiucci and Nascetti 2006).

2) Low variability of metazoan parasite communities according to physiological characteristics

  • (developmental stage, sex) and environmental conditions (salinity, geographical area).
  • Differences in prevalences and abundances of H. appendiculatus, Anisakis spp., and P. ventricosa suggest that compared to A. fallax adults, immatures preyed a greater proportion of planktonic crustaceans and chaetognaths infected by H. appendiculatus and/or Anisakis spp., but a smaller proportion of amphipods infected by P. ventricosa (Table 3).
  • The mean number of parasite taxa harbored per fish was not different between host species, but the total abundance of parasites per fish was 1.5 times higher in A. alosa than in A. fallax, potentially resulting from a size effect that enable larger fish to acquire more parasites than smaller counterparts (Zelmer 2014).
  • The distribution patterns of some parasite taxa shared by A. alosa and A. fallax could be different between host species, including in sympatric conditions.
  • Thus, despite overall parasite similarity, their data underline increasing differences with the age between shad species, in particular in their diet, mainly occurring after sexual maturity in relation with semelparous vs iteroparous reproductive strategy (Baglinière and Elie, 2000; Aprahamian et al. 2003a for reviews), but also probably due to a variety of other abiotic and biotic factors.

Conclusions

  • The authors study demonstrates that during their oceanic growth and anadromous breeding phases in European Atlantic coastal-estuarine waters and rivers, A. alosa and A. fallax harbor stable metazoan parasite communities.
  • All shads are parasitized whatever environmental and physiological conditions, and mostly by euryhaline and generalist trophically-transmitted helminths.
  • Metazoan parasites may negatively impact the condition of A. alosa and A. fallax, thus increasing their vulnerability at a time when they greatly declined in abundance throughout their geographic range (Baglinière and Elie 2000; Aprahamian et al. 2003a).
  • This study was funded by the French Ministry of Ecology and Sustainable Development (‘Programme de connaissances Natura2000 amphihalins en mer’).
  • Authors warmly thank the numerous fishermen and local angling federation for providing the fish.

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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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"Metazoan parasite communities in Al..." refers methods in this paper

  • ...The mitochondrial cytochrome c oxidase subunit II (cox2) gene was amplified using the primers 211 F (5′-TTT TCT AGT TAT ATA GAT TGR TTYAT-3′) and 210 R (5′-CAC CAA CTC TTA AAA TTATC-3′) as described in Nadler and Hudspeth (2000) and Valentini et al. (2006)....

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    [...]

  • ...…depending on developmental stage, partly due to the anadromous life cycle inducing changes in diet and habitat use (for reviews: Baglinière and Elie 2000; Aprahamian et al. 2003a), and more generally, due to increasing probability of meeting parasites over time/with age (Dogiel et al. 1958)....

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TL;DR: The work published over the past decade on the use of parasites as biological tags in population studies of marine fish, mammals and invertebrates, particularly on demersal fish, is reviewed.
Abstract: This paper reviews the work published over the past decade on the use of parasites as biological tags in population studies of marine fish, mammals and invertebrates. Fish hosts are considered in taxonomic and ecological groups as follows: demersal, anadromous, small pelagic, large pelagic and elasmobranch. Most studies were carried out on demersal fish, particularly on members of the genera Merluccius (hake), Sebastes (rockfish) and on Atlantic cod Gadus morhua L., but Pacific salmonids and small pelagic fish of the genus Trachurus are also well-represented. A current multidisciplinary study of the population biology of horse mackerel Trachurus trachurus in European waters, which includes the use of parasites as tags, is described. Two studies recognize the potential for using parasites as tags for cetaceans but, in spite of the considerable potential for this approach in population studies of elasmobranchs, no original study has been carried out on this group for over ten years. Studies of parasites as tags for marine invertebrates have concentrated on squid. Recent trends in the use of parasites as biological tags for marine hosts are discussed.

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"Metazoan parasite communities in Al..." refers background in this paper

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TL;DR: It is recognized that parasites influence species coexistence and extirpation by altering competition, predation, and herbivory, and that these effects can, in turn, influence ecosystem properties.
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TL;DR: Preliminary data for reconstruction of a possible co-evolutionary scenario between cetacean hosts and their Anisakis endoparasites suggests that cospeciation and host-switching events may have accompanied the evolution of this group of parasites.
Abstract: Advances in the taxonomy and ecological aspects concerning geographical distribution and hosts of the so far genetically recognised nine taxa of the nematodes belonging to genus Anisakis (i.e. A. pegreffii, A. simplex s.s., A. simplex C, A. typica, A. ziphidarum, Anisakis sp., A. physeteris, A. brevispiculata and A. paggiae) are here summarized. Genetic differentiation and phylogenetic relationships inferred from allozyme (20 enzyme-loci) and mitochondrial (sequences of cox-2 gene) markers, are revised and compared. The two genetic analyses are congruent in depicting their phylogenetic relationships. Two main clusters are showed to exist in the obtained trees, one encompassing the species A. pegreffii, A. simplex s.s., A. simplex C, A. typica, A. ziphidarum and Anisakis sp.; while, the second including A. physeteris, A. brevispiculata and A. paggiae. The existence of two clades is also supported by their morphological differentiation in adult and larval morphology. Comparison of phylogenetic relationships among Anisakis spp. with those currently available for their cetacean definitive hosts suggests parallelism between host and parasite phylogenetic tree topologies. Preliminary data for reconstruction of a possible co-evolutionary scenario between cetacean hosts and their Anisakis endoparasites suggests that cospeciation and host-switching events may have accompanied the evolution of this group of parasites. Finally, genetic/molecular markers for the identification of the so far genetically recognized taxa of Anisakis at any life-stage and both sexes were given also in relation to human anisakiosis is discussed.

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  • ...Further studies are needed to explore A. pegreffi distribution in North-East Atlantic and to understand why no Anisakis spp. were found in shads from English and Irish waters....

    [...]

  • ...These results (Tables 11 and 12) confirm that A. alosa is the preferred host of M. alosae compared to A. fallax in North-East Atlantic and connected rivers (Gérard et al. 2016), the life cycle of the monogenean being closely synchronized with those of its host (Bychowsky 1957)....

    [...]

  • ...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....

    [...]

  • ...Moreover, the absence of Anisakis spp. in English and Irish waters is questioning since A. simplex s.s. is widespread between 35° N and the Arctic Polar Circle whereas the upper limit of A. pegreffi is the Iberian coast of the North-East Atlantic (Mattiucci and Nascetti 2006)....

    [...]

  • ...pegreffii is the Iberian coast of North-East Atlantic (Mattiucci and Nascetti 2006)....

    [...]

Frequently Asked Questions (14)
Q1. What are the contributions in "Metazoan parasite communities in alosa alosa (linnaeus, 1758) and alosa fallax (lac,psde, 1803) (clupeidae) from north-east atlantic coastal waters and connected rivers" ?

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. 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. 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. 

Further studies are needed to explore A. pegreffii distribution in North-East Atlantic and to understand why no Anisakis spp. was found in shads from English and Irish waters. 

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). 

Because of their omnipresence and ecological significance, there is a dire need to integrate parasitic helminths in further multidisciplinary investigations to get knowledge on A. alosa and A. fallax and to develop efficient management and conservation programs. 

Only one metazoan parasite taxon (i.e. the gill monogenean Gyrodactylus von Nordmann, 1832commonly infecting freshwater fish) has previously been reported in larvae of A. fallax, and four taxa [i.e. 

The absence of overlap between parasite communities of immature shads may be due to i) age (larvae, 0+ and older immatures) resulting in potential differences in habitat and food use (Baglinière and Elie 2000), ii) inter-site prey availability inducing differences in the euryphagous and opportunistic diet of immatures (Nunn et al. 2008; Baglinière and Elie 2000), iii) absence of host species needed to complete the heteroxenous life cycle of most helminths, and/or iv) potential mortality of infected immatures as shown for Gyrodactylus (GranoMaldonado et al. 2011). 

Chi-square tests and Student t-tests were performed to compare prevalence and abundance of the six common parasite taxa between hosts separately for each of the sympatric sites (Loire, Adour, and North Biscay Bay). 

The parasitological parameters used to describe the parasite community structure were: prevalence (P,number of hosts infected with a particular parasite species / number of hosts examined), taxa richness (number of parasite taxa infecting a host species), and abundance (number of individuals of a particular parasite species in/on a single host regardless of whether or not the host is infected) (Bush et al. 1997). 

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. 

The most prevalent taxa were the monogenean M. alosae (dominant species for A. alosa), the digeneans H. appendiculatus (dominant species for A. fallax) and P. ventricosa (only recorded in A. fallax), the cestode E. fragile (rare in A. alosa), and the nematodes Anisakis spp. (i.e. A. simplex s.s., A. pegreffii) and H. aduncum. 

Because greater pathogenicity is often observed for recent host-parasite associations (e.g. Kennedy 1994; Kania et al. 2010), the association between H. appendiculatus and A. alosa could be more recent, thus inducing a significant host fitness loss. 

In models analyzing all individuals, explanatory variables considered were the host species, the sympatry (yes/no) and the interaction between these two factors. 

Their study highlights the importance of metazoan parasites in A. alosa and A. fallax in terms of theirtotal prevalence of 100% and their high mean abundance (respectively 167 ± 10 and 112 ± 11 parasites per fish) and diversity (nine parasite taxa per host species). 

All the metazoan parasites found were numbered per organ and per fish, and morphologically identified to the species level excepted for nematodes.