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Ichthyological note – Note ichtyologique

Range extension: records of denticulatus (: ) caught in the southern Bay

© SFI © of Biscay (NE Atlantic) Received: 2 Dec. 2014 Accepted: 2 Feb. 2015 Editor: R. Causse by

Cristina Rodríguez-Cabello* (1), Guzman Díez (2), Montse Pérez (3) & Rafael Bañón (4)

Résumé. – Signalements les plus méridionaux de Anarhichas den- In the northwestern Atlantic and Canadian Arctic, its range extends ticulatus (Perciformes : Anarhichadidae) capturés dans le sud du from Baffin Bay to the Gulf of Maine including the Labrador and golfe de Gascogne (NE Atlantique). northeast Newfoundland Shelves, the Grand Banks, the Flem- ish Cap, the Gulf of St. Lawrence and the Scotian Shelf. Adults of Deux spécimens adultes d’Anarhichas denticulatus (Krøyer, A. denticulatus are known from depths of 0-1000 m but are more 1845) ont été capturés pour la première fois dans la partie méri- dionale du golfe de Gascogne (Nord-Est Atlantique). Ces nouvel- frequently encountered from 350-750 m (Albikovskaya, 1982). les occurrences permettent d’élargir considérablement vers le sud, This paper reports the capture of two A. denticulatus in the l’aire de répartition de cette espèce et de fournir de plus amples north of Spain (southern Bay of Biscay, NE Atlantic), which consti- informations sur certains aspects de sa biologie. tute new southernmost records from the Eastern Atlantic. Key words. – Anarhichadidae - Anarhichas denticulatus - Bay of Biscay - Northeast Atlantic - New records. MATERIAL AND METHODS

Two specimens of A. denticulatus were captured at differ- The wolffish family Anarhichadidae Bonaparte, 1846 is a small ent locations by gillnetters targeting monkfish (Lophius spp.) in family of blenny-like marine fishes found on rocky and hard bot- the southern area of the Bay of Biscay in May of 2013 and 2014 tom areas of the northern oceans (O’Dea and Haedrich, 2002). It (Fig. 1). The specimens were transported to the laboratory where comprises five species, four of them belonging to the Anarhi- they were identified following Barsukov (1986) and Kulka et al. chas Linnaeus, 1758: broad-head or Anarhichas (2007). Measurements to the nearest millimetre and meristic char- denticulatus (Krøyer, 1845), striped or A. lupus acters were also recorded. In the case of the first wolfish caught in (Linnaeus, 1758), spotted wolffish A. minor (Olafsen, 1772) and 2013, measurements were recorded on the fresh specimen while in the second case the fish had been previously frozen. Muscle tissue Bering wolffish A. orientalis (Pallas, 1814). All Anarhichas spe- of the specimen caught in 2014 was collected for genetic analysis cies are characterized by being large fish reaching over 1 m, a large and stored at 4ºC in 99% ethanol. head, snout rounded and jaws with canine-like teeth in front and Total genomic DNA was extracted from ethanol-preserved conical or rounded teeth at sides and on roof of the mouth. The first muscle tissue using the FENOSALT method (Pérez and Presa, three species are pan-Atlantic, widely distributed in the eastern and 2011). A 425 bp fragment of CYTB (Cytochrome b, mitochondrial western north-Atlantic and the Arctic Oceans. gene) was amplified and sequenced using the primer pair L14735 A. denticulatus is distinguished from the others two Atlantic and H15149AD (Wolf et al., 2000). The molecular identification species by its more uniform dark body colour (sometimes with was made using Basic Local Alignment Search Tool (BLAST, spots), its soft jelly-like musculature, a large head and relatively Zhang et al., 2000) available in GenBank. According to Johnstone smaller jaws in proportion to the body, better suited for a semi- et al. (2007), it is one of the most variable protein-code loci in pelagic diet (Simpson et al., 2013a). Its upper lip thick covered Anarhichas genomes with 4.22 SNPs/100 bp. The specimen caught with papillae and the position of the vomerine teeth relative to the in 2014 was preserved in 70% ethanol and stored in the fish collec- palatine teeth also distinguish it from the other three wolffish spe- tion of the Instituto Español de Oceanografía (IEO) in Santander cies (Barsukov, 1986; Kulka et al., 2007). Moreover, it appears to (IEOST 2014_1_520). have several other morphological and ecological differences (Kulka et al., 2004; González et al., 2006). In the northeast Atlantic, A. denticulatus habitual distribution RESULTS area ranges from Iceland and the Faroe Islands to the waters of Nor- way and the Barents Sea (Barsukov, 1986). Sporadic records have Material examined also been reported in the north of British Islands (Minchin, 1988). Anarhichas denticulatus Krøyer, 1845. (1) Adult specimen (not

(1) Instituto Español de Oceanografía, Promontorio San Martin s/n, Santander 39004, Santander, Spain. (2) Marine Research Division, AZTI, Txatxarramendi s/n, Sukarrieta 48395, Bizkaia, Spain. [[email protected]] (3) Instituto Español de Oceanografía, Subida a Radio Faro, 50, Vigo 36390, Spain. [[email protected]] (4) Servizo de Planificación, Consellería do Mar e Medio Rural, Xunta de Galicia, Santiago de Compostela, Spain. [[email protected]] * Corresponding author [[email protected]]

Cybium 2015, 39(4): 309-312. Anarhichas denticulatus in the Bay of Biscay Ro d r í g u e z -Ca b e l l o e t a l .

Figure 1. - Location of the southern NE Atlantic records of A. denticulatus (in chronological order). 1: Gueguen et al., 1974 ; 2: Du Buit, et al., 1979; 3: Ponomarenko, 1979; 4: Minchin, 1988; 5: GBIF, 1992 (www.gbif.org); 6: MHNH, 1995; 7: Mar-ECO-2004_7137 (www.mar-eco.no); 8: Iglesias, 2014 and the new records (*) caught in the southern Bay of Biscay (present study). The shaded area corresponds to the general distribution of this spe- cies according to Fishbase (Froese and Pauly, 2014). sexed): 111.0 cm TL, weight: 14,360 g, Bay of Biscay, 1 May 2013, 44º13.00’N-2º08.00’W, 650 m depth. Anarhichas denticulatus Krøyer, 1845. (2) Adult female speci- men (Fig. 2): 109.5 cm TL, weight: 12,751 g, Bay of Biscay, 24 May 2014, 43º50.20’N-2º08.50’W, 549 m depth. Figure 3. - Detail of the teeth on vomer and mandible of Anarhichas den- ticulatus female 109.5 cm TL. Diagnostic characters The specimens were identified by: all teeth on vomer and man- length (%SL) were observed in predorsal and preanal length, cau- dible canine-like; the large conical and pointed teeth on vomer did dal and anal fin length and in the interorbital distance. not reach backwards as far as rows of median palatine teeth (Fig. 3); caudal fin length less than twice of caudal peduncle depth; jellylike Genetic analysis texture of the body and coloration bluish-black with indistinct spots The DNA analysis corroborated the identification of A. den- on the sides (Fig. 2). ticulatus. Comparisons were made using the complete mitochon- Morphometric and meristic characters are shown on table I. Fin drial genomes of three species of wolffish and the 425 bp fragment ray counts were: c.a. 77 dorsal, 18 pectoral, 22 caudal and c.a. 42 obtained in this work. Our sequence (all the replicates) perfectly anal. Canine-like teeth in mandible superior and inferior were 4 and matched the available A. denticulatus sequence. The DNA sequence 6 respectively. Main differences in morphometric measurements obtained presented a 100% maximum identity (EF427918.1, A. between both specimens, expressed as percentage of standard denticulatus mitochondrion, complete genome) (Tab. II).

Figure 2. - Anarhichas denticulatus, female 109.5 cm TL caught in the southern Bay of Biscay (NE Atlantic).

310 Cybium 2015, 39(4) Ro d r í g u e z -Ca b e l l o e t a l . Anarhichas denticulatus in the Bay of Biscay

Table I. - Selected morphometric and meristic characters of the two indi- Table II. - Maximum identity results obtained in GenBank (BLAST) data- viduals of Anarhichas denticulatus caught. Values expressed in centimetres base. and in percentage of standard length (% SL). Sequence ID Expect Identities Gaps A.denticulatus (1) A. denticulatus (2) EF427918.1 0.0 425/425 (100%) 0/425 (0%) Morphometric character cm % SL cm % SL EF427917.1 0.0 414/425 (97%) 1/425 (0%) Total Length 111.0 109.5 EF427916.1 0.0 413/425 (97%) 1/425 (0%) Standard length 105.5 100.0 103.5 100.0 Head length 21.8 20.7 21.5 20.8 The stomach of the specimen caught in 2014 contained remains Preorbital length 4.4 4.2 5.0 4.8 of Brachyura, likely Geryon longipes. According to a comparative Postorbital length 14.9 14.1 13.4 12.9 study of wolffish feeding habits, no particular prey item dominated Interorbital distance 3.2 3.0 5.5 5.3 the diet of any Anarhichas species; however the two most important prey groups for Northern wolffish were pelagic fish and benthic fish Eye horizontal diameter 2.5 2.4 3.1 3.0 (Simpson et al., 2013a) rather than benthic crabs as observed here. Predorsal length 17.1 16.2 21.0 20.3 Nevertheless, geographical differences in feeding habits have been Preanal length 58.5 55.5 52.0 50.2 reported in wolffish species and particularly A. denticulatus that Dorsal fin length 85.6 81.1 87.0 84.1 were reported to have some benthic components in its diet (Barsu- Pectoral fin length 13.8 13.1 14.0 13.5 kov and Nizovtsev, 1960; González et al., 2006). Pectoral fin base length 6.1 5.8 6.5 6.3 The analysis of the stomach content revealed that this individ- ual was parasitized with nematodes in the stomach and epithelium Pectoral fin width length 14.6 13.8 13.5 13.0 surrounding the visceral cavity. More than 200 nematodes were Anal fin length 43 40.8 44.0 42.5 counted and identified as larvae L3 of Anisakis simplex. Caudal fin length 8.3 7.9 6.8 6.6 The genetic analysis corroborated the identification of A. den- Caudal fin base length 4.2 4.0 4.0 3.9 ticulatus and is in agreement with those of Johnstone et al. (2007) Caudal fin width length 9.2 8.7 7.0 6.8 and McCusker and Bentzen (2010). Regarding morphometric Girth length n.a 74.0 71.5 measurements, some differences between the two specimens col- lected were observed, which could be due to several factors: vari- Total weight (g) 14360 12751 ability, sex, or the fact that one fish had been previously frozen and was slightly damaged (Fig. 2). According to Simpson et al. (2013b) Meristic character Number sexual dimorphism is observed in certain morphometric and mer- Dorsal fin rays n.a. c.a.77 istic characters in particular: jaw length, eye diameter, caudal fin Pectoral fin rays 22 22 length and pectoral fin length. Most of the measurements recorded in this study were in agreement with those from specimens caught Caudal fin rays 18 18 in Newfoundland and Labrador waters (Simpson et al., 2013b) with Anal fin rays n.a. c.a.42 the exception of anal fin length and pectoral fin width. According Teeth in superior mandible n.a. 4 to these authors some variables such as girth length or interorbital Teeth in inferior mandible n.a. 6 width could be good indicators for identifying different subpopula- tions. These new records of Anarhichas denticulatus in the southern DISCUSSION area of the Bay of Biscay considerably extend the known range of the species and expand its thermal habitat, contribute to increase Previously, scattered records of A. denticulatus in Irish waters the number of northern species caught in these waters (Rodríguez- constituted the southern limit of A. denticulatus in the northeast Cabello et al., 2013) and are interesting to elucidate possible migra- Atlantic (Quigley and Flannery, 1993). The southernmost published tion routes of this species. record from the eastern Atlantic was one specimen caught by bot- tom trawl in the Porcupine Bank on August 1986, at a depth close to 550 m at approximately 52º 00.20’N-13º 15.14’W (Minchin, Acknowledgments. – We would like to thank all the trip of the gillnet ves- 1988), 1228 km far from the second specimen described. sels Peñil Barcena from San Vicente de la Barquera (Cantabria) fishing port This species inhabits offshore waters often in midwater; adults and Almikeko Alba from Bermeo (Basque Country) for their help and col- are also found near the bottom from 60-970 m, mainly 100-900 m laboration in providing this data. and at temperatures of 1.5-4.5º C, although they have been found in water as warm as 9ºC (Albikovskaya, 1982; Barsukov, 1986; Kulka et al., 2004). 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