Marphysa hongkongensa, Wang & Zhang & Qiu, 2018

Wang, Zhi, Zhang, Yanjie & Qiu, Jian-Wen, 2018, A New Species in the Marphysa sanguinea Complex (Annelida, Eunicidae) from Hong Kong, Zoological Studies 57 (48), pp. 1-13 : 5-10

Marphysa hongkongensa n. sp.

( Figs. 1-4 , Tables 1-2)

urn:lsid:zoobank.org:act:B0F18CCD-A482-4873-9525-1E6889F153EF

Materials examined: 24 type specimens collected from the intertidal zone of six beaches in Tolo Harbour, Hong Kong during 2015-2018 ( Table 1). Holotype: SWIMS-ANN-18-012. Paratypes: SWIMS-ANN-18-013-SWIMS-ANN-18-023; AM W.50930-AM W.50941.

Description: Live worms light green with iridescence; middle part with red branchial filaments on dorsal side ( Fig. 1A ). Preserved specimens beige. Complete specimens 23-147 mm long, 129-288 chaetigers; anterior prostomial margin to chaetiger 10 3.3-7.0 mm; chaetiger 10 (without parapodia) 2.2-5.3 mm wide ( Table 1).

Prostomium with two dorsoventrally flattened buccal lips and an anterior notch between them ( Fig. 1 B-D). Two palps and three antennae slender, attached on short palpiphore, arranged in a more or less curved line on the posterior margin of the prostomium. All five prostomial appendages approximately the same length, 1.5 times as long as prostomium ( Fig. 1 B-D). Peristomium approximately 3 times as long as segment 2, with notched anterior margin on ventral side ( Fig. 1C ).

Mandibles slightly longer than Mx I plus carriers ( Fig. 1 I-J). Mx I approximately 2.4 times as long as carriers. Mx II edge serrated, with teeth on left and right sides well matched. Mx III single, arched, slightly smaller than right Mx IV. Mx IV paired, both attached with basal lamellae; left Mx IV smaller than the right one. Mx V paired, flat, left one slightly smaller than right one ( Fig. 1 I-J). Maxillary formula: I = 1 + 1, II = 5-6 + 5-6, III = 7 + 0, IV = 4 + 8, V = 1 + 1.

Parapodia commencing from segment 3 ( Fig. 1 B-D). First parapodia located below the middle line of body wall, but gradually positioned dorsally in following segments ( Fig. 1 D-F). Notopodial cirri tapering, approximately as along as neuropodial cirri, longer than acicular lobes in anterior chaetigers, and similar in length with acicular lobes in posterior chaetigers ( Fig. 2 ). Neuropodial cirri conical, similar in size with notopodial cirri in first few chaetigers, but inflated in middle and posterior chaetigers ( Fig. 2 ).

Branchiae pectinate, commencing from anterior (15th-35th chaetiger) to near end. Branchiae single filament in anterior parapodia, pectinate with up to 5-10 filaments in middle parapodia ( Fig. 2B ), reducing to 1 in last several chaetigers.

Aciculae black with paler tip, approximately three per parapodia in anterior chaetigers, two per parapodia in middle chaetigers, and one per parapodia in posterior chaetigers. Supraacicular chaetae with limbate capillaries and pectinates. Capillaries present from first chaetiger to near pygidium, numbering up to 20 in anterior chaetigers. Pectinate chaetae commencing from first few chaetigers to near end, four types: a) isodont with 8-15 fine and short teeth, lateral teeth longer and usually straight, plate symmetrical or slightly asymmetrical, distributed in anterior chaetigers, 1-3 per parapodia ( Fig. 3G, J ); b) isodont with 15-23 fine and short teeth, lateral teeth longer and usually incurved, plate asymmetrical, distributed from middle to posterior chaetigers, 1-7 per parapodia ( Fig. 3I, K , O-P); c) anodont with approximately 15 median teeth, teeth length approximately ¼-⅓ plate width, plate asymmetrical, distributed in posterior chaetigers, 1-3 per parapodia ( Fig. 3L, P ); d) anodont with 7-13 large teeth, three medial teeth larger or similar in size with adjacent teeth, teeth length approximately ½ of plate width, plate asymmetrical, distributed in posterior chaetigers, 1-2 per parapodia ( Fig. 3 M-P). Pectinates arranged in rows in posterior chaetigers, with asymmetrical short and fine-toothed isodonts (type b) in anterior two rows, median- and large-toothed anodonts in posterior row (types c and d); Median-toothed anodonts (type c) in near middle chaetigers (anterior part of posterior chaetigers), approximately three in posterior row and gradually replaced by 1-2 large-toothed anodonts (type d) in posterior chaetigers ( Fig. 3L , O-P).

Subacicular chaetae compound spinigers and subacicular hooks ( Fig. 2 D-F). Compound spinigers commencing from first chaetiger to near pygidium, with long, tapered blade bearing unilateral fine serration ( Fig. 3C, F ). Subacicular hooks amber in colour, commencing from anterior chaetiger (26th-58th) to near end and inferior to bundle of spinigers, one per parapodia; slightly thinner than aciculae; Most subacicular hooks unidentate, thin and bidentate ones only present in last few parapodia ( Figs. 2 D-F; 3D-E).

Pygidium round, dorsally positioned, with two pairs of tapering pygidial cirri attached at the ventral edge, one pair 2 x and another pair half of pygidial diameter ( Fig. 1 G-H).

Variations in morphological characters: The complete specimens vary in length from 2.3 cm for 147 segments to 14.7 cm for 288 segments ( Table 1). The first pair of branchia occurs in chaetiger 15- 35, being more posterior in larger individuals. The maximum number of branchial filaments varied between 5-10. In complete specimens, the last pair of branchia is present in the last 8th-10th chaetiger with only one filament. Most of the specimens have a maxilla formula of Mx II = 5 + 5-6 (21 specimens) or Mx II = 6 + 5-6 (2 specimens); but in one specimen the left Mx II was broken and the right has five teeth. Subacicular hooks commence from parapodia 26-58, but all of these parapodia carry only one subacicular hook. Hooded bidentate subacicular hooks are only present on terminal posterior chaetigers, which explains why these hooks are missing in the several incomplete specimens.

Distinction from closely related species: Marphysa hongkongensa n. sp. resembles the other 25 Marphysa species belonging to Group B2 by having compound spinigers but no compound falcigers, and having branchiae in middle and posterior segments. This species can be distinguished from the type species M. sanguinea ( Montagu, 1813) by having unidentate and unhooded subacicular hook from anterior to middle chaetigers, hooded bidentate hook only present in terminal posterior chaetigers and subacicular limbate capillaries absent. Of the seven species that have been considered to be valid in Chinese waters ( Liu et al. 2017 2018), M. sinensis Monro, 1934 belongs to the Belli group (Group D1) by having both compound spinigers and falcigers. M. orientalis Treadwell, 1936 has pectinate chaetae from more posterior chaetigers (193th vs. 1st chaetiger), fewer teeth in Mx II (3 + 3 vs. 5-6 + 5-6), and a smaller maximal number of branchial filaments (3 vs. 5-10). M. multipectinata Liu, Hutchings & Sun, 2017 has pectinate chaetae first present from more posterior chaetigers (70th vs. 1st chaetiger), fewer teeth in Mx II (3 + 3 vs. 5-6 + 5-6), and a smaller maximal number of branchial filaments (3-5 vs. 5-10). M. tribranchiata Liu, Hutchings & Sun, 2017 has pectinate chaetae first present from more posterior chaetigers (20th vs. 1st chaetiger), fewer teeth in Mx II (4 + 4 vs. 5-6 + 5-6), and a smaller maximal number of branchial filaments (2-3 vs. 5-10). M. tripectinata Liu, Hutchings & Sun, 2017 has subacicular hook from more posterior chaetigers (170th vs. 26th- 58th chaetiger), and has only one pair of pygidial cirri. M. bulla Liu, Hutchings & Kupriyanova, 2018 has fewer teeth in Mx II (4 + 4 vs. 5-6 + 5-6), subacicular hooks from more posterior chaetigers (71th vs. 26th-58th chaetiger), more teeth (30-40 vs. 15-23) in posterior fine-toothed isodonts, and fewer teeth (3-5 vs. 7-13) in posterior large-toothed anodonts. M. maxidenticulata Liu, Hutchings & Kupriyanova, 2018 has smaller maximal number of branchial filaments (3 vs. 5-10), and fewer teeth (3-6 vs. 7-13) in posterior large-toothed anodonts.

Marphysa hongkongensa n. sp. can also be distinguished from the other 18 species of Marphysa of the Group B2 that were originally described from localities beyond Chinese waters. Nine species [i.e. M. acicularum Webster, 1884 ( Molina-Acevedo & Carrera-Parra, 2015); M. brasiliensis ( Hansen, 1882) ; M. elityeni Lewis & Karageorgopoulos, 2008 ; M. fauchaldi Glasby & Hutchings, 2010 ; M. gravelyi Southern, 1921; M. kristiani Zanol, da Silva & Hutchings, 2016 ; M. mullawa Hutchings & Karageorgopoulis, 2003 ; M. schmardai Gravier, 1907 and M. viridis Treadwell, 1917 ( Molina-Acevedo & Carrera-Parra, 2015)] have bidentate subacicuar hook, but M. hongkongensa n. sp. has unidentate subacicular hook. M. victori Lavesque, Daffe, Bonifácio & Hutchings, 2017 has no subacicular hook. M. januarii ( Grube, 1881) and M. teretiuscula ( Schmarda, 1861) have a smaller maximal number of branchial filaments (4 vs. 5-10). M. borradailei Pillai, 1958 ( Glasby and Hutchings, 2010) has a larger maximal number of branchial filaments (10- 20 vs. 5-10). Three species (i.e. M. macintoshi Crossland, 1903 ; M. mangeri Augener, 1918 and M. tamurai Okuda, 1934 ) have an undivided prostomium but M. hongkongensa n. sp. has a bilobed prostomium. M. sanguinea ( Montagu, 1813) and M. furcellata Crossland, 1903 have subacicular limbate capillaries but this type of chaetae are absent in M. hongkongensa n. sp. M. simplex ( Langerhans, 1884) ( Crossland 1903) has fewer teeth in Mx II than M. hongkongensa n. sp. (3 + 3 vs. 5 + 5-6).

Etymology: The specific epithet hongkongensa refers to the type locality of Hong Kong.

Habitat: Lower intertidal zone on sandy shores.

Distribution: Currently only known from Tolo Harbour, Hong Kong. Given its common occurrence on several beaches in Tolo Harbour (as found in this study) and the wide presence of “ Marphysa sanguinea ” recorded from local sea shores ( Morton and Morton 1983), it is expected that this species is also distributed on other shores along the eastern coasts of Hong Kong.

Molecular analysis

Partial DNA sequences of COI (435bp) and 16S RNA (466bp) were used for phylogenetic analysis based on the Maximum Likelihood (ML) method ( Fig. 4 ). Results based on the two single genes showed that Marphysa species form a monophyletic clade; however, support for the clade is weak for both single genes (bootstrap values <65). The results of COI and 16S concatenated sequences are consistent with each single gene in that Marphysa species form a monophyletic clade, but the support value was higher (bootstrap values = 82). These results are in agreement with the results of Zanol et al. (2010 2014). Phylogenetic analysis placed M. hongkongensa n. sp. as sister to M. tripectinata Liu, Hutchings and Sun, 2017 based on the COI gene; and as sister to a clade consisting of M. victori Lavesque, Daffe, Bonifácio & Hutchings, 2017 and M. viridis Treadwell, 1917 based on 16S gene with low bootstrap values (bootstrap values <50). Nevertheless, there are much larger interspecific divergences in COI sequences (19.5%) and 16S sequences (12.1%) between M. hongkongensa n. sp. and the closest related Marphysa species than the intraspecific divergences (<1%) of both two genes in Marphysa species. These analyses, therefore, support M. hongkongensa n. sp. as a valid species.

Key to species in the Marphysa sanguinea complex from Chinese waters

(modified after Liu et al. 2017)

1. Subacicular hooks present after chaetiger 70 .................. 2

1. Subacicular hooks present before chaetiger 60 ............... 3

2. Subacicular hooks present from posterior chaetigers, Mx II = 3 + 3, branchiae from chaetigers 35-45, up to 3 filaments; pectinates from chaetiger 193, posterior pectinate 3 types: asymmetrical isodont approximately 30 teeth, median teeth anodont 16 teeth, large-toothed anodont 4-5 teeth ............. .......................................................................... M. orientalis

2. Subacicular hooks present from 170th chaetiger, Mx II = 5 + 5, branchiae from chaetiger 15-24, up to 6-8 filaments; Pectinates from first few chaetigers, four types, anterior isodonts approximately 10 teeth, posterior pectinates 3 types: fine-toothed isodont> 30 teeth, median teeth anodont 14-18 teeth, large-toothed anodont 5-7 teeth ........ ...................................................................... M. tripectinata

2. Subacicular hooks present from approximately 71th chaetiger, Mx II = 4 + 4, branchiae from chaetiger 29-36, up to 5 filaments; pectinates from first few chaetigers, four types, anterior isodonts 13-17 teeth, posterior pectinates 3 types: fine-toothed isodont approximately 30-40 teeth, median-toothed anodont approximately 14 teeth, large-toothed anodonts 3-5 teeth, ventral cirri with a swollen base and a globular tip ................................................... M. bulla

3. Subacicular hooks present after 20th chaetiger, pectinates present from first few chaetigers, 4 types ......................... 4

3. Subacicular hooks present from 20th chaetiger, pectinates present after 20th chaetiger, 3 types ................................ 5

4. Subacicular hooks present from chaetiger 25, Mx II = 4 + 6, branchiae from chaetiger 28, up to 3 filaments; anterior isodonts 10-12 teeth; posterior pectinates 3 types: fine-toothed isodont approximately 25 teeth, median-toothed anodont 14 teeth, large-toothed anodont 3-6 teeth ............. ............................................................... M. maxidenticulata

4. Subacicular hooks present from 26 to 58 chaetigers, Mx II = 5 + 5-6, branchiae from chaetiger 14-35, up to 5-10 filaments, 1-3 anterior isodonts, 8-15 teeth, posterior pectinate 3 types: approximately 5 fine-toothed isodonts arranged in 2 rows, approximately 23 teeth; 1-2 median-toothed anodonts, approximately 15 teeth; 2-3 large-toothed anodonts, 7-13 teeth........ M. hongkongensa n. sp.

5. Mx II = 4 + 4, branchiae present from chaetigers 16-26, up to 2-3 filaments; pectinate from approximately 20th chaetiger, anterior fine-toothed isodonts approximately 12 teeth, posterior pectinate 2 types: fine-toothed isodont approximately 17 teeth, median-toothed anodont 14 teeth, large-toothed anodont absent.................... M. tribranchiata

5. Mx II = 3 + 3, branchiae present from chaetigers 29-32, up to 3-5 filaments; pectinate from approximately chaetiger 70, anterior fine-toothed isodonts absent; posterior pectinate 3 types: fine-toothed isodont approximately 12-16 teeth, median-toothed anodont 14 teeth, large-toothed anodont approximately 4 teeth .............................. M. multipectinata

Figures

Fig. 1. Marphysa hongkongensa n. sp. A-E, I-J, paratype (AM W.50939); F-H, paratype (AM W.50940). (A) living worm, dorsal view; (B) anterior end, dorsal view; (C) anterior end, ventral view; (D) anterior end, lateral view, labels represent chaetiger numbers; (E) anterior parapodia, lateral view, labels represent chaetiger numbers; (F) posterior parapodia, lateral view; (G) pygidium, dorsal view, showing pygidium and long pygidial cirri (lpc); (H) pygidium, ventral view, showing short (spc) and long pygidial cirri (lpc); (I) dissected maxillary apparatuses, dorsal view; (J) mandible, ventral view. Abbr. bf, branchial filament; bl, buccal lip; dc, dorsal cirrus; la, lateral antenna; lpc, long pygidial cirrus; ma, median antenna; pa, palps; pt, peristomium; py, pygidium; spc, short pygidial cirrus; vc, ventral cirrus. Scale bars: A = 2 mm; B-J = 1 mm.

Fig. 2. Marphysa hongkongensa n. sp. parapodia, left side, anterior views. A-C, paratype (SWIMS-ANN-18-014); D-F, paratype (SWIMS-ANN-18-023). (A) chaetiger 2; (B) chaetiger 30; (C) chaetiger 70; (D) chaetiger 143; (E) chaetiger 153; (F) chaetiger 163. Abbreviations: ac, acicula; bf, branchial filament; dc, dorsal cirrus; sbh, subacicular hook; sbs, subacicular spinigers; spc, supra-acicular capillary; vc, ventral cirrus. Scale bars: A, D-F = 200 μm; B-C = 500 μm.

Fig. 3. Marphysa hongkongensa n. sp. chaetae. A-C, G-I, L-N: paratype (SWIMS-ANN-18-014); D-E: paratype (SWIMS-ANN-18-023); F, J-K, O-P: holotype (SWIMS-ANN-18-012). (A) chaetiger 30, capillaries; (B) posterior chaetiger, capillaries; (C) chaetiger 30, CS; (D) chaetiger 75, unidentate SH; (E) chaetiger 165, bidentate SH; (F) chaetiger 30, CS; (G) chaetiger 2, AFI; (H) chaetiger 70, FI; (I) chaetiger 160, PFI; (J) chaetiger 26, AFI; (K) chaetiger 103, PFI; (L) chaetiger 160, PMA; (M-N) chaetiger 165, PLA; (O-P) chaetiger 147-148, arrangement of pectinates, showing PFI, PMA and PLA. Abbr. AFI: anterior fine-toothed isodont (a); CS: compound spiniger; FI: fine-toothed isodont; PFI: posterior fine-toothed isodont (b); PLA: posterior large-toothed anodont (d); PMA: posterior mediantoothed anodont (c); SH: subacicular hook. Scale bars: A-D, L-P = 50 μm; E, G-K = 20 μm; F = 10 μm.

Fig. 4. Phylogenetic tree generated by maximum likelihood (ML) method based on COI (A), 16S (B) and their concatenated sequences (C). Numbers on the branches represent ML bootstrap values (maximum: 100) based on 1000 replicates. Genbank accession numbers of the COI and 16S genes used are shown in parentheses.