Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae) from North-East Atlantic coastal waters and connected rivers
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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248 citations
"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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240 citations
"Metazoan parasite communities in Al..." refers background in this paper
...Adults harbored a thrice higher abundance of parasites compared to immatures, partly explained by a higher carrying capacity of adults (1.6 times greater body size compared to immatures) but also indicating parasite accumulation which is a common time-driven process (Dogiel et al. 1958)....
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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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...2003a), and more generally, due to increasing probability of meeting parasites over time/with age (Dogiel et al. 1958)....
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...fallax adults (vs immatures) and the general time-dependent parasite accumulation (Dogiel et al. 1958), the mean total abundance of parasites was similar Table 12 Metazoan parasite taxa recorded in adults of A....
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...6 times greater body size compared to immatures) but also indicating parasite accumulation which is a common time-driven process (Dogiel et al. 1958)....
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224 citations
"Metazoan parasite communities in Al..." refers background in this paper
...…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 ecosystem structure and functioning (MacKenzie 2002; Marcogliese 2005 for reviews)....
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219 citations
"Metazoan parasite communities in Al..." refers background in this paper
...…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)....
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202 citations
"Metazoan parasite communities in Al..." refers background in this paper
...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....
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...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)....
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Frequently Asked Questions (14)
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.