Onuphis and Aponuphis (Annelida: Onuphidae) from southwestern Europe, with the description of a new species Author Arias, Andrés Author Paxton, Hannelore text Zootaxa 2015 3949 3 345 369 journal article 10.11646/zootaxa.3949.3.3 25ece91c-6566-4122-a406-236f147b58b1 1175-5326 238900 CBEF804D-5FBF-48D2-8CCD-036B70FE6ECD Onuphis anadonae sp. nov. Figures 1–5 ; Table 1 Material examined. Type material. Holotype ( MNCN 16.01/16159) COCACE station: D3 ( 43.85º N , 5.68 ºW ), N. Spain , Cantabrian Sea, Bay of Biscay, 162 m , 89.06 % sand, 4.76 % silt, 6.18 % clay, 29 Jun 1987 ; 1 paratype ( MNCN 16.01/16160) COCACE station: D3 ( 43.85º N , 5.68 ºW ), N. Spain , Cantabrian Sea, Bay of Biscay, 162 m , 89.06 % sand, 4.76 % silt, 6.18 % clay, 29 Jun 1987 ; 1 paratype (AM W.47513) COCACE station: B2 ( 43.70º N , 5.77º W ), N. Spain , Cantabrian Sea, Bay of Biscay, 86 m , 76.84 % sand, 14.95 % silt, 8.21 % clay, 5 Jul 1987 . Type locality . Off Asturias, Cantabrian shelf, 43.85º N , 5.68 ºW , 162 m depth, northern Spain , Bay of Biscay, East Atlantic. Diagnosis. Colour pattern absent on dorsum of anterior chaetigers; peristomium with one brown transverse band. Prostomium almost rounded. Antennae moderately short to chaetiger 3–7; ceratophores strongly ringed with maximum of six to seven rings. Peristomial cirri not exceeding anterior margin of prostomium. First four pairs of parapodia modified, directed slightly anterolaterally with bi-, tri- and quatridentate pseudocompound hooks. Subulate ventral cirri in first four chaetigers; distinct subulate postchaetal lobes in first 10 chaetigers. Subacicular hooks from chaetiger 9. Branchiae as single filament from first chaetiger. Tube parchment-like and externally covered with sand grains and shell fragments. Description. Description based on holotype , with variation of paratypes included. Holotype complete with 223 chaetigers, consisting of two fragments, anterior one with 82 chaetigers and posterior fragment with 141 chaetigers; total length of 145 mm and width at chaetiger 10 (excluding parapodia) of 2.7 mm ( Figs 1 , 3 ). Both paratypes incomplete with 79 chaetigers, 43 mm long and 2.8 mm wide and 62 chaetigers, 37 mm long and 2 mm wide respectively. Body cream coloured in preserved condition with one transverse dorsal pigment band on peristomium ( Fig. 1 ). Prostomium globular with pair of conical frontal lips ( Figs 1 A–C). Large pair of eyespots present, situated between bases of lateral antennae and palps. Palps reaching chaetiger 1–2 with nine basal rings and longer distal one. Lateral antennae reaching chaetiger 6–7 with six basal rings, median antenna reaching chaetiger 3–4 with five basal rings, all three antennae with longer distal ring ( Figs 1 A, 2A, B). Sensory buds of antennae and palps scarce and very inconspicuous, arranged in irregular rows ( Figs 2 E, F). Peristomial cirri inserted distally on peristomium below lateral antennae, shorter than length of peristomium not exceeding anterior margin of prostomium ( Figs 1 C, 2A, C). Anterior chaetigers (1–3) slighty longer than those following ( Figs 1 A, 2C, 3A). First four pairs of parapodia modified, not enlarged, directed slightly anterolaterally, with low prechaetal fold, triangular prechaetal lobe and spindle-shaped postchaetal lobe, longer than base of parapodium; subulate dorsal cirrus about as long as postchaetal lobe, ventral cirrus shorter than postchaetal lobe ( Figs 3 B, C, 4A). Subulate ventral cirri in first four chaetigers and pad-like thereafter. Postchaetal lobe as distinct subulate lobe in first 10 chaetigers, becoming smaller and conical in shape thereafter. Branchiae as single filament, strap-like, from first chaetiger to about chaetiger 180, lacking in last 40 chaetigers (in holotype ). Branchial filament becoming longer from chaetiger 20–22, from chaetiger 29–31 longest three times as long as anterior ones ( Fig. 4 B); then getting smaller by chaetiger 150, being absent from chaetiger 183. Aciculae yellowish with pointed tips, generally three per parapodium. Hooded pseudocompound hooks in first four chaetigers. First two parapodia ( Fig. 3 B) with following chaetal complement going from superior to inferior part of chaetal fan: one simple chaeta, three protruding distal tips of aciculae, three strongly tridentate pseudocompound hooks ( Figs 3 H, I, 4D), two quatridentate ( Fig. 4 E) or tridentate pseudocompound hooks with most proximal denticle much smaller and protruding directly from base of second distal tooth ( Fig. 3 G) and one bidentate pseudocompound hook ( Fig. 3 F). Parapodia 3 and 4 with six pseudocompound tridentate hooks ( Fig. 4 C). Hoods of pseudocompound hooks falcate with pointed tip ( Figs 4 C, D). All hooks of equal thickness without slender long-appendaged ones. Pseudocompound hooks replaced by limbate chaetae from chaetiger 5 ( Fig. 4 F). Pectinate chaetae flat and slightly oblique with seven to nine long teeth each, starting in chaetiger 5 ( Figs 3 J, 4G). Hooded bidentate subacicular hooks from chaetiger 9. Mandibles ( Fig. 3 L) with white calcified cutting plates and slender shafts. Maxillae ( Fig. 3 K) weakly sclerotised; maxillary formula (based on paratype ): Mx I = 1 + 1; Mx II = 8 + 6; Mx III = 5 + 0; Mx IV = 5 + 5; Mx V = 1+1. Mx VI absent. Tube cylindrical in shape, parchment-like and externally covered with sand-grains and shell fragments ( Fig. 1 D). FIGURE 1. Onuphis anadonae sp. nov . Holotype (MNCN 16.01/16159). Photomicrographs. A, anterior end, dorsal view; B, anterior end, ventral view; C, detailed view of prostomium and peristomium; D, tube. Remarks. Onuphis anadonae sp. nov . is characterised by having single strap-like branchiae from chaetiger 1, shared with nine other known Onuphis species (Table 1). It is the only species with bi-, tri- and a few quadridentate pseudocompound hooks. Three other species with single branchiae from chaetiger 1 ( O. amakuensis , O. elegans and O. kammurijamaensis ) have bi- and tridentate pseudocompound hooks in the first four chaetigers, and O. farallonensis has these hooks on chaetigers 4–6. However, O. anadonae sp. nov. differs from these species by lacking any brown bands, spots or other kind of colour pattern on the anterior chaetigers, by presenting bidentate pseudocompound hooks only in the first two chaetigers, instead of in the first four like in other species, as well as quatridentate pseudocompound hooks and by the early origin of the subacicular hooks, starting in chaetiger 9 in O. anadonae sp. nov. and in chaetiger 10–11, in the other species. Onuphis anadonae sp. nov. also differs from these four species in having peristomial cirri shorter than the peristomium, while they are as long as or longer than the peristomial length in the others. Other differences are with respect to the length of the antennae, the maximum number of rings of antennal ceratophores, the number of chaetigers with subulate ventral cirri and their length, and are summarised in Table 1. FIGURE 2. Onuphis anadonae sp. nov . Paratype (MNCN 16.01/16160). Scanning electron micrographs. A, detailed view of prostomium and peristomium, dorsal view; B, detailed view of prostomium, lateroventral view; C, anterior end, lateral view; D, detailed view of nuchal groove; E, detailed view of style of antenna; F, detailed view of a sensory bud of the antenna. c, ceratophore; fl, frontal lip; la, lateral antenna, ma, median antenna; ng, nuchal groove; ll, lower lip; p, palp; up, upper lip. FIGURE 3. Onuphis anadonae sp. nov . Holotype A (MNCN 16.01/16159), paratype B-L (AM W47513). Line drawings. A, anterior end, dorsal view; B, parapodium 2, anterior view; C, parapodium 4, anterior view; D, parapodium 5, anterior view; E, parapodium 20, anterior view; F, bidentate pseudocompound hook, chaetiger 2; G, slighly tridentate pseudocompound hook, chaetiger 2; H, I, tridentate pseudocompound hooks, chaetiger 4; J, pectinate chaeta, chaetiger 5; K, maxillae; L, mandibles. FIGURE 4. Onuphis anadonae sp. nov. Paratype (MNCN 16.01/16160). Scanning electron micrographs. A, parapodium 2, lateral view; B, median chaetigers, lateral view; C, pseudocompound hooks of chaetiger 1; D, detailed view of tridentate pseudocompound hooks of chaetiger 3; E, detailed view of a quatridentate pseudocompound hook of chaetiger 2; F, limbate chaetae from chaetiger 5; G, pectinate chaeta from chaetiger 5; H, subacicular hooks from chaetiger 9. b, branchia; dc, dorsal cirrus; pol, postchaetal lobe; prl, prechaetal lobe; SAH, subacicular hook; vc, ventral cirrus. FIGURE 5. Onuphis anadonae sp. nov. Paratype (MNCN 16.01/16160). Scanning electron micrographs. A, parapodium 5, lateral view; B, median chaetigers, lateral view, arrows point to Epistylis epibionts; C, Epistylis colony on parapodia of anterior body end; D, detailed view of Epistylis sp. showing the corona of cilia and its peduncle. b, branchia; dc, dorsal cirrus; gp, glandular pad; pol, postchaetal lobe; prl, prechaetal lobe; SAH, subacicular hook. Etymology. It is a pleasure to name this species in honour of Professor Nuria Anadón, who in many ways helped to make this study possible. TABLE 1. Comparison of key features and habitats of the Onuphis spp. characterized by having single strap-like branchiae from chaetiger 1. PC, peristomial cirri; PCH, pseudocompound hook; PSL, postchaetal; SAH, subacicular hook; VC, ventral cirrus. Character O. amakuensis O. anadonae O. elegans O.farallonensis O. holobranchiata O. iridescens O.kammurijamaensis O. opalina O. rullieriana O.shirikishinaiensis Maekawa & sp. nov. (Johnson, 1901) Hobson, 1971 Marenzeller, 1879 (Johnson, Maekawa & Hayashi, (Verrill, 1873) (Amoureux, ( Imajima, 1960 ) Hayashi, 1999 1901) 1989 1977) Colour pattern on brown dorsal absent brown reddish brown brown dorsal band and Brown dorsal Light brown dorsal bar Brown dorsal absent Black dorsal bars anterior chaetigers bands dorsolateral spots dorsal bars patches near base of bars bands parapodium Median antenna 8 3-4 2 10 7 9-10 4 5-7 9 5 reaching chaetiger Lateral antennae 8 6-7 5-7 13 11 13-14 7 10-13 12 7 reaching chaetiger Maximum number 8 7 11 12 15 13-14 12 12 16 11 rings on antennal ceratophores Maximum number 11 10 10 8 10 14 9 11 10 9 rings on palpal ceratophores length as long as shorter than as long as longer than longer than longer than longer than longer than longer than as long as peristomium peristomium peristomiun peristomium peristomium peristomium peristomium peristomium peristomiun peristomium Length of VC of as long as PSL shorter than longer than PSL shorter than PSL as long as PSL as long as PSL shorter than PSL as long as PSL as long as PSL longer than PSL modified chaetigers PSL

Chaetigers with subulate VC Chaetigers with subulate PSL Chaetigers with PCH Tip of PCH	4 10 4 bi- and tridentate	4 10 4 bi-, tri- and quatridentate	5 (6) 5 12 (13) 10 4 4 (6) bi- and tridentate bi- and tridentate	4 10 4 tridentate	6 16 4 tridentate	4 11 4 bi- and tridentate	6 (7) 10 4 tridentate	5 (6) 10 (12) 4 tridentate	7 (6-8) 16 7 bi- and tridentate
Slender long- appendaged hooks	absent	absent	present present	absent	absent	present	present	absent	present
Origin of SAH	11	9	10-11 10	11-13	12	11	12-15	12-14	11-13
Type locality Habitat	Amakusa Shimojima Japan E. Pacific intertidal	Cantabrian shelf Spain E. Atlantic 86-162 m	Townsend off Southern Washington California USA USA W. Pacific W. Pacific intertidal and 68 m shallow subtidal	Off Japan E. Pacific 149 m	Off British Columbia USA W. Pacific intertidal and shallow subtidal	Wakasa Bay Japan E. Pacific 72 m	Off New England USA W. Pacific 200 m	English Channel France E. Atlantic 860-1400 m	South Hokkaido Japan E. Pacific intertidal
Reference	Maekawa & Hayashi 1999	present study	Hobson 1971; Hobson 1971 Fauchald 1982; Hilbig 1995	Imajima 1986	Hobson 1971; Fauchald 1982; Hilbig 1995	Maekawa & Hayashi 1989	Fauchald 1982; Imajima 1986	Amoureux 1977; present study	Imajima 1960

Biology and faunal associates. The holotype contains oocytes in its body cavity, ranging from 200 to 250 µm in diameter. Ectosymbiotic microorganisms were found on the surface of the anterior and medial parapodia of O. anadonae sp. nov. ( Figs 5 A, B). These epibionts were identified as peritrich ciliates belonging to the genus Epistylis Ehrenberg, 1830 characterised by forming colonies utilising its noncontractile and longer peduncle or stalk for attachment to the worm cuticle ( Figs 5 C, D). The symbiotic association “onuphid-peritrich” was previously reported for Diopatra marocensis Paxton et al. , 1995 and Onuphis eremita Audouin & Milne-Edwards, 1833 ( Arias et al. 2010 ; Arias & Paxton 2014 respectively) suggesting that this association may occur commonly among onuphid polychaetes. Distribution and ecology. Onuphis anadonae sp. nov. is known from the southern part of the Bay of Biscay (East Atlantic) from the Cantabrian shelf, depth range 86–162 m in sandy substrate. This species was only collected singly at two stations, indicating a very low population density and suggesting that it is apparently a rare species with a restricted distribution in the Bay of Biscay. The specimens previously incorrectly reported as Aponuphis holobranchiata (= Onuphis holobranchiata Marenzeller, 1879 ) from the Basque shelf, northern Spain ( Martínez et al. 2010 ) may also represent O. anadonae sp. nov.