Rajidae

Gérard, Claudia, Trochard, Caroline, Hervé, Maxime R., Hamel, Héloïse, Gay, Mélanie, Barbier, Michel, Trancart, Thomas & Barreau, Thomas, 2024, Communities of metazoan parasites in seven sympatric skate species (Elasmobranchii, Rajidae) from the English Channel and Celtic Sea differing in conservation status, Journal of Fish Biology 105 (3), pp. 975-987 : 978-979

3.1 | Metazoan parasites found in Rajidae

In total, 51% (CI 42–60%) of the skates harbored one to four taxa of metazoan parasites, with a taxa richness of 0.8 ± 0.2 parasite taxa per individual and an abundance of 8.7 ± 4.5 parasites per individual (Tables 2 and 3). According to morphological identification, 11 parasite taxa occurred in the whole sampling of skates: one Myxosporea (unidentified) and one Monogenea ( Rajonchocotyle emarginata ) on gills, and six Cestoda ( Grillotia erinaceus , Tritaphros retzii , and the genera Echeneibothrium , Nybelinia , Onchobothrium , and Rockacestus ) and three Nematoda ( Anisakis simplex , and the genera Phocanema and Proleptus ), all trophically transmitted (Table 2). Based on DNA-sequencing made on 27 isolated nematodes from skates, 20 individuals were molecularly identified, i.e., seven Phocanema krabbei , five Proleptus sp. , four Phocanema azarasi , and four Anisakis simplex s.s. (Table 4). All sequences had an identity percentage with sequences present in the National Center for Biological Information database above 99%, and percentage of coverage was always at least 99% for all sequences (Table 4). All the sequences generated in this study were deposited in GenBank.

A total of 16 new host–parasite associations are documented in Table 2 (in bold).

Parasites were mainly recorded in the digestive tract (38% of the skates, CI 29–47%), then in the body cavity (23%, CI 16–31%) and to a lesser extent on the gills (11%, CI 6–18%). No infections were found in the other organs examined (eyes, skin, heart, and liver).

Trophically transmitted (vs gill) parasites were largely dominant, with prevalence and abundance of 48% (CI 39–57%) and 5.8 ± 2.4 parasites per skate individual, respectively. Among trophically

Rajidae IUCN N Overall P % (CI) Pth% (CI)

Lful Vu 9 100 (70–100) a 100 (70–100) a Lnae LC 15 47 (25–70) bc 33 (15–58) c Rbra NT 21 29 (14–47) c 29 (14–47) c Rcla NT 20 40 (22–61) c 40 (22–61) c Rmic NT 14 93 (69–99) a 93 (69–99) a Rmon LC 21 19 (8–40) c 19 (8–40) c Rund NT 14 79 (52–92) ab 71 (42–60) b

Overall A ± CI Ath ± CI Parasite taxa

29.7 ± 45.1 a 18.6 ± 19.9 a Myxo, Nybe, Asim, Phoc, Prol

7.6 ± 9.8 a 0.9 ± 0.8 b Myxo, Rema, Eche , Geri, Asim, Phoc 0.8 ± 1.0 b 0.8 ± 1.0 b Geri, Asim, Prol

1.9 ± 1.8 b 1.9 ± 1.8 b Eche, Tret, Asim, Prol

28.3 ± 22.9 a 19.3 ± 10.6 a Myxo, Eche, Onch, Asim, Phoc, † Prol 1.3 ± 1.6 b 1.3 ± 1.6 b Eche, Phoc, Prol

9.7 ± 6.9 a 9.4 ± 7.0 a Myxo, Nybe, Onch, Rock, Phoc †

Note: Parasite taxa: Myxosporea (Myxo), Rajonchocotyle emarginata ( Rema ), Echeneibothrium spp. ( Eche), Grillotia erinaceus ( Geri ), Nybelinia spp. ( Nybe), Onchobothrium spp. ( Onch), Rockacestus sp. ( Rock), Tritaphros retzii ( Tret) , Anisakis simplex ( Asim) , Phocanema spp. ( Phoc), Proleptus sp. ( Prol). First records of parasites in bold. N = sample size, CI = confidence interval (95%). Due to the generally high specificity of Cestoda for their definitive host ( Caira and Jensen, 2014 for review), we considered that Eche, Nybe and Onch recorded in several skate species in our study corresponded to several parasite species (one per skate host species). Different letters indicated statistical differences between skate species for each parasitological parameter.

† Both Phocanema azarasi and Phocanema krabbei molecularly identified and recorded for the first time.

et al. (2023)

Parasite taxa MH P% (CI) A ± CI

Myxozoa

Max A Infection pathways

Myxosporea G 9.6 (6.7–19.8) 3.52 ± 3.29 100 Random contact with spores

Monogenea

Rajonchocotyle emarginata G 1.1 (0.2–5.8) 0.01 ± 0.02 1 Active attachment on gill lamellae

Cestoda

Echeneibothrium spp. SV 7.9 (4.2–14.3) 0.30 ± 0.29 15 Ingestion of crustaceans, teleosts (Hi2, Hp)

Grillotia erinaceus ES, SV 3.5 (1.4–8.7) 0.04 ± 0.05 2 Ingestion of teleosts (Hi2)

Nybelinia spp. ES, SV 7.9 (4.2–14.3) 0.46 ± 0.43 20 Ingestion of cephalopods, fish (Hi2)

Onchobothrium spp. SV 7.9 (4.2–14.3) 0.15 ± 0.11 4 Ingestion of crustaceans, cephalopods, fish (Hi2, Hp) Rockacestus sp. SV 0.9 (0.2–4.8) 0.01 ± 0.02 1 Ingestion of benthic invertebrates, fish (Hi2, Hp)

Tritaphros retzii SV 0.9 (0.2–4.8) 0.01 ± 0.02 1 Ingestion of teleosts (Hi2)

Nematoda Anisakis simplex BC, SV 9.6 (5.5–16.5) 1.05 ± 1.05 55 Ingestion of crustaceans, cephalopods, fish (Hi, Hp)

Phocanema spp. a BC 18.4 (12.4–26.5) 3.04 ± 1.67 56 Ingestion of crustaceans, cephalopods, fish (Hi, Hp) Proleptus sp. ES 14.0 (8.8–21.6) 0.74 ± 0.61 30 Ingestion of decapods (Hi)

Abbreviations: BC, body cavity; CI, confidence interval (95%); ES, esophagous and stomach; G, gills; Hd, definitive host; Hi, intermediate host; Hp, paratenic host; SV, spiral valve.

a Two species of Phocanema were molecularly identified ( P. azarasi and P. krabbei ).

transmitted parasites, nematodes were the most prevalent infecting 37% (CI 29–46%) of the skates with an abundance of 1.6 ± 1.2 parasites per individual, followed by cestodes for which total prevalence and abundance were, respectively, 25% (CI 18–33%) and 0.2 ± 0.2 parasite per individual. The dominant taxa of metazoan parasites were, in decreasing order, the nematodes Phocanema spp. , Proleptus sp. , and Anisakis simplex , each taxon being encountered in five of the seven skate species (Tables 2 and 3).