Open Access
Issue
Aquat. Living Resour.
Volume 35, 2022
Article Number 3
Number of page(s) 18
DOI https://doi.org/10.1051/alr/2022002
Published online 20 May 2022

© C. Gérard et al., published by EDP Sciences 2022

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1 Introduction

The starry smooth-hound Mustelus asterias Cloquet, 1819 is a demersal coastal species of triakid shark, commercially exploited and distributed on the continental shelf to 200 m depth from Northern Europe to Northwest Africa, including the Mediterranean Sea (Jabado et al., 2021). ICES Working Group on Elasmobranch Fishes (ICES WGEF, 2019) considers there is a single biological stock unit in the continental shelf waters of Northeast Atlantic (ICES areas IV, VI–VIII), but with uncertain southern limits in the absence of relevant studies on stock identity. According to the IUCN's Red List (Jabado et al., 2021), M. asterias is considered “Near Threatened”. This assessment is mainly due to its decline in the Mediterranean Sea recorded from 1994 onwards and its disappearance from most Mediterranean coastal areas, suggesting a high risk of regional extinction (Colloca et al., 2017; Jabado et al., 2021). Stock evaluation of M. asterias required for management and conservation measures remains difficult due to current taxonomical confusion between M. asterias and Mustelus mustelus, and sometimes between Mustelus spp. and early juveniles of Galeorhinus galeus, as demonstrated in the Northeast Atlantic (Farrell et al., 2009; ICES WGEF, 2019).

Although some recent data occurred on reproduction, growth and seasonal migrations of M. asterias (Farrell et al., 2010a,b; McCully Phillips and Ellis, 2015; Brefeld and Meyer, 2018; ICES WGEF, 2019; Brevé et al., 2016, 2020; Griffiths et al., 2020), it remains a lack of knowledge on various biological and ecological aspects such as population structure, distribution, and behaviour. Surprisingly, the parasitofauna has received very little attention in previous works on M. asterias, despite parasites are ubiquitous natural stressors of great interest to understand population dynamics and to implement management strategies. Indeed, first, metazoan parasites decrease the host fitness (e.g., lower energy reserves and life traits such as growth and fecundity) and increase the host mortality risk (almost thrice higher for infected hosts compared to uninfected) (e.g., Thomas et al., 2007; Robar et al., 2010; McElroy and De Buron, 2014; Timi and Poulin, 2020 for reviews). Second, metazoan parasites influence biotic interactions (e.g., competition, predation) and host responses to other environmental stresses (e.g., overfishing, pollution, and degradation of marine habitat), reducing animal health in myriad ways (e.g., Price et al., 1986; Marcogliese and Pietrock, 2011; Frainer et al., 2018; Timi and Poulin, 2020 for reviews). Third, metazoan parasites such as helminths may provide perspective on the biology of their hosts (e.g., diet, habitat use, movements, stock discrimination), environmental pollution (e.g., heavy metals), and on free-living biodiversity, as shown by their increasingly use as bioindicators (e.g., MacKenzie, 2002; Marcogliese, 2005; De Buron et al., 2009; Catalano et al., 2014; Timi and Poulin, 2020 for reviews).

To date, the parasitofauna of M. asterias is poorly known, especially in case of immature sharks, and data have been scarcely and scattered published [e.g., a parasitological study on three females of M. asterias among other shark species in Ireland (Henderson et al., 2003); a phylogenetic study on cestodes of triakids including 11 specimens of M. asterias from the North Sea (Bernot et al., 2016)].

In this context and to address this knowledge gap, we have investigated the metazoan parasites of M. asterias juveniles sampled in the English Channel, an important fishing ground of Northeast Atlantic. Our aims were: (i) to describe the community of metazoan parasites in M. asterias; (ii) to study the relationships between parasite occurrence and M. asterias health using two condition indices (hepato-somatic ratio, Fulton's K) as proxies of fitness (Bolger and Connolly, 1989; Lloret et al., 2012; Gérard et al., 2017; Silva et al., 2017; Ryberg et al., 2020); (iii) to examine the potential use of metazoan parasites as host bioindicators.

2 Material and methods

2.1 Study-sites and fish samplings

Twenty immature starry smooth-hounds were caught in 2018 by professional fishermen in the Northeast Atlantic in three ICES areas, respectively VIId (Eastern Channel = one individual in September 2018), VIIe (Western Channel = 15 in January 2018) and VIIf (Bristol Channel = four in March 2018) (Fig. 1).

thumbnail Fig. 1

Geographical position of the three ICES areas in the North-East Atlantic where Mustelus asterias was caught: VIId (Eastern Channel), VIIe (Western Channel) and VIIf (Bristol Channel).

2.2 Fish measurements

We measured total mass (TM in g) and total length (TL in cm) of each fish, then we determined the sex and assessed the immaturity stage (McCully Phillips and Ellis, 2015). Upon dissection, we recorded liver mass (LM in g) and eviscerated mass of each fish (EM in g). We calculated two indices of body condition as proxies of fitness: Hepato-Somatic Index (HSI) and Fulton's K (K) (Bolger and Connolly, 1989; Lloret et al., 2012; Gérard et al., 2017; Silva et al., 2017; Ryberg et al., 2020). For both indices, we used the eviscerated mass to avoid bias due to the mass of parasites and gut contents (Lagrue and Poulin, 2015) as follows: HSI = (LM/EM) × 100 and K = 105 EM/TL3. We chose HSI to evaluate host condition because the liver of elasmobranchs is the main lipid storage site and a major site of lipid synthesis (Speers-Roesch and Treberg, 2010 for review). We selected K among the primary condition factors based on length-mass relationships because of the quasi-isometric length-weight growth of M. asterias (Bolger and Connolly, 1989; Silva et al., 2013), and because K has previously been documented to be the best predictor of parasite load in Lepomis macrochirus (Centrarchidae) (Neff and Cargnelli, 2004).

2.3 Parasitological research

All the fish were frozen before the search for metazoan parasites. The following organs and tissues: eyes, skin, muscles, gills, heart, digestive tract, liver, and body cavity were meticulously dissected under a binocular stereomicroscope. Excepted for Myxozoa (myxosporean cysts), all the 609 metazoan parasites found were numbered per organ and per fish, and then morphologically identified. Morphological identification referred to Price (1942) for Monogenea; Curran and Overstreet (2000) and Gibson et al. (2001) for Digenea; Barker et al. (1984), Khalil et al. (1994), Ruhnke (2011), Palm and Walter (2000), Ruhnke and Caira (2009), Schaeffner (2014) and Bernot et al. (2016) for Cestoda; Petter et al. (1991), Moravec et al. (2002) and Anderson et al. (2009) for Nematoda; Lom and Dyková (2006) for Myxozoa; and Isawa (2008) for Copepoda.

Some nematode specimens (i.e., Achanthocheilus rotundatus and Proleptus obtusus) were preserved in 70% ethanol for molecular identification to validate morphological identification (see below).

The parasitological parameters used to describe the parasite community structure were: prevalence (P, number of hosts infected with a particular parasite taxon divided by the number of hosts examined), taxa richness (R, number of parasite taxa infecting a host species), abundance (A, number of individuals of a particular parasite taxon divided by the total number of hosts, infected plus uninfected), and intensity (I, number of individuals of a particular parasite taxon divided by the number of infected hosts) (Bush et al., 1997).

2.4 Molecular identification of nematodes via DNA sequencing

The DNA of each individual parasite was extracted using Wizard® Genomic DNA Purification Kit (Promega) following manufacturer's instructions after grinding of the parasite with a sterile piston pellet. DNA was kept at −20 °C until used. The 18S rDNA partial gene (18S) was amplified using the primers 18SF (5'-CGCGAATRGCTCATTACAACAGC-3') and 18SR (5'-GGGCGGTATCTGATCGCC-3') as described in Floyd et al. (2005), with an initial denaturation of 15 min at 95 °C, 40 cycles of 94 °C for 30 s, 55 °C for 40 s and 68°C for 1 min 30s and a final elongation step of 10 min at 68 °C. The amplification of the nuclear rDNA region comprising ITS-1, 5.8S, and ITS-2 sequences was carried out with the primers A (5'-GTCGAATTCGTAGGTGAACCTGCGGAAGGAT-3') and B (5'-CCGATCCGAATCCTGGTTA-GTTTCTTTTCCT-3') as described in D'Amelio et al. (2000). The amplification of the nuclear rDNA ITS-2 region was carried out with the primers XZ1F (5'-ATTGCGCCATCGGGTTCATTCC-3') and NC2 R (5'-TTAGTTTCTTTTCCTCCGCT-3') as described in Zhu et al. (2000). Automated DNA sequencing was performed by Genoscreen (Lille, France), and then sequences were analyzed using BioEdit software to obtain consensus sequences from forward and reverse sequences. They were subsequently compared with available 18S or ITS sequences of nematode species by GenBank Blast software (Basic Local Alignment Search Tool) (Altschul et al., 1997).

2.5 Statistical analysis

Throughout the following sections, data are reported as means followed by 95% confidence interval (CI). For prevalence, 95% CI was calculated using the score method (Newcombe, 1998). All statistical analyses were performed with the R software v. 4.0.2 (R Core Team, 2020).

Prevalence was compared between parasite taxa using a likelihood ratio test (LRTest) applied to a Generalized Linear Model (GLM, distribution: binomial, link function: logit) including the parasite taxon and the shark individual as independent variables. Pairwise comparisons of estimated marginal means (EMMeans) were subsequently performed using the ‘emmeans’ R package (Lenth, 2021), with P-values adjusted using the false discovery rate correction (Benjamini and Hochberg, 1995). The same approach was used to analyse abundance data (GLM distribution: negative binomial, link function: log) and intensity data (GLM with parasite taxon as only independent variable, distribution: negative binomial, link function: log).

Condition parameters were compared between host sexes using both a multivariate approach (redundancy analysis (RDA) on centred and scaled data, and associated permutation test with 9999 permutations; ‘vegan’ R package (Oksanen et al., 2020)) and a univariate approach (t test for each parameter). The same procedure was used to compare the parasite community (parasite taxa with prevalence >5% only) between host sexes (presence-absence data: RDA on Hellinger-transformed data (Legendre and Gallagher, 2001) and univariate LRTests on GLMs (distribution: binomial, link function: logit); abundance data: RDA on Hellinger-transformed data and univariate F tests on GLMs (distribution: quasi-Poisson, link function: log)). Total parasite abundance and taxa richness (both including all parasite taxa) were compared between sexes using LRTests based on GLMs (distribution: negative binomial and Poisson respectively, link function: log in both models).

Relationships between the parasitofauna and host condition parameters were assessed using F tests on LMs. For each condition parameter, two models were built per parasite taxon (taxa with prevalence >5% only): one relating the presence of the parasite (binary factor) to the condition parameter and another one relating the abundance of the parasite to the condition parameter. The effect of the total parasite abundance was also assessed in the same way. The whole procedure was repeated for all host individuals, males only and females only.

Differences were considered statistically significant at P < 0.05.

3 Results

3.1 Metazoan parasite community of M. asterias juveniles

Each immature specimen of M. asterias was infected (total prevalence of 100%; CI 84–100%) by one to six metazoan parasite taxa among the 12 identified in the whole sampling (Tab. 1). The mean number of parasite taxa per fish was 3.55 ± 0.70 (range: 1–6) and the mean total abundance (= mean total intensity) of parasites (Myxozoa excluded) was 30.45 ± 21.36 parasites per fish (range: 1–170).

Parasites were mainly recorded in the digestive tract, i.e., nine gastro-intestinal helminth taxa in 19 fish, with a prevalence of 95% (CI 76–99%) and a mean intensity of 13.16 ± 5.09 helminths per fish (Tab. 1). In a lesser extent, parasites occurred on the gills, i.e., three taxa in 13 fish, with a prevalence of 65% (CI 43–82%) (Tab. 1). The other organs examined (eyes, skin, muscles, heart, liver, and body cavity) were not found infected.

Among the 12 parasite taxa recorded, helminths were the best represented (10 taxa among them six cestodes), in contrast with crustaceans (one copepod species) and Myxozoa (one myxosporean taxon) (Tab. 1). At least one helminth taxon was recorded in each specimen of M. asterias (helminth prevalence of 100%; CI 84–100%) with a mean of 16.05 ± 6.37 helminths per fish, and in total, 80% (CI 58–92%) of the sharks harboured a mean of 6.81 ± 2.93 cestodes in their spiral valve.

Prevalences, mean abundances and intensities significantly varied between parasite taxa (χ2 = 82.416, 98.795 and 53.309 respectively, df = 11, 10 and 10 respectively, all P < 0.001) (Tab. 1). The three major parasite taxa were in decreasing order (prevalence value in parenthesis): the nematode Acanthocheilus rotundatus (75%, CI 53–89%), then the cestode Eutetrarhynchus sp. (70%, CI 48–85%), both in the digestive tract, and the monogenean Erpocotyle laevis (60%, CI 39–78%) on the gills. All these highly prevalent taxa were recorded in the three ICES areas (Tab. 1). Five other parasite taxa had intermediate prevalence (15–35%); among them, the copepode Kroyeria lineata (35%, CI 18–57%) on the gills, characterized by a significantly much higher mean intensity (41.14 ± 55.79, up to 155 parasites per fish) compared to all other parasite taxa (Tab. 1). The four last taxa (cestodes in the spiral valve) were rare with only one specimen of M. asterias found infected in VIIe ICES area (Tab. 1).

Among the 97 isolated nematodes from 13 immature starry smooth-hounds, 27 individuals were molecularly identified, i.e., 20 A. rotundatus and seven Proleptus sp. (P. obtusus according to morphology, not confirmed by molecular analysis due to the absence of reference sequence of this species) (Tab. 2). Individual 18S sequences had an identity percentage with sequences present in National Center for Biological Information above 99.8% and 99.6% respectively for A. rotundatus and Proleptus sp. (Tab. 2). For three A. rotundatus individuals, identification was also confirmed by ITS2 sequences with identity percentage above 99.6%. Percentage of coverage was always at least 96% whatever sequences. All the sequences generated in this study were deposited in GenBank (accession numbers OM177246-OM177262, OM177185-OM177187 and OM200080-OM200086).

Table 1

Prevalence (P ± CI %), mean abundance (A ± CI) and mean intensity (I ± CI) of metazoan parasites in 20 immatures of Mustelus asterias, and ecological parameters: ICES area, microhabitat (MH) and infection pathway according to Joyeux and Baer (1936), Dogiel et al. (1958), Diaz (1971), Gibson and Bray (1977), Caira and Ruhnke (1991), Pascual et al. (1996), Palm and Walter (2000), Lom and Dykova (2006), Moravec (2007), Isawa (2008), Jensen and Bullard (2010) and Tedesco et al. (2020a). Different letters (a, b, c, d) indicate statistically significant differences between parasite taxa for each parasitological descriptor (P, A and I). ES = esophagous-stomach, D = duodenum, G = gills, SV = spiral valve, HI = intermediate host. Myxosporeans were not numbered.

Table 2

Molecular identification of 27 nematodes from Mustelus asterias immatures: comparison of 18S and ITS2 sequences with previously published data in GenBank.

3.2 Parasites as potential biological indicators

All the 20 specimens of M. asterias were immature based on their size (Tab. 3) and comprised seven females and 13 males. Despite the relatively low and unbalanced sample size between females and males, no significant differences occurred between sexes in total mass, total length and body condition indices HSI and K (RDA: F = 1.250, P = 0.299; t tests: t = 0.679, 0.277, 1.883 and 1.128 respectively, all df = 18, P ≥ 0.076), as well as in total parasite abundance (χ2 = 0.814, df = 1, P = 0.367) and number of parasite taxa (χ2 = 0.215, df = 1, P = 0.643) (Tab. 3). Except the four rare taxa of cestodes found in a single host individual, females and males harboured the same taxa of metazoan parasites (eight in common) (Tab. 4). However, the parasitic assemblage significantly differed between sexes in terms of prevalences (F = 2.914, P = 0.007) and abundances (F = 3.018, P = 0.011) (Tab. 4, Fig. 2). In particular, the cestode Eutetrarhynchus sp. was clearly both more prevalent and more abundant in males than in females, whereas the gill monogenean E. laevis and the cestode Anthobothrium sp. were significantly more abundant in females than in males (Tab. 4, Fig. 2, and Tab. S1). The prevalence of E. laevis tended also to be higher in females than in males (Fig. 2a).

Table 3

Biometrics [total mass (TM, g) and length (TL, cm), body condition indices (Hepato-Somatic Index HSI and Fulton's K)] and parasitological parameters [total prevalence (P, %), mean abundance (A), mean taxa richness (R), and number of metazoan parasite taxa] (± CI) in 20 immatures of M. asterias (7 females and 13 males). Mean abundance of metazoan parasites equals mean intensity because prevalence equals to 100% whatever the sex. No significant differences between sexes occur in biometrics and parasitological parameters.

Table 4

Community of metazoan parasites in Mustelus asterias according to the sex: total prevalence (P ± CI %), mean abundance (A ± CI) and mean intensity (I ± CI) of metazoan parasites in immature females (7) and immature males (13). Myxosporeans were not numbered.

thumbnail Fig. 2

A) Redundancy analysis (RDA) performed on the parasite community (Hellinger-transformed presence-absence data). Individual coordinates on the RDA constrained axis scaled to [-1;1] (circles) and sexes placed at the mean of the corresponding individuals (squares and names). Arrows show correlations of each parasite taxon with the RDA constrained axis (bold arrows for |r| > 0.5). P-values on the left show results of univariate Likelihood ratio tests. B) Same as A for abundance data (Hellinger-transformed data, univariate F tests).

3.3 Parasites and host condition

When considering the total number of metazoan parasites, no significant relationship was detected between the parasite abundance and the total length, total mass or condition indices (HSI and K) of M. asterias, whatever taking or not into account the sex (Fig. 3, Tabs. S2–S7). However, some relationships were significant when considering parasite taxa separately (Fig. 3, Tabs. S2–S7). Indeed, the abundance of the nematode P. obtusus was negatively related to K considering all individuals or males only (not females); and for males only, the prevalence of P. obtusus was negatively related to the total length and total mass (Figs. 3A and 3B). A negative relationship was also found for males only between the prevalence of the copepod K. lineata and K (Fig. 3B). On the contrary, positive relationships occurred between gill myxosporean prevalence and HSI considering all individuals (Fig. 3), and for females only, between the prevalence of the nematode A. rotundatus and total mass, and between its abundance and both total length and total mass (Fig. 3C). Finally, considering all individuals, contrasting relationships occurred for the monogenean E. laevis: its prevalence was negatively related to total length whereas its abundance was positively related to HSI (Fig. 3A).

thumbnail Fig. 3

Relationships between host condition and parasite prevalence (left) or abundance (right), for all individuals (A), males only (B) and females only (C). Effect sizes are represented, with symbols depicting results of the corresponding F tests (∼ < 0.1, * < 0.05, ** < 0.01). Effect sizes for the impact of parasites' presence are regression coefficients of the Linear Model (LM) linking parasite presence (binary factor) with centered-scaled condition parameters. Effect sizes for the impact of parasites' abundance are standardized regression coefficients, i.e., regression coefficients of the LM linking centered-scaled parasite abundance with centered-scaled condition parameters.

4 Discussion

4.1 Metazoan parasite community of M. asterias juveniles

Our study demonstrates for the first time the importance to take into account the parasitofauna of M. asterias in further investigations since all the specimens were infected despite their immature stage (McCully Phillips and Ellis, 2015) and the relatively low sample size of 20 individuals. It is worthy to note that both parasitic load and diversity are expected to be greater for adults (vs immatures) of M. asterias, based on the increasing probability of meeting parasites with age (Polyanski, 1958) and the strong positive correlation between maximum parasite biomass and host mass (Poulin and George-Nascimento, 2007).

In total, we recorded 12 metazoan parasite taxa (one monogenean, one trematode, six cestodes, two nematodes, one copepod, and one myxosporean) in immature sharks (Tab. 1). Among them, seven taxa were already described in adults of M. asterias, i.e., K. lineata, E. laevis, Anthobothrium sp., Proleptus sp. (Henderson et al., 2003); Heteronybelinia robusta (Palm and Walter, 2000); Phyllobothrium sp. (Ruhnke, 2011); Symcallio leuckarti (Bernot et al., 2016). The other parasite taxa are a priori new records for M. asterias, previously registered in the closely related M. mustelus (Acanthocheilus rotundatus, Eutetrarhynchus sp., Ptychogonimus megastomum) (Petter et al., 1991; Gračan et al., 2014) and Mustelus manazo (Orygmatobothrium sp.) (Yamaguchi et al., 2003), apart from the unknown Myxosporea. To date, only 20 species of Myxosporea have been described in Carcharhiniformes, but not on the host gills, and a large number of Myxosporea species certainly remains to be discovered (Lom and Dyková, 2006; MacKenzie and Kalavati, 2014 for reviews). Moreover, we did not find Calliobothrium wightmanorum, a cestode described in each of the 11 adults of M. asterias (78–109 cm TL) from the North Sea by Bernot et al. (2016), possibly due to the age difference with our immature specimens (55–70 cm). Overall, further molecular systematic investigations are needed to specifically identify all metazoan parasites and assess new records, as demonstrated by our DNA sequences for A. rotundatus, recorded for the first time in M. asterias.

The diversity of metazoan parasites we found in immature M. asterias is of the same order than for M. manazo (life stage and size not mentioned) in which Yamaguchi et al. (2003) recorded 13 taxa (eight cestodes, one nematode, two myxosporeans, and two copepods), but from 1038 host specimens examined. Moreover, prevalences of each parasite taxon recorded in M. asterias (from 5% to 75%) appear higher than for M. manazo (from 0 to 41%) (Yamaguchi et al., 2003). Some parasitological studies focused on helminths from the digestive tract of adult Mustelus spp. (Cisio and Caira, 1993; Gračan et al., 2014). According to these studies, Mustelus canis (16 females and 28 males of 43–123 cm TL) harboured four species of cestodes (Cisio and Caira, 1993), whereas M. mustelus (six females and nine males of 101.1 ± 27.3 cm TL, range 50.5–152.5 cm) hosted four helminth taxa (among them three recorded in our study): one nematode, two cestodes and one trematode (Gračan et al., 2014). In comparison, helminths found in the digestive tract of M. asterias immatures are more diverse with nine taxa recorded, despite the difference in host size/age. However, the total prevalence and the mean intensity of gastro-intestinal helminths were of the same order for M. asterias (95% and 13 ± 5 helminths per host) and M. mustelus (87% and 29 helminths per host) (Gračan et al., 2014).

The community of metazoan parasites of immature M. asterias includes three core (dominant) taxa, five secondary taxa and four satellite taxa (i.e., cestodes in the spiral valve).

The most prevalent species (75%) is the nematode A. rotundatus, which is a priori a first record for M. asterias. This dominant species is widely distributed (North Sea, Adriatic Sea, Mediterranean Sea, North Pacific Ocean) and occurred in closely related species such as M. mustelus, Mustelus griseus, M. manazo and G. galeus (Diaz, 1971; Petter et al., 1991; Moravec and Nagasawa, 2000; Yamaguchi et al., 2003). The two-host life cycle comprises the hermit crab Pagurus prideauxi as intermediate host ingested by the elasmobranch definitive host (Diaz, 1971). Both prevalence (50%) and intensity (1–15) of P. prideauxi reported on the French Mediterranean Coast (Sète) are relatively high, suggesting it is the main intermediate host of A. rotundatus (Diaz, 1971). Pagurus spp. such as P. prideauxi and P. bernhardus are common in the North-East Atlantic where they are the main prey species ingested by M. asterias at Plymouth, UK, i.e., found in 64.6% of 48 stomachs (a priori of male adults) and representing 24.6% of the diet (Ford, 1921). In the Irish Sea, Pagurus spp. constitute 7.1% of the preys ingested by M. asterias (46 individuals of 72.2 ± 18.7 cm total length, range 43–100 cm) (Ellis et al., 1996).

The second most prevalent parasite (70%) is the cestode Eutetrarhynchus sp., already found in M. mustelus (Gračan et al., 2014), and possibly belonging to the type species, Eutetrarhynchus ruficollis, described before modern taxonomy in M. asterias on the French coast (Joyeux and Baer, 1936). E. ruficollis parasitizes decapods as second intermediate host, mostly crabs, i.e., Cancer pagurus, Carcinus maenas, Liocarcinus depurator, Hyas araneus, Pachygrapsus marmoratus, Inachus dorsettensis, Macropodia longirostris, and pagures, i.e., Eupagurus bernhardus (Joyeux and Baer, 1936; Ginetsinskaya, 1958). These prey species frequently occur in the stomach of M. asterias where crabs and pagures constitute respectively up to 70% and 25% of the diet in the Northeast Atlantic (Ford, 1921; Ellis et al., 1996).

The third most prevalent species (60%) is the blood-feeder gill monogenean Erpocotyle laevis, already recorded from M. asterias in the Northeast Atlantic (Henderson et al., 2003). The life cycle is direct and swimming larval oncomiracidia actively attach themselves on gill lamellae of fish host where sexual reproduction of the monogenean parasite occurs (Ginetsinskaya, 1958).

The five secondary parasite taxa whose prevalence varied from 15% to 35% correspond to two branchial parasites (the copepod K. lineata and the unidentified myxosporean) and three trophically-transmitted helminths (the cestode Anthobothrium sp., the digenean trematode P. megastomum and the nematode P. obtusus). These taxa are a priori first records for M. asterias except K. lineata and Anthobothrium sp. already recorded by Henderson et al. (2003) in the Irish Sea. These authors also found Proleptus sp. in M. asterias but without species identification. As for E. laevis, the direct life cycle of K. lineata comprises free-living infective larvae (copepodid stage) that actively attach themselves on gill lamellae of M. asterias (Raibaut et al., 1998). It is different for heteroxenous myxosporeans for which actinospores, discharged from an annelid definitive host into water, randomly encounter the fish intermediate host (Lom and Dyková, 2006). Regarding the gastro-intestinal helminths, the intermediate hosts preyed by the shark definitive host are mainly crabs (e.g., Portunus sp.) for P. megastomum (Gibson and Bray, 1977) and various crabs and pagures (i.e., C. maenas, E. bernhardus, H. araneus and Pachygrapsus marmoratus) for P. obtusus (Moravec, 2007), but teleosts and cephalopods for Anthobothrium sp. (Jensen and Bullard, 2010; Tedesco et al., 2020a).

The four satellite taxa (prevalence of 5%), i.e., the cestodes H. robusta, Phyllobothrium sp., S. leuckarti and Orygmatobothrium sp., were already described in M. asterias or in M. manazo for the latter (Ruhnke, 2011; Palm and Walter, 2000; Yamaguchi et al., 2003; Bernot et al., 2016). In contrast with the wide geographical and low host specificity of tentaculariid trypanorhynchs such as H. robusta (Palm and Walter, 2000), the three tetraphyllideans are specific of the Mustelus genus (Barker et al., 1984; Ruhnke, 2011; Bernot et al., 2016). The second intermediate host of H. robusta may be various teleosts (Palm and Walter, 2000), whereas a great variety of cephalopod species have been found infected by larval plerocercoids of Phyllobothrium sp. (Pascual et al., 1996), but only the octopod Eledone moschata for Orygmatobothrium sp. (Joyeux and Baer, 1936). To our knowledge, the life cycle is unknown for S. leuckarti. However, Calliobothrium verticillatum, a closely related species to S. leuckarti infecting M. mustelus and M. canis as definitive hosts, uses Pagurus pollicaris, and possibly C. maenas, as second intermediate hosts (Joyeux and Baer, 1936; Caira and Ruhnke, 1991).

4.2 Parasites as potential biological indicators

The taxonomically diverse metazoan parasites hosted by M. asterias may provide a wide variety of information and be potentially used as biological tags, as shown for many teleost species but scarcely for elasmobranch species (MacKenzie, 2002; Marcogliese, 2005; Poulin and Kamiya, 2013; Catalano et al., 2014 for reviews). In that respect, Yamaguchi et al. (2003) demonstrated the feasibility of using helminth parasites, in particular cestodes, for the identification of different host stocks of M. manazo.

Interestingly, our study on immatures of M. asterias highlights differences in the distribution patterns of the parasitofauna according to the sex, even if the same parasite taxa occurred in males and females apart from rare cestodes. In particular, three helminths, i.e., the gill monogenean E. laevis and the gut cestodes Eutetrarhynchus sp. and Anthobothrium sp., were of interest due to significant inter-sex differences in their prevalence and/or abundance.

E. laevis was nearly thrice more abundant and tended to be twice more prevalent in females than in males. Several reasons may explain these differences. First, immune response and susceptibility to parasite infection may be different between sexes, possibly in relation with the more or less attractiveness of mucus covering the gills and with humoral immune factors and immune cells contained in gill tissues (Ilgová et al., 2021 for review). Second, immature females may be more exposed than immature males to infective oncomiracidia of E. laevis, possibly due to differences in their spatial distribution. Information suggested by E. laevis patterns is in accordance with spatial segregation by sex demonstrated for adults of M. asterias in the Northeast Atlantic, where females disperse across a wider geographic range than males (Brevé et al., 2016, 2020; Griffiths et al., 2020). Some gill monogeneans such as Mazocraes alosae and Dactylogyrus sp. have been already found to discriminate fish host species or hybrids with different spatial distribution (Dupont and Crivelli, 1988; Gérard et al., 2016). In the same way, E. laevis may constitute a valuable marker of spatial segregation between males and females of M. asterias at an immature stage.

In contrast to monoxenous E. laevis, Eutetrarhynchus sp. and Anthobothrium sp. are heteroxenous and trophically-transmitted, and therefore may be indicative of inter-sex differences in preys consumed by M. asterias immatures, and more generally in feeding ecology and habitat use.

Eutetrarhynchus sp., the dominant taxon of the parasite community in males, was both thrice more prevalent and twice more abundant than in females. These differences suggest that immature males ingest more frequently and in higher quantity the second intermediate host species of Eutetrarhynchus sp., and therefore are more exposed to parasite infection. Another explanation may be that male and female immatures forage in different habitats varying in food resource availability and parasite infection risk.

Contrarily to Eutetrarhynchus sp., Anthobothrium sp. was more abundant in immature females than in immature males, but similarly prevalent in both sexes. It suggests that the second intermediate hosts of Anthobothrium sp. preyed by immature females were more heavily infected than those ingested by immature males, and possibly originated from different areas. Immature females of M. asterias may be more pelagic vs immature males more benthic, since pelagic sharks eat more teleosts and cephalopods, and less crustaceans than benthic ones [database on the diet of 29 shark species (Capapé, 1975)].

The inter-sex differences in the infection patterns of E. laevis, Eutetrarhynchus sp. and Anthobothrium sp. strongly suggest different spatial distribution and habitat use of male and female immatures. Therefore, these three helminth taxa may constitute useful tags of spatial segregation between males and females at immature stage. Despite recent studies on M. asterias distribution and the demonstration of sex-biased dispersal (Brevé et al., 2016, 2020; Griffiths et al., 2020), knowledge on immatures is lacking. Predicted suitable habitats of M. asterias immatures generally coincide with those of adults but sex of immatures was not identified in available data (Brefeld and Meyer, 2018). Thus, potential differences in behaviour, migrations and diet ecology of M. asterias according to both developmental stage and sex should be further investigated for a better understanding and use of information provided by parasite taxa of M. asterias.

Our data on trophically-transmitted parasites (nine taxa) also underline high resemblances in the diet of immature males and females of M. asterias, such as the importance of preying crabs and pagures [already described by Ford (1921), Capapé (1975) and Ellis et al. (1996)] based on the occurrence in both sexes of Eutetrarhynchus sp., A. rotundatus, P. obtusus and P. megastomum. Moreover, the occurrence of Orygmatobothrium sp. in females and of Phyllobothrium sp. in males, even rare, proves the consumption of cephalopods, not mentioned among the preys of M. asterias in the Northeast Atlantic (Ford, 1921; Ellis et al., 1996), but recorded in the Tunisian coast, i.e., Sepia officinalis and E. moschata (Capapé, 1975). Concerning teleosts, the record of two specimens of H. robusta in one male of M. asterias proved that teleosts may be preyed by males (Palm and Walter, 2000). We cannot assess that females of M. asterias from our study have ingested teleosts based on the occurrence Anthobothrium sp. since second intermediate hosts may be both cephalopods and teleosts (Jensen and Bullard, 2010; Tedesco et al., 2020a). According to stomach analysis, teleosts are rarely consumed by M. asterias in the Northeast Atlantic where they constitute only 2% of its diet (Ellis et al., 1996) or are not found (Ford, 1921), whereas 11 species of teleosts are distinguished in the stomach contents of M. asterias in the Tunisian coast (Capapé, 1975). Further studies on the relationships between parasitofauna and diet of M. asterias at different ages of both sexes and from different geographical areas are needed to increase knowledge and make the best use of parasites as host biological tags.

4.3 Parasites and host condition

Whatever host-parasite combination, parasites and their hosts compete for resources in such way that host survival and fecundity could be affected, even if no pathology is obvious and even if this effect may be drowned in the background noise of all other factors that affect these life-traits (Thomas et al., 2007; Robar et al., 2010; McElroy and De Buron, 2014 for reviews). Metazoan parasites are ubiquitous natural stressors inducing a host fitness loss, with more or less pathogen effects depending, among several factors, on host life stage, infected organs/tissues and parasite load, most parasites being pathogen by accumulation (Bauer, 1958; Woo, 2006; Thomas et al., 2007; Robar et al., 2010; McElroy and De Buron, 2014 for reviews). The body condition can be used as a proxy of fitness to evaluate the severity of parasite infection (e.g., Neff and Cargnelli, 2004; Bean and Bonner, 2009; Gérard et al., 2013, 2017; Ryberg et al., 2020). Here, we obtained contrasting results depending on the parasite taxa considered, and we demonstrated a clearly negative relationship between parasites and host condition for the gill copepod K. lineata and the gut nematode P. obtusus, suggesting they induced a host fitness loss.

Gill parasites, including the three taxa found in M. asterias, can result in lesions that facilitate infections by various opportunist pathogens (virus, bacteria, and fungi), and, in case of blood-feeders such as copepods and polyopisthocotylid monogeneans, in potentially lethal anemia (Bauer, 1958; Woo, 2006 for reviews). Moreover, severe hyperplasic lesions of gills can also reduce or block the respiratory water flow over lamellae, and reduce gas and ion exchange across the lamellar epithelium, as demonstrated for sharks highly infected by the blood-feeder monogenean Erpocotyle tiburonis (about 100 parasites per fish) (Bullard et al., 2001). The death of two aquarium-held M. asterias adults was attributed to respectively 50 and 70–90 specimens of Erpocotyle sp. on the gills (MacKenzie and Smith, 2016). In our study, the parasitic load of E. laevis in immature M. asterias was lower (up to 26 monogeneans per host) and no negative impact was evident since contrasting correlations occurred, i.e., prevalence negatively related to total length but abundance positively related to HSI. By contrast, the negative relationship between the hematophagous K. lineata and host condition was clearly assessed, but only for males. Among them, two males harbored intense infections on their gills, with respectively 101 and 155 copepods, probably inducing respiration impairment and anemia. Regarding the unknown Myxosporea, the positive relation only between its prevalence and HSI is difficult to interpret since myxosporeans may cause necrosis and destruction of gill tissues (Bauer, 1958; Lom and Dyková, 2006). According to our results, multiple infections of gill parasites frequently occur on the same host individual, i.e., 77% with two taxa, 15% with three taxa, and probably induce cumulative pathogen effects on M. asterias. This issue needs to be explored in further investigations.

Pathogen effects can also occur due to helminth parasites in the digestive tract, such as the nine taxa recorded in M. asterias (nematodes, cestodes and trematodes). Indeed, parasitic helminths may lead to obstruction of the lumen of the gut and damage to its wall, and have an impact on the host's physiology and nutrition (Bauer, 1958; Petkevičius, 2007 for reviews). Some of them such as spirurine nematodes are especially pathogenic and known as causative agents of serious fish diseases (Moravec, 2007 for review). Due to host-parasite competition for resources, gastro-intestinal helminths reduce the host reserves from their own gain and commonly induce weight loss and lower condition (e.g., Bean and Bonner, 2009; Gérard et al., 2017; Ryberg et al., 2020). In our study, M. asterias immatures hosted up to 43 helminths in their digestive tract with a mean of 13 ± 5 worms per host, probably resulting in a decrease of energy available for the host with side-effects on its life traits. The spirurine nematode P. obtusus was the single helminth species negatively related with host condition (K), and in case of males, with host total mass, suggesting a negative impact on host health. P. obtusus is known to induce histopathogeny since repeated attachment to the gut wall, toxic secretions and external digestion of host tissues by the nematode result in lesions, ulcerations and hemorrhage (Schuurmans Stekhoven and Botman, 1932). No negative relationship was obvious for the other nematode A. rotundatus for which, in case of females only, prevalence and abundance were even positively related with host total mass. Here again, we need further parasitological studies to understand these results.

5 Conclusions

To conclude, our study describes for the first time the widely diverse and significant community of metazoan parasites of M. asterias at an immature stage. We demonstrate a negative relationship between host condition and parasitism by K. lineata and P. obtusus in immature sharks, suggesting a pathogeny that may compromise future reproduction and/or affect reproductive success. Even if host fitness loss was not obvious for the other taxa of metazoan parasites, one can expect a severe impact of gill and gut metazoan parasites on the health of the most heavily infected M. asterias individuals or those infected by especially harmful parasites, with potential consequences at the population level. Parasitism is ubiquitous and an additional stress that may regulate host populations (e.g., Esch et al., 1997; Knudsen et al., 2002; Frainer et al., 2018). Therefore, it is crucial to understand complex host-parasite relationships and cumulative pathogen effects depending on parasite taxa, host characteristics (life stage, sex) and environmental factors, and to know how metazoan parasites may contribute to the decline of vulnerable host species. Moreover, we demonstrated the use of some parasite taxa to increase knowledge on host feeding ecology and spatial distribution. Since conflicting results occur about the existence of a single biological stock unit for M. asterias (McCully Phillips and Ellis, 2015; Brevé et al., 2016; ICES WGEF, 2019), parasites may help to discriminate sub-populations and to assess the metapopulation-like stock structure. Another aspect to consider in further research is the bioindication by parasitic helminths of environmental pollutants such as heavy metals, which accumulate more in parasites than in host tissues (De Buron et al., 2009 for review), as demonstrated for Anthobothrium sp. infecting the shark Carcharhinus dussumieri (Malek et al., 2007). Parasites are ubiquitous but rarely incorporated into framework, despite they may constitute a confounding factor leading to biased interpretations if not accounted for (Frainer et al., 2018; Timi and Poulin, 2020 for reviews). Thus, future research must include parasitological studies in multidisciplinary research programs on M. asterias in order to improve the efficiency of sustainable conservation and management strategies.

Acknowledgments

This study was funded by the Marine Fishery and Aquaculture Department (DPMA) of the French Ministry for Agriculture and Food. We thank the national survey “Elasmobranch On Shore” (EOS, 2014-2021) and the program “Raie Brunette” (2017–2020) funded by the European Maritime and Fisheries Fund (FEAMP) for providing the starry smooth-hounds. We also thank the Service of Marine Station from the National Museum of Natural History (CRESCO, Dinard) for sharing working space for dissections. We gratefully acknowledge A. Carpentier and S. Mayot for their technical assistance during fish dissections and data management, as well as T. Cribb (Centre for Marine Studies, Univ. Queensland, Australia) for his help with the identification of digenean parasites, and V. Briand (UMR ECOBIO 6553) for her bibliographical support.

Appendix A

Appendix comprises seven tables that detail statistical results. Table A1 Effect of host sex on the prevalence and abundance of parasite taxa with total prevalence >5%. Table A2 Effect of parasites' prevalence on host biometrics and body condition (both sexes confounded). Table A3 Effect of parasites' abundance on host biometrics and body condition (both sexes confounded). Table A4 Effect of parasites' prevalence on host biometrics and body condition (males only). Table A5 Effect of parasites' abundance on host biometrics and body condition (males only). Table A6 Effect of parasites' prevalence on host biometrics and body condition (females only). Table A7 Effect of parasites' abundance on host biometrics and body condition (females only).

Table A1

Effect of host sex on the prevalence and abundance of parasite taxa with total prevalence > 5 %. Prevalence: likelihood ratio test on generalized linear models (distribution: binomial, link function: logit). Abundance: F tests on generalized linear models (distribution: quasi-Poisson, link function: log).

Table A2

Effect of parasites' prevalence on host biometrics and body condition (both sexes confounded). F tests on linear models.

Table A3

Effect of parasites' abundance on host biometrics and body condition (both sexes confounded). F tests on linear models.

Table A4

Effect of parasites' prevalence on host biometrics and body condition (males only). F tests on linear models.

Table A5

Effect of parasites' abundance on host biometrics and body condition (males only). F tests on linear models.

Table A6

Effect of parasites' prevalence on host biometrics and body condition (females only). F tests on linear models.

Table A7

Effect of parasites' abundance on host biometrics and body condition (females only). F tests on linear models.

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Cite this article as: Gérard C, Hervé MR, Hamel H, Gay M, Barbier M, Barreau T. 2022. Metazoan parasite community as a potential biological indicator in juveniles of the starry smooth-hound Mustelus asterias Cloquet, 1819 (Carcharhiniformes Triakidae). Aquat. Living Resour. 35: 3

All Tables

Table 1

Prevalence (P ± CI %), mean abundance (A ± CI) and mean intensity (I ± CI) of metazoan parasites in 20 immatures of Mustelus asterias, and ecological parameters: ICES area, microhabitat (MH) and infection pathway according to Joyeux and Baer (1936), Dogiel et al. (1958), Diaz (1971), Gibson and Bray (1977), Caira and Ruhnke (1991), Pascual et al. (1996), Palm and Walter (2000), Lom and Dykova (2006), Moravec (2007), Isawa (2008), Jensen and Bullard (2010) and Tedesco et al. (2020a). Different letters (a, b, c, d) indicate statistically significant differences between parasite taxa for each parasitological descriptor (P, A and I). ES = esophagous-stomach, D = duodenum, G = gills, SV = spiral valve, HI = intermediate host. Myxosporeans were not numbered.

Table 2

Molecular identification of 27 nematodes from Mustelus asterias immatures: comparison of 18S and ITS2 sequences with previously published data in GenBank.

Table 3

Biometrics [total mass (TM, g) and length (TL, cm), body condition indices (Hepato-Somatic Index HSI and Fulton's K)] and parasitological parameters [total prevalence (P, %), mean abundance (A), mean taxa richness (R), and number of metazoan parasite taxa] (± CI) in 20 immatures of M. asterias (7 females and 13 males). Mean abundance of metazoan parasites equals mean intensity because prevalence equals to 100% whatever the sex. No significant differences between sexes occur in biometrics and parasitological parameters.

Table 4

Community of metazoan parasites in Mustelus asterias according to the sex: total prevalence (P ± CI %), mean abundance (A ± CI) and mean intensity (I ± CI) of metazoan parasites in immature females (7) and immature males (13). Myxosporeans were not numbered.

Table A1

Effect of host sex on the prevalence and abundance of parasite taxa with total prevalence > 5 %. Prevalence: likelihood ratio test on generalized linear models (distribution: binomial, link function: logit). Abundance: F tests on generalized linear models (distribution: quasi-Poisson, link function: log).

Table A2

Effect of parasites' prevalence on host biometrics and body condition (both sexes confounded). F tests on linear models.

Table A3

Effect of parasites' abundance on host biometrics and body condition (both sexes confounded). F tests on linear models.

Table A4

Effect of parasites' prevalence on host biometrics and body condition (males only). F tests on linear models.

Table A5

Effect of parasites' abundance on host biometrics and body condition (males only). F tests on linear models.

Table A6

Effect of parasites' prevalence on host biometrics and body condition (females only). F tests on linear models.

Table A7

Effect of parasites' abundance on host biometrics and body condition (females only). F tests on linear models.

All Figures

thumbnail Fig. 1

Geographical position of the three ICES areas in the North-East Atlantic where Mustelus asterias was caught: VIId (Eastern Channel), VIIe (Western Channel) and VIIf (Bristol Channel).

In the text
thumbnail Fig. 2

A) Redundancy analysis (RDA) performed on the parasite community (Hellinger-transformed presence-absence data). Individual coordinates on the RDA constrained axis scaled to [-1;1] (circles) and sexes placed at the mean of the corresponding individuals (squares and names). Arrows show correlations of each parasite taxon with the RDA constrained axis (bold arrows for |r| > 0.5). P-values on the left show results of univariate Likelihood ratio tests. B) Same as A for abundance data (Hellinger-transformed data, univariate F tests).

In the text
thumbnail Fig. 3

Relationships between host condition and parasite prevalence (left) or abundance (right), for all individuals (A), males only (B) and females only (C). Effect sizes are represented, with symbols depicting results of the corresponding F tests (∼ < 0.1, * < 0.05, ** < 0.01). Effect sizes for the impact of parasites' presence are regression coefficients of the Linear Model (LM) linking parasite presence (binary factor) with centered-scaled condition parameters. Effect sizes for the impact of parasites' abundance are standardized regression coefficients, i.e., regression coefficients of the LM linking centered-scaled parasite abundance with centered-scaled condition parameters.

In the text

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