Paucibranchia bellii ( Audouin & Milne-Edwards, 1833 ) Molina-Acevedo, 2018

Molina-Acevedo, Isabel C., 2018, Morphological revision of the Subgroup 1 Fauchald, 1970 of Marphysa de Quatrefages, 1865 (Eunicidae: Polychaeta), Zootaxa 4480 (1), pp. 1-125 : 20-26

Paucibranchia bellii ( Audouin & Milne-Edwards, 1833) n. comb.

Figures 11–14 , Tables 1, 3

Eunice belliii Audouin & Milne-Edwards in Cuvier 1830:200 nomen nudum

Eunice bellii Audouin & Milne-Edwards, 1833:223 –224, Pl. XI, Figs. 1–4 , 8 , 9 text-fig. XXVII; Cuvier 1836 –1849:32; Grube 1850:44 –45.

Marphysa belli de Quatrefages 1866:333 –334; McIntosh 1910: 448 –451; Lu & Fauchald 1998:829 –834, Figs. 1a–j , 2–6 , Tab. 1 (partim)

Eunice (Marphysa) bellii Grube 1878:59 .

Marphysa bellii von Marenzeller 1874:59 –60; de Saint-Joseph 1888:204 –205; Fauvel 1923:410, Fig. 161i–q.

Material examined. Type material: Lectotype MNHN TYPE 568, paralectotype MNHN TYPE 567 , Chausey Island , France, English Channel, Atlantic. Additional material: MNHN-A39 (1), (R.) 1868 N° 155 d (1), St. Vaast , Normandy , France, Atlantic Ocean, 1868. MNHN-A39 (1), (R.) N° 155 f (1), St. Vaast , Normandy , France, Atlantic Ocean, 1868. MNHN-A39 (2), Pier of Croisic , France, Atlantic Ocean, Jun 1908, L. du Réau, Collection of Fauvel. MNHN-A39 (2), Tatihou Island , Normandy , France, Atlantic Ocean, 1895, Collection of Fauvel. MNHN-A39 , AZ778 30–16 (2), Cosqueville , Normandy , France, Atlantic Ocean, 19 Apr 1909. MNCN 16.01 /2445 (1), sta. F–32, Between Cabo de San Antonio and Port of Valencia , Spain, Mediterranean Sea, coll. G. San Martin. MNCN 16.01 /2446 (1), sta. F–152, Between Cabo de San Antonio and Port of Valencia , Spain, Mediterranean Sea, coll. G. San Martin. ECOSUR –P2173, Carnac, Morbihan , France, 21 Apr 1967, coll. F. Rullier. ZMB 3996 (3), Roscoff, Finisterre , France, Atlantic Ocean, coll. Grube.

Description. Lectotype MNHN TYPE 568 incomplete, with 102 chaetigers, L10= 4 mm, W10= 0.9 mm, the fragment with TL= 30 mm. Anterior region of body with convex dorsum and flat ventrum, without groove; body depressed from chaetiger 5, widest at chaetiger 35, tapering after chaetiger 70.

Prostomium entire, 1 mm long, 0.7 mm wide, frontally rounded, without median sulcus ( Fig. 11A, C ), ventral sulcus deep ( Fig. 11B ). Prostomial appendages in a semicircle, median antenna isolated by a gap. Palps reaching second peristomial ring; lateral antennae reaching first chaetiger; median antenna reaching the middle of second chaetiger. Palpophores and ceratophores ring-shaped, short, slender; palpostyles and ceratostyles tapering, thick, without articulation. Eyes not observed (see Remarks section).

Peristomium wider than prostomium (0.7 mm long, 1.3 mm wide), first ring two times longer than second ring, separation between rings distinct on all sides ( Fig. 11A–B ). Inferior lip with a slight central depression ( Fig. 11B ).

Maxillary apparatus with MF= 1+1, 7+7, 7+0, 7+10, 1+1 ( Fig. 12A–B ). Maxillary carriers 1.8 times shorter than length of MI. MI forceps-like; closing system 7 times shorter than length of MI; ligament between MI and MII not sclerotized ( Fig. 12A–D ). MII wide; teeth recurved, sharped; cavity opening oval, 4 times shorter than length of MII; ligament between MII and MIII, and right MIV, not sclerotized ( Fig. 12A–D ). MIII short; with triangular teeth; with attachment lamella slightly sclerotized ( Fig. 12A–D ). Left MIV with a small basal tooth; attachment lamella semicircular, wide, situated 1/2 along length of posterior edge of maxilla. Right MIV with small teeth; attachment lamella wide, semicircular, better developed in the middle, situated 1/2 along length of posterior edge of maxilla ( Fig. 12A–D ). MV square, with a short, rounded tooth ( Fig. 12A–D ). Mandibles in poor condition; examined in MNHN-A39 (Croisic), dark, cutting plates whitish, with 10 growth rings.

Branchiae pectinate with up to 13 filaments, in chaetigers 12–30 ( Figs. 11C ; 13B ). Number of branchial filaments per chaetiger in order anterior-posterior: 8, 9, 10, 11, 11, 13, 13, 12, 12, 12, 11, 10, 10, 12, 11, 10, 9, 7, 5. Branchial filaments longer than dorsal cirri.

First two parapodia smallest; most developed in chaetigers 4–29, following ones becoming gradually smaller. Notopodial cirri conical, increasing in size from chaetiger 5 (Ldc3: 0.28 mm; Ldc12: 0.36 mm), from chaetiger 35, gradually decreasing in size, in posterior region 1.2 times longer than pre-branchial region ones (Ldc93: 0.33 mm) ( Fig. 13A–E ). Prechaetal lobes as a transverse fold in all chaetigers ( Fig. 13A–E ). Chaetal lobes in chaetigers 1–29, rounded, shorter than postchaetal lobes, with aciculae emerging dorsal to midline; from chaetiger 30, triangular, with acicula emerging in midline, longer than other lobes ( Fig. 13A–E ). Postchaetal lobes well developed in chaetigers 1–57; tongue-shaped in pre-branchial chaetigers; from branchial chaetigers conical, thinner; decreasing in size in chaetigers 33–57, following ones inconspicuous ( Fig. 13A–E ). Ventral cirri digitiform in chaetigers 1–4; in chaetigers 5–42 with oval swollen base and digitiform tip; from chaetiger 43, digitiform, gradually reducing in size posteriorly ( Fig. 13A–E ).

Aciculae blunt, dark in anterior chaetigers, in median-posterior region the intensity of color reduces to look amber ( Fig. 13A–E ). First 16 chaetigers with 2 or 3 aciculae; in chaetigers 17–26 with 2 aciculae; from chaetiger 27, with only one acicula.

Limbate chaetae of two sizes in same chaetiger, larger in anterior region, reduced in number around chaetiger 13. Two types of pectinate chaetae; in anterior chaetigers isodonts narrow with long and slender teeth, with 1–2 pectinate, with up to 4–5 teeth, with oblique distal edge ( Fig. 14E ); in median-posterior chaetigers isodonts narrow with short and slender teeth, with 4–5 pectinate, with up to 10–13 teeth, with transverse distal edge ( Fig. 14F ). Compound spinigers present only in first 40 chaetigers, six or seven per chaetiger, blades of similar size ( Fig. 14D ). Compound falcigers present in all chaetigers, more abundant than spinigers; in anterior region with blades of two sizes (longer 57 µm, Fig. 14A ; smaller 48 µm, Fig. 14B ), smaller more abundant; all with triangular teeth, of similar size, distal tooth directed upward, proximal tooth directed laterally; in median-posterior chaetigers with all blades of similar size, slightly shorter than blades of anterior chaetigers (43.4 µm, Fig. 14C ), with triangular teeth, distal tooth shorter than proximal, distal tooth directed upward, proximal tooth directed laterally. Subacicular hooks bidentate, amber, starting from chaetiger 27, with one or two hooks per chaetiger; with triangular teeth, distal tooth smaller than proximal tooth, directed upward; proximal tooth directed laterally ( Fig. 14G ).

In non-type specimen (ECOSUR–P2173), pygidium with two pairs of anal cirri; dorsal pair as long as last four chaetigers; ventral pair short, as long as last chaetiger ( Fig. 11D ).

Variation. Material examined varied in the following features: L10= 3.7–9 mm, W10= 0.6–2.3 mm. Palps reaching first peristomial ring or second peristomial ring. Lateral antennae reaching second peristomial ring or first chaetiger. Median antenna reaching second peristomial ring or middle of second chaetiger. The maxillary formula varies as follows: MII 6–8+7–9, MIII 6–8, MIV 5–7+9–10. The proportion of maxillary apparatus varies as follows: maxillary carriers shorter with respect to the MI varies 1.6–2.2 times; closing system shorter with respect to the MI varies 6–7 times; cavity opening shorter with respect to MII varies 3.2–4 times. Branchiae from chaetigers 10–15 to chaetigers 22–43. Maximum number of branchial filaments varied from 9 to 22. Well developed postchaetal lobe in first 32–72 chaetigers. Ventral cirri with swollen base from chaetigers 4–5 to chaetigers 37–78. Start of subacicular hooks in chaetigers 24–38. Compound spinigers present only in first 23–53 chaetigers.

Distribution. English Channel, western Mediterranean.

Remarks. The type material of P. bellii n. comb. consists of two syntypes, one of them (MNHN TYPE 568) is designated as the lectotype because it is in better condition. The other (MNHN TYPE 567) is regarded as paralectotype, which is dry and in poor condition.

Audouin & Milne-Edwards (1833) described the type species of the group based on the branchiae being restricted to the anterior end. The species name, Eunice bellii , was dedicated to the zoologist M. T. Bell and they probably transformed the noun Bell to the genitive noun Belli, and added to the name another "i" to indicate that it was dedicated to a man ( ICZN, 1999, Art. 31.1.1, 31.1.2). However, some authors wrote the species name as belli without any comment about this change (e.g., de Quatrefages 1866; McIntosh 1910; Treadwell 1921; Lu & Fauchald 1998), introducing incorrect subsequent spellings ( ICZN 1999, Art. 33.3). According to Art. 33.4 ( ICZN 1999), the original spelling is the correct form of writing the name of the species.

There was controversy regarding the absence of eyes in P. bellii n. comb.. Treadwell indicated that Audouin & Milne-Edwards (1833) did not describe eyes as present in this species, and he did not find evidence for eyes in the species in the literature. As a result, Treadwell assumed that the species was blind and described the subspecies M. bellii oculata Treadwell, 1921 (now P. oculata n. comb.) based on specimens from Florida which had eyes. However, before Treadwell’s description, Fauvel (1923) examined some specimens from the Atlantic coast of France and the Mediterranean Sea and showed the presence of eyes in P. bellii n. comb.. Lu & Fauchald (1998) studied material of P. bellii n. comb. from the MNHN collection, and they found that the oldest specimens lacked eyes; however, they argued that this absence was due to preservation. Although the lectotype and paralectotype of P. bellii n. comb. do not have eyes, I agree with Lu & Fauchald (1998) that the loss of the eyes pigmentation is likely related to preservation.

Paucibranchia bellii n. comb. is considered a species with a wide distribution, since it has been reported from the Mediterranean Sea (von Marenzeller 1874; Fauvel 1923; among others), Northwestern Atlantic coast ( Pettibone 1963; Lu & Fauchald 1998), Grand Caribbean ( Ehlers 1887; Gathof 1984; Lu & Fauchald 1998), Persian Gulf ( Wesenberg-Lund 1949), and Vietnam ( Gallardo 1968). However, some of these reports correspond to different species.

Specimens from the Northwestern Atlantic coast (Massachusetts) and Gulf of Mexico were reviewed and compared with P. bellii n. comb.. The specimens of both areas belong to two different species ( P. andresi n. sp. from Massachusetts and Paucibranchia sp. 1 from Gulf of Mexico) (see Remarks section for each species). Therefore, P. bellii n. comb. is not distributed in this region. The specimens of P. bellii n. comb. reported by Gallardo (1968) from Vietnam were studied and found to be a new species, P. carrerai n. sp. (see Remarks section of this species).

Regarding the presence of P. bellii n. comb. in the Persian Gulf ( Wesenberg-Lund 1949), the characterization of the only specimen described differing from P. bellii n. comb. by the branchial distribution; however, it is necessary to review this material to confirm if it belongs to an undescribed species. A similar question arises with some specimens reported in the middle and eastern region of the Mediterranean Sea ( Çinar 2005), which could belong to another species due to geographic distance and ecological conditions. Recently, it has been demonstrated that the fauna of the eastern Mediterranean may be different from that of the western Mediterranean ( Iannotta et al. 2009). For example, Iannotta et al. (2009) demonstrated (based on molecular and morphological data) that the eunicid Lysidice ninetta Audouin & Milne-Edwards, 1833, widely recorded in the Mediterranean Sea, constitute two sibling species distributed one on each side of the Mediterranean. It would require sampling of specimens from the eastern region of the Mediterranean to test this hypothesis for P. bellii n. comb.

Paucibranchia bellii n. comb. resembles P. andresi n. sp., P. carrerai n. sp., P. fallax n. comb., P. oculata n. comb., P. sinensis n. comb., P. stragula n. comb. and P. totospinata n. comb. by having compound spinigers and falcigers, and bidentate subacicular hooks. However, P. bellii n. comb. differs from P. totospinata n. comb. by the color of the subacicular hooks and distribution of the compound spinigers, since the former has amber hooks and spinigers is only present in the anterior region; whereas, the latter species has hooks with a reddish basal end and distally is amber, and the spinigers is present in all chaetigers. Also, P. fallax n. comb. has branchiae from chaetigers 15 to 48, with only two filaments (MNHN-A39, L10: 3.3 mm); whereas in P. bellii n. comb. branchiae are in chaetigers 12 to 30, with up to 13 filaments (MNCN 16.01/2445, L10: 4 mm). On the other hand, P. oculata n. comb. differs in the distribution and abundance of compound chaetae (spinigers and falcigers). This species has spinigers in anterior chaetigers (1–35) and falcigers from chaetiger 26 (holotype); also, spinigers are always more abundant than falcigers; whereas in P. bellii n. comb. spinigers and falcigers start from the first chaetiger, and falcigers are always more abundant than spinigers. P. stragula n. comb. differs by the presence of several subacicular hooks in each chaetiger, with up to 5–6 hooks per chaetiger, whereas in P. bellii n. comb. there are only one or two hooks per chaetiger. The morphological differentiation of P. bellii n. comb. from P. andresi n. sp., P. carrerai n. sp., and P. sinensis n. comb. is provided in the Remarks section of each species. The comparison with other Paucibranchia n. gen. species having compound falcigers and spinigers present is provided in Table 3.

Figures

FIGURE 1. Maxillary apparatus. A. Paucibranchia disjuncta n. comb. (Hartman, 1961), LACM-AHF POLY 6447, dorsal view; B. Marphysa viridis Treadwell, 1917, ECOSUR-P2678, dorsal view; C. Treadwellphysa yucatanensis Molina-Acevedo & Carrera-Parra, 2017, ECOSUR-P2811, dorsal view; D. Left MI-II-III-IV-V of P. disjuncta n. comb., dorsal view; E. Left MI- II-III-IV-V of M. viridis, dorsal view; F. Left MI-II-III-IV-V of T. yucatanensis, dorsal view. Scale bars: A, D, 0.4 mm; B, E, 0.45 mm; C, F, 0.25 mm. Dark and thin lines in D, E and F indicate the different forms in the MI of the apparatus of each species. fa= falcal arch, boe= basal outer edge, bie= basal inner edge, rp= rounded projection in base of MII.

FIGURE 2. Marphysa bonhardi McIntosh, 1885, holotype BMNH 1885.12.1.210. A. Anterior end, dorsal view; B. Anterior end, ventral view; C. Aciculae, anterior chaetigers. Scale bars: A, 0.8 mm; B, C, 0.67 mm.

FIGURE 3. Paucibranchia adenensis (Gravier, 1900) n. comb. A. Anterior end with branchiae, dorsal view; B. Anterior end, dorsal view; C. Anterior end, ventral view; D. Anterior end, dorsal view; E. Anterior end with branchiae, dorsal view; F. Anterior end, ventral view. A, B, C from holotype MNHN-531; D, E, F from non-type MNHN-A148. Scale bars: A, 2 mm; B, 1 mm, C, 2.6 mm, D, F, 0.7 mm; E, 1.3 mm.

FIGURE 4. Paucibranchia adenensis (Gravier, 1900) n. comb., non-type MNHN-A148. A. Maxillary apparatus, dorsal view; B. Mandibles; C. Left MII-III-IV-V, dorsal view; D. Maxilla I, dorsal view. Apparatus stained with methyl green. Scale bars: A, C, 50 µm; B, 150 µm; D, 130 µm. al-MIV= attachment lamellae in MIV, LMI-MII= ligament between MI and MII.

FIGURE 5. Paucibranchia adenensis (Gravier, 1900) n. comb., non-type MNHN-A148. A. Parapodium 3; B. Parapodium 11; C. Parapodium 26; D. Parapodium 70; E. Parapodium 158; F. Parapodium 216. All in anterior view. Scale bars: A–F, 0.7 mm.

FIGURE 6. Paucibranchia adenensis (Gravier, 1900) n. comb., non-type MNHN-A148. A. Compound falciger, long blade, chaetiger, 11; B. Compound falciger, median blade, chaetiger, 11; C. Compound falciger, short blade, chaetiger, 216; D. Isodonts pectinate narrow with long and slender teeth, chaetiger 3; E. Isodonts pectinate narrow with short and slender teeth, chaetiger 216; F. Subacicular hook, distal end, chaetiger 158. Scale bars: A, 12.5 µm; B, 20 µm; C, F, 9.8 µm; D, 14 µm, E, 4.9 µm.

FIGURE 8. Paucibranchia andresi n. sp., holotype USNM 28955. A. Maxillary apparatus, dorsal view; B. Left MI-II-III-IV; C. Mandibles. Apparatus stained with schirlastain. Scale bars: A, 0.075 mm; B, 0.13 mm; C, 0.25 mm. al-MIV= attachment lamella in MIV.

FIGURE 9. Paucibranchia andresi n. sp., holotype USNM 28955. A. Parapodium 3; B. Parapodium 8; C. Parapodium 14; D. Parapodium 55; E. Parapodium 213. All in anterior view. Scale bars: A, 0.17 mm; B, D, E, 0.2 mm; C, 0.4 mm.

FIGURE 11. Paucibranchia bellii (Audouin & Milne-Edwards, 1833) n. comb. A. Anterior end, dorsal view; B. Anterior end, ventral view; C. Anterior end with branchiae, dorsal view; D. Pygidium, ventral view. A–C from lectotype MNHN TYPE 568; D from non-type ECOSUR–P2173. Scale bars: A, B, D, 1 mm; C, 2 mm.

FIGURE 12. Paucibranchia bellii (Audouin & Milne-Edwards, 1833) n. comb. A. Maxillary apparatus, dorsal view; B. Maxillary apparatus, dorsal view; C. Left MI-II-III-IV-V; D. Right MI-II-IV-V. A from lectotype MNHN TYPE 568, B, C, D, from non-type ECOSUR–P2173. Scale bars: A, 0.2 mm; B, 0.7 mm, C, D, 0.3 mm.

FIGURE 13. Paucibranchia bellii (Audouin & Milne-Edwards, 1833) n. comb. A. Parapodium 3; B. Parapodium 29; C. Parapodium 46; D. Parapodium 93; E. Parapodium 138. All in anterior view. A, E from non-type MNHN-A39; B–D from lectotype MNHN TYPE 568. Scale bars: A, 140 µm; B, 180 µm; C, 160 µm; D, 111 µm; E, 230 µm.

FIGURE 14. Paucibranchia bellii (Audouin & Milne-Edwards 1833) n. comb. A. Compound falciger, long blade, chaetiger 3; B. Compound falciger, median blade, chaetiger 3; C. Compound falciger, short blade, chaetiger 138; D. Compound spiniger, chaetiger 3; E. Isodonts pectinate narrow with long and slender teeth, chaetiger 9; F. Isodonts pectinate narrow with short and slender teeth, chaetiger 200; G. Subacicular hook, distal end, chaetiger 93. A from lectotype MNHN TYPE 568; B, C, D from non-type MNHN-A39; E, F, G, from ECOSUR–P2173. Scale bars: A, 14.5 µm; B, 24 µm; C, 21.64 µm; D, E, 7 µm; F, 9.8 µm; G, 6 µm.