Integrative taxonomy of West African Magelona (Annelida: Magelonidae): species with thoracic pigmentation Author Mortimer, Kate Author Kongsrud, Jon Anders Author Willassen, Endre text Zoological Journal of the Linnean Society 2022 2021-10-22 194 4 1134 1176 journal article 55992 10.1093/zoolinnean/zlab070 b9609b0c-597f-4617-8bc5-7fbd253302c2 0024-4082 6459404 278AA1B0-674E-414D-A47A-D87F43E2D6E4 MAGELONA ALLENI WILSON, 1958 ( FIGS 3–6 ) Magelona alleni Wilson (1958) , Mackie et al . (1995 , 2006), Fiege et al. (2000) , Meiβner & Darr (2009), Robinson et al. (2009) , Mills & Mortimer (2019) , Mortimer et al. (2020) . Magelona cincta Fauvel (1936) , Mare (1942) , Clarke & Milne (1955) (see: Wilson, 1958 ). Type locality: UK : Plymouth , Rame Mud (a deposit of black sandy mud, close to station 93 of Ford (1923) , viz. Rame Head, E. ½ N. Tregantle, N. ½ E., see Mare (1942) , approximately 50.302°N , 4.244°W and 60 m . Type material examined: Holotype , af ( BMNH 1958.5.2.1), mud, Coll. D.P Wilson, 1958 ; Paratypes : Rame Head, 1c ( BMNH 1958.5.2.2); 1af ( BMNH 1958.5.2.3); 15af, 3f, 3 palps (BMNH 1958.5.2.4–10), Coll. E. Ford / M.F. Mare , 1939 . Table 4. Statistics from Species Delimitation with Rosenberg’s Test ( Masters et al. , 2011 ) and bPTP support ( Zhang et al. , 2013 ) computed from the species tree and from the COI gene tree. See text for explanation. NA: not computed

Species	n	Closest	Monophyletic?	Intra	Inter	Intra/	P ID(Strict)	P ID (Liberal)	Av(MRCA-tips)	P(Randomly	Rosenberg’s	bPTP	bPTP
Species	Dist	Dist - Closest	Inter	Distinct)	P(AB)	COI
M. johnstoni	1	M. mirabilis	yes	0.000	0.656	0.000	0.000	0.96 (0.83, 1.0)	0.0000	NA	1.22E-03	1.00	1.00
M. minuta	1	M. fasciata	yes	0.000	0.457	0.000	0.000	0.96 (0.83, 1.0)	0.0000	NA	1	1.00	1.00
M. picta	2	M. guineensis	yes	0.002	0.073	0.030	0.58 (0.43, 0.73)	0.97 (0.81, 1.0)	0.0010	0.05	0.03	1.00	0.99
M. mackiei	6	M. fasciata	yes	0.003	0.186	0.020	0.92 (0.80, 1.0)	0.98 (0.88, 1.0)	0.0015	0.05	1.00E-05	0.96	0.97
M. filiformis	1	M. minuta	yes	0.000	0.465	0.000	0.000	0.96 (0.83, 1.0)	0.0000	NA	1	1.00	1.00
M. guineensis	3	M. nanseni	yes	0.006	0.067	0.080	0.74 (0.56, 0.91)	0.96 (0.82, 1.0)	0.0035	0.05	0.17	1.00	0.99
M. fasciata	11	M. mackiei	yes	0.002	0.186	0.010	0.98 (0.89, 1.0)	1.00 (0.95, 1.0)	0.0012	0.05	1.00E-05	0.98	0.95
M. alleni	14	M. fasciata	yes	0.004	0.31	0.010	0.98 (0.92, 1.0)	1.00 (0.96, 1.0)	0.0036	0.05	9.00E-12	0.95	0.98
M. mirabilis	1	M. fasciata	yes	0.000	0.641	0.000	0.000	0.96 (0.83, 1.0)	0.0000	NA	1.22E-03	1.00	1.00
M. nanseni	1	M. guineensis	yes	0.000	0.067	0.000	0.000	0.96 (0.83, 1.0)	0.0000	NA	0.17	1.00	1.00

Table 5. Mean p -distance (below diagonal) with standard errors (above diagonal) between and within species of Magelona , with standard error (SE). n/c, not calculated. For all species, BIN assignments in BOLD with numbers (N) of COI sequences assigned to each BIN

Species	1	2	3	4	5	6	7	8	9	10	Within	Within SE	BOLD BIN	N
1	M. alleni	0,017	0,017	0,018	0,016	0,017	0,018	0,018	0,016	0,015	0,006	0,002	ADA7054	14
2	M. mackiei	0,207	0,016	0,014	0,017	0,017	0,015	0,013	0,016	0,015	0,004	0,001	ADA5678	6
3	M. picta	0,226	0,189	0,016	0,011	0,012	0,016	0,017	0,018	0,016	0,002	0,001	ADA5677	2
4	M. fasciata	0,207	0,177	0,189	0,016	0,016	0,015	0,016	0,016	0,016	0,004	0,001	ADA6415	11
5	M. nanseni	0,225	0,193	0,104	0,192	0,011	0,016	0,018	0,018	0,016	n/c	n/c	ADB4817	1
6	M. guineensis	0,223	0,199	0,100	0,203	0,093	0,015	0,017	0,019	0,016	0,007	0,003	ADA6414	3
7	M. johnstoni	0,239	0,198	0,218	0,231	0,226	0,211	0,016	0,018	0,014	n/c	n/c	ABU8508	1
8	M. mirabilis	0,241	0,194	0,203	0,207	0,215	0,198	0,231	0,017	0,016	n/c	n/c	ADA7606	1
9	M. filiformis	0,227	0,243	0,255	0,241	0,269	0,264	0,257	0,242	0,018	n/c	n/c	ADA6413	1
10	M. minuta	0,224	0,218	0,210	0,226	0,199	0,208	0,226	0,208	0,254	n/c	n/c	ACJ4785	1

Figure 3. Magelona alleni (Morocco St. 2011410–GR45, NMW.Z.2021.001.0001): A, anterior region (dorsal view showing pigment band); B, prostomium, dorsal view (base of RH palp visible); C, E–K, M, O, parapodia of chaetigers 1–9, 11, respectively (anterior views); D, neuropodial lamella of chaetiger 1 (ventral view); L, parapodium of chaetiger 8 (lateral view); N, neuropodium of chaetiger 9 (lateral view); P, Q, tridentate abdominal hooded hooks (oblique lateral and lateral views, respectively). Figure 4. Magelona alleni (Morocco St. 2011410–GR45, NMW.Z.2021.001.0001), methyl green staining pattern: A, anterior region (dorsal view, showing pigment band. RH palp attached); B, anterior region (ventral view, showing partially everted burrowing organ); C, prostomium and first chaetiger (dorsal view); D, right-hand parapodia of chaetigers 7–10 (lateral view). West African material: Morocco : St. 2011410–GR45, 1af in 75%Etoh ( NMW .Z.2021.001.0001, figured); 8af, 2f, 2pf in 75%Etoh ( NMW .Z.2021.001.0002); St. 2011410–GR50, 2af in 75%Etoh ( ZMBN 132134). Western Sahara : St. 2011410–GR27: 2af in 75%Etoh ( ZMBN 132136); 1af in 96%Etoh ( ZMBN 132125); 1af in 96%Etoh ( ZMBN 107315, DNA-voucher); 1af in 96%Etoh ( ZMBN 115754, DNA-voucher). Senegal : St. 2011410–SL12: 18af in 96%Etoh ( ZMBN 132135); 22af in 96%Etoh ( ZMBN 132124); 1af in 96%Etoh ( ZMBN 107321, DNA-voucher); 1af in 96%Etoh ( ZMBN 115753, DNA-voucher); 6af in 96%Etoh ( NMW .Z.2020.000.0003). Guinea (Conakry) : St. 2012404–GR02, 1af in 96%Etoh ( ZMBN 107335, DNA-voucher). São Tomé and Príncipe : St. ES–77–- SBE: 3af in 75%Etoh (exact locality unknown). Figure 5. Magelona alleni (A, B, holotype BMNH 1958.5.2.1; C, paratype BMNH 1958.5.2.2): A, anterior region (dorsal view); B, prostomium and first chaetiger (ventral view, showing mouth and base of LH palp); C, posterior region (dorsal view). Figure 6. Magelona alleni (A–F, holotype BMNH 1958.5.2.1; G, paratype BMNH 1958.5.2.2): A, B, anterior region (dorsal and ventral views, respectively); C, D, prostomium and first five chaetigers (dorsal and ventral views, respectively); E, anterior region (laterodorsal view); F, thoracic/abdominal junction showing chaetigers 4(RH) to 13 (LH) (lateral view); G, posterior region (dorsal view). Additional European material: Norway : Skagerrak coast, 58.388°N 8.749°E , 66 m , 28.06.2006 , 1af in 96%Etoh ( ZMBN95087 , DNA-voucher); 1af in 96%Etoh ( ZMBN95091 , DNA-voucher) . UK : Isles of Scilly , 49.9210°N 6.3352°W , 15 m , 25.06.2009 , 1af in 96% Etoh ( NMW .Z.2009.027.0523, DNA-voucher); Old Grimsby, Tresco, Isles of Scilly , 49.96°N 6.33°W , low tide, 10.09.2006 , 1af in 96%Etoh ( NMW .Z.2006.019.0799, DNA-voucher); Mill Bay near East Portlemouth , Devon , 50.2304 ° N 3.7679 ° W , low shore, 17.05.2003 , 1 af in 96 % Etoh ( NMW . Z. 2003.035.0018, DNA- voucher); Jennycliff Bay , Plymouth , 50.3483°N 4.1288° W , 8 m , 27.03.2017 , 1 af in 96 %Etoh ( NMW .Z.2018.007.0001, DNA-voucher); 1af in 96%Etoh ( NMW .Z.2018.007.0002, DNA-voucher); 1af in 96%Etoh ( NMW .Z.2018.007.0003, DNAvoucher); Cardigan Bay , Wales, 52.3626°N 4.1776°W , 26 m , 31.11.2010 , 1af in 96%Etoh ( NMW .Z.2010.039. 0001, DNA-voucher) . Diagnosis: Prostomium width similar to length, no prostomial horns. Chaetigers 1–9 with slender triangular lamellae, distinct pigment band of the posterior thorax. All thoracic chaetae capillary. Abdominal lateral lamellae subequal, those of the notopodia clearly larger. Abdominal hooks tridentate, in two groups, vis-à-vis (face to face). No pouches observed, pygidium with stout lateral projections. Description: A large, stout species; with marked constriction between thorax and abdomen ( Figs 3A , 4A, D ), thorax dorsoventrally flattened, much thinner (when viewed laterally), but marginally wider (particularly in mid thorax) than the rounded abdomen. Holotype , anterior fragment: prostomium 0.75 mm long, 0.8 mm wide; thorax 4.25 mm long (including prostomium), 0.95 mm wide (between chaetigers 5 and 6); total length 6.1 mm for 14 chaetigers. Complete paratype : 3.5 cm long for 67 chaetigers. Figured MIWA specimen ( NMW .Z.2021.001.0001), anterior fragment:prostomium 1.2 mm long, 1.4 mm wide; thorax 7.1 mm long (including prostomium), 1.55 mm wide; abdomen 1.4 mm wide; total length approximately 12.4 mm for 20 chaetigers (width measurements not including parapodia).Thoracic chaetigers characteristically bulbous ( Figs 3A , 4A , 5A , 6A, B ), width greatest around chaetigers 4–6, body tapering towards chaetiger 9. Other anterior fragments measuring: 7.6–22.5 mm long for 14–41 chaetigers. Prostomium triangular ( Figs 3B , 4C , 6C ), length marginally shorter but similar to width (L: W ratio 0.79–0.96), distal portion clearly narrower than proximal. No prostomial horns, anterior margin straight and square, lateral prostomial margins slightly rounded. Prostomium with one pair of prominent longitudinal dorsal muscular ridges, abutting for majority of length, diverging only at distal third. Light angular striations apparent on dorsal surface of ridges towards distal tips in certain lights. A second pair of minute triangular ridges abutting prominent pair at their base, approximately a fifth of their length. Two large, roughly triangular areas noticeable (semitransparent and wrinkled), either side of the ridges, although not marked as in other species. Burrowing organ [previously termed ‘proboscis’, see Mortimer et al. (2012) for discussion on terminology] everted in 17 specimens , heart-shaped when fully everted, oval when partially everted ( Fig. 4B ). Burrowing organ transversely ridged, although that of the superior surface much fainter, ridges of figured anterior region distinct, almost zigzagged, giving a somewhat ‘wrinkled’ appearance. Palps arising ventrolaterally from base of prostomium, short and thick ( Figs 4A, B , 5B ) (retained, at least partially, on 11 specimens ) appearing ‘frilly’, with long papillae. Palps reaching approximately chaetigers 9–18 when folded backwards. Non–papillated proximal region of palps reaching chaetigers 2–3 (occasionally 4). Papillae short proximally, increasing gradually in size; papillae at distal tips long. Proximally 6–8 rows of papillae either side of an inconspicuous mid-palp line, devoid of papillae, medially 4–6, and distally 1–3 rows either side. Exact number of papillae, difficult to ascertain due to their size and abundance, and due to neighbouring rows of papillae being somewhat offset. Achaetous region behind the prostomium, roughly twice the size of chaetiger 1 ( Figs 3A , 5A ). Chaetigers 1–8 similar ( Figs 3C–L , 4D ); parapodia biramous. Notopodia with low prechaetal lamellae confluent with slender smooth-edged triangular to sinuous postchaetal lamellae, decreasing in size to chaetiger 6, but then increasing to chaetiger 9. No prechaetal superior dorsal lobes present on thoracic chaetigers. Neuropodia with low pre- and postchaetal lamellae encircling the chaetae, cuff-like, confluent with long slender triangular lamellae with pointed tips ( Fig. 3D ). These lamellae, although beneath the chaetal bundle, are initially in a slightly prechaetal position, becoming completely ventral by chaetiger 7. Neuropodial lamellae initially similar in size to the notopodia, but decreasing in size along the thorax. Chaetiger 9 ( Figs 3A , 4A, D ): shorter and narrower than preceding chaetigers. Notopodial prechaetal lamellae low, confluent with larger slender triangular postchaetal lamellae, slightly larger than those of the preceding chaetigers ( Fig. 3M ). No superior dorsal lobes observed. Neuropodia similar to preceding chaetigers ( Fig. 3N ), however, pre- and postchaetal lamellae roughly twice the height. Ventral lamellae shorter and more slender, directly underneath chaetal bundle. Chaetae of chaetigers 1–9 simple bilimbate winged capillaries. Parapodia of abdominal chaetigers ( Figs 3O , 4D ) with subequal lateral lamellae, much larger in the notopodia than neuropodia. Lamellae not basally constricted and with no obvious postchaetal expansion of lamellae behind chaetal rows. No dorsal (DML) or ventral (VML) processes observed at inner margins of chaetal rows. Abdominal chaetae tridentate hooded hooks ( Fig. 3P, Q ) of a similar size, superior two fangs parallel, above main fang. Hooks in two approximately equal groups for each ramus, main fangs vis-à-vis ( Fig. 3O ). Approximately 12–14 hooks per ramus in the anterior abdomen. No abdominal pouches observed. Pygidium with two stout triangular lateral projections ( Figs 5C , 6G ), anus large, terminal (see: Mills & Mortimer, 2019 ). One specimen ( Morocco , St. 2011410– GR45) ovigerous, eggs measuring approximately 130 μm in diameter. Brown, sediment-covered tube present on many specimens, inner surface consisting of layers of brown/ purple papery material, as noted by Mills & Mortimer (2019) . Tube tight-fitting and difficult to remove from preserved specimens without damaging parapodial lamellae. Colour: No living material observed, although live photographs of the species are provided by Mortimer et al. (2018) and Mills & Mortimer (2019) . Animals yellow to orange, often with distinct orange patches at the base of the prostomium and on achaetous first segment. Preserved specimens markedly white in colour with obvious dark brown pigment band present in the posterior thorax (now lost on type material, and faded in some MIWA specimens). Band strongest between chaetigers 5–9, an additional stripe is present between chaetigers 4–5, with speckled pigment in between ( Figs 3A , 4A, B ). Pigment band extends around the body from dorsal to ventral surface. However, some areas around the parapodia, particularly those of chaetigers 7–9, are devoid of pigmentation. Dorsal, white-speckled (glandular?) areas present between chaetigers 1–4, particularly noticeable on holotype ( Figs 5A , 6E ), but present on other specimens as well. Staining with methyl green ( Fig. 4 ) indistinct, showing no clear pattern. Although, speckled areas in the thoracic region and abdominal interparapodial patches more distinct in stained specimens. Habitat: Type specimens collected in muddy sediments from the shallow sublittoral. West African specimens collected at six stations from five countries, Morocco to São Tomé and Príncipe , at depths of 32–106 m . Other material collected from the intertidal zone to 66 m in fine muddy sands, fine sand and mud. Distribution: Confirmed records suggest that M. alleni is a North-East Atlantic species occurring from Norwegian waters to São Tomé and Príncipe , in the Gulf of Guinea ( Fig. 1 ). Remarks: The West African M. alleni specimens agree well with the type material, first described off Plymouth , England . Whilst, the breadth of the thoracic neuropodial lobes vary depending on the size of the animal, with those of larger specimens (e.g. ZMBN 107335) being comparatively wider, they are never broad and scoop-shaped, as seen in M. fasciata (described below) or M. cincta . The abdominal parapodium drawn by Wilson (1958 : fig. 1g ), shows a basically triangular abdominal neuropodial lamella, which appears different to that drawn from MIWA material ( Fig. 3O ). However, re-examination of the type material shows that the abdominal neuropodial lamellae are more slender and pointier than originally drawn by Wilson, and thus comparable to the West African material. Magelona alleni differs from all pigmented species in the MIWA region in the nature of the neuropodia of chaetiger 9, possessing slender, distinctly ventral lamellae, rather than postchaetal (those of M. fasciata , M. guineensis and M. mackiei possessing additional small triangular processes underneath the neurochaetal bundle, not present in M. alleni ). It further differs from M. guineensis , M. mackiei , M. nanseni and M. picta in not possessing superior dorsal lobes in the thorax. Additionally, it differs from M. guineensis , M. nanseni and M. picta in the nature of the prostomia, showing less distinct patternation either side of the dorsal muscular ridges. Magelona alleni differs from M. fasciata and M. mackiei , in possessing tridentate not bidentate abdominal hooded hooks. Lastly, M. alleni differs from all above-mentioned species and all known species carrying posterior thoracic pigmentation, except Magelona koreana Okuda, 1937 [originally M. japonica var. koreana , see Jones (1971) ] in possessing subequal lateral lamellae in the abdomen. Magelona koreana shares many similarities with M. alleni , but differs in having prostomial horns and in the lamellae of chaetiger 9, which have superior dorsal lobes and large postchaetal neuropodial lamellae. Wilson (1958) stated that M. alleni is likely to be a temperate-water species of the north-eastern Atlantic, further noting its presence from Dogger Bank (North Sea), Quiberon Bay (north-western France ) and possibly the Atlantic coast of Morocco . The latter locality was based on a fragment identified by Fauvel as M. cincta . Fauvel (1936) stated that ‘les pieds portent une grande lamellae dorsale et une plus petite ventral, et sont dépourvus de cirre’ and, as Wilson (1958) suggested, ‘This description almost perfectly describes the posterior parapodia of alleni ’. Kirkegaard (1959) agreed with Wilson and considered Fauvel’s (1936) record of M. cincta off Morocco to represent M. alleni . He further reported one additional specimen of M. alleni off Western Sahara ( Galathea St. 4). Amoureux (1976) additionally recorded M. alleni to be present from the Moroccan coast of the Straits of Gibraltar (at depths of 60 m ) and Bayed & Glémarec (1987a) recorded its occurrence off Moulay Bousselham and Casablanca ( 35–47 m ). The MIWA material confirms the presence of M. alleni off north-west Africa as noted by the above authors, and further extends its known distribution to São Tomé and Príncipe , in the Gulf of Guinea . The species has additionally been recorded in the Mediterranean, co-occurring with the morphologically similar M. equilamellae ( Mortimer et al. , 2020 ) , a species with which it has been previously confused ( Fiege et al. , 2000 ).