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

TLDR: 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.

Figures

Table 11. Metazoan parasite taxa recorded in adults of A. alosa in this study, in the Irish Barrow river and Waterford estuary (Doherty and McCarthy 2002), and in Western Iberian Peninsula rivers (Bao et al. 2015ab). (P = prevalence, A = abundance, SE = standard error, SD = standard deviation).

Table 6. Prevalence (P ± SE %) and mean abundance (A ± SE) of the parasite taxa in Alosa fallax (78) according to the age (immatures vs adults), the sex (males vs females), and the salinity (sea vs rivers). See abbreviations of parasite taxa in Table 3.

Table 7. Component communities of metazoan parasites (prevalence P ± SE%, mean abundance (A ± SE) in Alosa alosa according to the sampled site. Rivers = Vire, Vilaine, and Loire; coastal and estuarine waters = North Biscay Bay and Adour. See abbreviations of parasite taxa in Table 3.

Table 10. Statistical comparison of the total prevalences (χ2) and the mean abundances (F) of each parasite taxa common to A. alosa (96) and A. fallax (78) according to the developmental stage (immatures vs adults). See abbreviations of the six parasite taxa in Table 3.

Table 2. Number and mean fork length (FL ± SE, mm) of Alosa alosa and Alosa fallax (immatures, males, females) sampled in the 8 study-sites of North-East Atlantic coastal/estuarine waters and connected rivers.

Table 3. Metazoan parasites in Alosa alosa (96) and Alosa fallax (78) in North-East Atlantic waters and connected rivers: abbreviation (abb), microhabitat in fish (MH), total prevalence (P ± SE %), mean abundance (A ± SE), and bibliographic data on salinity, infection pathway and definitive host (Kabata 1964; Chiriac and Udrescu 1973; Bray and Gibson 1980; Kennedy 1981, 2006; Gibson and Bray 1986; Køie 1993; Pasternak et al. 2000; Klimpel and Rückert 2005; Mattiucci and Nascetti 2008; Taverny and Elie 2010; Smit et al. 2014; Gérard et al. 2016). BC = body cavity, DT = digestive tract, ESC = esophagus-stomachcaecum, G = gills, I = intestine, PC = pyloric caeca, S = skin; FW = fresh water, BW = brackish water, SW = salt water; Hi = intermediate host, Hp = paratenic host.

Full text

HAL Id: hal-01577992
https://hal-univ-rennes1.archives-ouvertes.fr/hal-01577992
Submitted on 28 Aug 2017
HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entic research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.
L’archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diusion de documents
scientiques de niveau recherche, publiés ou non,
émanant des établissements d’enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.
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

Frequently asked questions

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. 

Q2. What have the authors stated for future works 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" ?

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. 

Q3. What are the main reasons for the increasing use of helminths as biological tags?

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). 

Q4. Why do the authors need to integrate shads into conservation programs?

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. 

Q5. How many species of shad have been reported in freshwater fish?

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. 

Q6. What is the reason for the absence of overlap between immatures and shads?

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). 

Q7. What was the procedure used to compare the prevalence and abundance of the six common parasite taxa?

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). 

Q8. What were the parameters used to describe the parasite community structure?

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). 

Q9. Why are helminths omnipresent in the shads?

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. 

Q10. What species of shads were prevalent in A. alosa?

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. 

Q11. Why is A. alosa more likely to have a host fitness loss?

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. 

Q12. What were the explanatory variables considered in the models analyzing all individuals?

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

Q13. What is the significance of the parasites in A. alosa?

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). 

Q14. What were the morphologically identified metazoan parasites?

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