Onuphis pancerii Claparède, 1868 Emended

Arias, Andrés & Paxton, Hannelore, 2014, Hidden diversity within the polychaete Onuphis eremita sensu lato (Annelida: Onuphidae) — redescription of O. eremita Audouin & Milne-Edwards, 1833 and reinstatement of Onuphis pancerii Claparède, 1868, Zootaxa 3861 (2), pp. 145-169 : 158-164

Onuphis pancerii Claparède, 1868 Emended

Figures 8–12 ; Tables 2 , 3

Onuphis pancerii Claparède, 1868: 438 –440, pl. VIII fig. 1; 1870: 387, pl. V fig. 5a; Rioja, 1918: 39, fig. 10 (Santander Bay, Spain).

Onuphis eremita — Fauvel, 1923 (in part): 413–415, fig. 163. Not Audouin & Milne Edwards, 1833.— Paxton, 1986: 56 –58, figs. 3, 6–8, 10.

Material examined. Neotype: Non-type specimens: Naples, Italy, specimen Num. 173 from the Rioja Collection 1894–1917 ( MNCN 16.01/311); Naples, Italy, McIntosh Collection, 3 specimens ( BMNH 1921.5.1.832-34); Naples, Italy, 4 specimens ( BMNH 1923.11.19.25-8); Enmedio sandy flat, Santander Bay, Spain, specimens Num. 686 from the Rioja Collection 1894–1917 (in part), 9 specimens ( MNCN 16.01/310); Enmedio sandy flat, Santander Bay, Spain, specimens Num. 686 from the Rioja Collection, 1894–1917 (in part), coated with gold, 2 specimens ( MNCN 16.01/15348); El Puntal, 43° 27’ N, 3° 25’ W, Santander Bay, Spain, April 2011, 2 specimens ( MNCN 16.01/15349, MNCN 16.01/15350); El Puntal, 43° 27’ N, 3° 25’ W, Santander Bay, Spain, April 2011, 1 specimen (AM W46620); Noiremoutier, near St. Nazaire, France, eastern Atlantic, coll. M. Bioner, det. as O. eremita by P. Fauvel, 2 specimens ( BMNH ZK 1928.4.26.290–291); Off shore between Vidio Cape and Peñas Cape, Cantabrian Sea, Spain, 15–32 m, 1998, 4 specimens ( MNCN 16.01/3967 – MNCN 16.01/3970).

Diagnosis. Based on specimens wider than 2.0 mm at chaetiger 10 excluding parapodia. Prostomium anteriorly extended. Eyespots absent. Palps reaching chaetiger 1–2, lateral antennae reaching chaetiger 5–6 and median antenna chaetiger 2–4. Ceratophores long and strongly ringed, palpal ceratophores with 22–26 rings, lateral antennae with 21–29 and median antenna with 15–20 rings. Subulate ventral cirri in first five to six chaetigers; distinct subulate postchaetal lobes in first 10–19 chaetigers. Small interramal papilla present between chaetigers 4–5 to 9. Bi- and tridentate (or even multidentate) pseudocompound hooks in first three chaetigers. Subacicular hooks from chaetiger 10. Flat, distally oblique pectinate chaetae with 13–17 teeth. Single branchial filaments from chaetiger 1 to 19–24, thereafter number increasing to maximum of six to eight. Tube with soft inner layer and outer layer of vegetal material, shell-fragments and sand grains.

Description. Moderate to relatively large species; almost complete preserved specimens 112–148 mm long, 2.4–3.9 mm width (10th chaetiger without parapodia) with about 180 chaetigers. Live specimens with iridescent violet colour on antennae and dorsum of anterior end. Two most common colour morphs, one darker than other but both with variations. Common colour pattern with wide brown transverse bands, occupying almost entire surface of each segment and giving dark or melanic appearance to worm ( Fig. 9 A, B, D); other colour pattern consisting of two brown lateral transverse stripes on dorsal anterior end on light background, anterior stripe thinner than posterior one ( Fig. 9 E). Body cream-coloured in alcohol stored animals or greenish in formalin preserved condition with wide dorsal pigment bands on anterior chaetigers, some specimens only clearly coloured at anterior margin of segments forming a transversal banding pattern ( Fig. 9 C). Prostomium conical with pair of subulate frontal lips. Eyespots absent. Palps reaching chaetiger 1–2 with 21–25 rings and longer distal one. Lateral antennae reaching chaetiger 5–6 with 20–28 basal rings, median antenna reaching chaetiger 2–4 with 14–19 basal rings, all three antennae with slightly longer distal ring ( Fig. 10 A, D). Ceratophores and gradually tapered styles with scattered sensory buds forming staggered rows—quincunxes—( Fig. 10 D); sensory buds flat, pores of serous glands forming irregular circles ( Fig. 10 E). Peristomial cirri inserted distally on peristomium slightly lateral to lateral antennae, shorter than length of peristomium not exceeding anterior margin of prostomium ( Figs 10 A, 11A).

Anterior chaetigers (1–3) slighty longer than those following ( Figs 10 A, B, 11A). First three 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; digitate dorsal cirrus longer than postchaetal lobe and ventral cirrus shorter than postchaetal lobe ( Figs 10 F, 11B). Subulate ventral cirri in first five to six chaetigers, followed by transitory forms on chaetigers 7 and 8 and pad-like thereafter ( Fig. 10 C). Postchaetal lobe as distinct subulate lobe in first 10–19 chaetigers, becoming smaller and conical knobs in shape thereafter. Small interramal papilla present between chaetigers 4–5 to 9 ( Figs 10 G, 11C). Parapodia of anterior chaetigers with high density of sensory buds ( Figs 10 G, 12G).

Branchiae as single filament from first chaetiger to chaetiger 19–24 ( Figs 10 F, 11B, C), usually longer than dorsal cirri, thereafter number of filaments increasing rapidly to maximum of six to eight ( Fig. 11 D), being present to end of fragment (about chaetiger 180 of almost complete specimens).

Aciculae yellowish with pointed tips, generally three per parapodium. Hooded pseudocompound hooks in first three chaetigers ( Figs 11 E–H, 12A–E). First three parapodia with following chaetal complement going from superior to inferior part of chaetal fan: one to two simple chaetae, two pectinate chaetae flat and slightly oblique with 13–17 teeth ( Fig. 12 F), three protruding distal tips of aciculae and five pseudocompound hooks: one to three tridentate pseudocompound hooks varying from strongly tridentate ( Figs 11 H, 12B, C) to hooks with most proximal denticle much smaller than other two ( Fig. 11 G), one to three bidentate pseudocompound hooks or one bidentate ( Figs 11 E, 12A) and sometimes two quatridentate hooks with two little denticles protuding directly from base of second distal tooth or with an additional fourth proximal tooth ( Fig. 12 D, E); all hooks of almost equal thickness and length of appendage. Pseudocompound hooks replaced by limbate chaetae from chaetiger 4. Hooded bidentate subacicular hooks from chaetiger 10 ( Fig. 12 G). Mandibles ( Fig. 11 J) with white calcified cutting plates and slender shafts. Maxillae ( Fig. 11 I) weakly sclerotised; maxillary formula (based on a specimen from Santander): Mx I = 1 + 1, Mx II = 7 + 7, Mx III = 8 + 0, Mx IV = 5 + 12, Mx V = 1 +1, Mx VI absent. Tube cylindrical in shape, parchment-like and externally covered with vegetal material, shell fragments and sand grains.

Variation. Although the pseudocompound hooks are basically bi- and tridentate, some specimens have additional tiny teeth associated with the second distal and proximal tooth and/or an additional fourth proximal tooth. The neotype, two specimens from Naples, four specimens from Santander and three specimens from the Cantabrian shelf presented pseudocompound hooks on anterior chaetigers with four and even five teeth, generally two hooks per parapodium ( Figs 11 F; 12E). The remaining examined specimens lacked quatridentate pseudocompound hooks (18 specimens), although the majority of these specimens had some broken hooks and the earlier presence of quatridentate hooks cannot be ruled out, others were complete and well preserved and lacked quatridentate hooks. Thus, the presence of hooks with four or more teeth on anterior chaetigers is variable and may be the result of abnormal growth.

Ontogenetic variation. Specimens smaller than 2.0 mm in width at the 10th chaetiger differed from larger specimens in having fewer pseudocompound hooks and more simple chaetae in the first three pairs of parapodia instead of the adult state of five hooks and one or two simple chaetae. This represents a juvenile phase in the attainment of the adult chaetal complement, as anterior hooks can be preceded by different chaetae in onuphids ( Paxton 1996; Budaeva & Paxton 2013). These small specimens also had a pair of eyespots on the prostomium which was sometimes only visible with confocal microscopy. Juvenile eyespots have been observed in species of different onuphid genera and are generally lost with increasing growth of the animal ( Paxton 1986). In view of these observed juvenile characteristics we have restricted the diagnosis of O. pancerii to specimens with a width of more than 2.0 mm at chaetiger 10.

Remarks. In the original description, there is some confusion with the number of anterior chaetigers with pseudocompound hooks. Claparède stated “ à partir du quatrième segment (3rd chaetiger) les soies composées (pseudocompound hooks) disparaissent et sont remplacées par de simples soies subulées”. The expression “ à partir de ” has been slightly confusing for the Latin languages and is today still subject to different interpretations as “from”, “after” or “followed by”. Although today the common translation is the first interpretation, we presume that Claparède wanted to use the expression “ à partir de ” in the sense of “after” not “from”, since at that time it was commonly used as synonym of “après” (= after). Furthermore, Rioja (1918) who was contemporary also interpreted Claparède’s expression as “after” establishing that the species has pseudocompound hooks in the first three chaetigers.

The two specimens from Noiremoutier, France (BMNH ZK 1928.4.26.290-291) identified by P. Fauvel as O. eremita and figured by Paxton (1986: fig. 3, 6–8, 10) as such have been re-examined and found to be O. pancerii .

Neotype. The neotype is an almost complete specimen with about 180 chaetigers, length of 121 mm and width at chaetiger 10 (excluding parapodia) of about 2 mm, although the freshly preserved specimen would have had a greater width ( Fig. 9 A, B). The specimen had become dehydrated, due to the loss of liquid from its container, but was rehydrated successfully following the method proposed by Moreno (2004). Despite not being in perfect condition, it displays the diagnostic features and is a good representative of the species as obvious from the brief description below: colour pattern consisting of wide transverse bands that occupy almost the entire surface of each anterior chaetiger; maximal number of 24–25 rings on antennae; subulate ventral cirri in first six chaetigers; interramal papillae present from chaetiger 4 to 9; branchiae from first chaetiger as single filament, with clearly two filaments from chaetiger 24 and reaching thereafter a maximum of six filaments; bi-, tri- and quatridentate pseudocompound hooks in first three chaetigers ( Fig. 11 E–H); pectinate chaeta with about 13 teeth, present from first chaetiger and hooded subacicular hooks from chaetiger 10.

Justification for the neotype. Onuphis pancerii was originally described by Claparède (1868) from the Gulf of Naples. He carried out the work during a five to six month stay in Naples during the winter of 1866–1867. As is well known, Claparède did not deposit specimens as he was convinced that polychaetes should be studied on live material only (M.C. Gambi, pers. com. to A.A.).

Among the Onuphis specimens from the Rioja Collection, now deposited at the Museo Nacional de Ciencias de Natural of Madrid ( Spain), we found a very interesting specimen labelled as “ Onuphis pancerii Clpd. Nápoles ”. This specimen was used by Rioja as comparative material for his work on the Santander Onuphis specimens where he referred several times to “a specimen from the Zoological Station at Naples” ( Rioja 1918). The specimen came into Rioja’s possession at an unknown date sometime between the late 19th century and the early 20th century (prior to 1917), but we do not know how he obtained it or whether it was part of Claparède’s original material. We consider the specimen an excellent candidate to establish new type material for O. pancerii and thus designate it as the neotype. By defining the neotype of O. pancerii the reinstatement of this species is herein formally established.

Reproductive biology. Two Cantabrian specimens collected in April 2011 carried eggs inside the coelomic cavity that protruded through openings of the body wall. Extracoelomic eggs ranged from 190 to 234 Μm in diameter (X = 209.7; SD = 16.48; N = 30). No brooded eggs or embryos were found inside the dissected tubes or attached to them.

Distribution, habitat and faunal associates. As the species has been considered a synonym of O. eremita for a long time we cannot assess its actual distribution based on literature records. Besides the type locality, Naples (central Mediterranean), O. pancerii is known from Santander, the central Cantabrian shelf (southern Bay of Biscay) and Noiremoutier (Atlantic coast of France) ( Fig. 7 ). However, it is possible that the species may be widespread throughout central and western Mediterranean basins as well as along the Atlantic coasts of the Iberian Peninsula, occurring sympatrically with O. eremita as is occurring in the central Cantabrian shelf between 15 to 32 m depth.

In the Mediterranean the species is considered typical of shallow subtidal sandy bottoms while at Santander Bay, O. pancerii inhabits an intertidal to shallow subtidal Tellina tenuis da Costa community along with the onuphid D. neapolitana ; both species are greatly appreciated as fishing-bait, constituting an important natural resource from the area. Local fishermen harvest the onuphids at low tide, commonly using the salt method, in a similar way as they do with the razor-shells Solen marginatus Pulteney and Ensis spp. Schumacher (A.A., pers. obs.).

Figures

FIGURE 7. Onuphis eremita. Scanning electron micrographs. A, detailed view of the ectosymbiont peritrich Epistylis sp. on anterior parapodia; B, intracoelomic developing oocytes; C, detailed view of immature oocyte with nurse cells attached; D – E, spermatozoa protruding from openings of the body wall; F, detailed view of spermatozoon, lateral view; G, detailed view of spermatozoon, frontal view. H – I, detailed view of spermatozoon, posterior view; a, acrosome; c, corona of cilia; f, flagellum; m, mitochondria; n, nucleus; nc, nurse cells; o, oocyte; p, peduncle; r, ring.

FIGURE 8. Distribution map of confirmed occurrences of Onuphis eremita and Onuphis pancerii. Squares, O. eremita localities; circles, O. pancerii localities.

FIGURE 9. Onuphis pancerii. Neotype A, B (MNCN 16.01 / 311), specimen from Santander Bay C (AM W 46620), specimen from McIntosh collection D (BMNH 1921.5.1.832 - 34), specimens from Naples E (BMNH 1923.11.19.25 - 8). Photomicrographs. A, C, D detailed view of anterior end, dorsal view; B, E anterior part of whole specimens showing colour pattern, dorsal view.

FIGURE 10. Onuphis pancerii. Specimens from Santander Bay (MNCN 16.01 / 15348, MNCN 16.01 / 15350). Scanning electron micrographs. A, anterior end, dorsal view; B, anterior end, ventral view; C, anterior end, lateral view; D, detailed view of antennal ceratophores; E, detailed view of scattered sensory buds of antenna; F, parapodium chaetiger 2, lateral view; G, detailed view of chaetigers 5 to 7, lateral view, arrows point to interramal papillae; b, branchia; ch, chaetiger; dc, dorsal cirrus; gp, glandular pad; p, interramal papilla; pol, postchaetal lobe; prl, prechaetal lobe; vc, ventral cirrus.

FIGURE 11. Onuphis pancerii. A – D modified from Paxton (1986) - as O. eremita-, Neotype E – F (MNCN 16.01 / 311), Santander specimen I, J (MNCN 16.01 / 310). Line drawings. A, anterior end, dorsal view; B, parapodium chaetiger 1, anterior view; C, parapodium chaetiger 8, anterior view; D, parapodium chaetiger 53, anterior view; E, bidentate pseudocompound hook, chaetiger 2; F, quatridentate pseudocompound hook, chaetiger 3; G, tridentate pseudocompound hook, chaetiger 3; H, strongly tridentate pseudocompound hook, chaetiger 2; I, maxillae; J, mandibles.

FIGURE 12. Onuphis pancerii. Specimens from Santander Bay (MNCN 16.01 / 15348, MNCN 16.01 / 15350). Scanning electron micrographs. A, bidentate pseudocompound hook, chaetiger 1; B, tridentate pseudocompound hook, chaetiger 1; C, tridentate pseudocompound hook, chaetiger 3; D, multidentate pseudocompound hook, chaetiger 3; E, multidentate pseudocompound hook, chaetiger 2; F, pectinate chaetae, chaetiger 10; G, subacicular hooks, chaetiger 10; sb, sensory bud.