Branchinotogluma jiaolongae, Han & Zhou & Chen & Wang, 2024

Han, Yuru, Zhou, Yadong, Chen, Chong & Wang, Yueyun, 2024, Diversity and biogeography of scale worms in the subfamily Lepidonotopodinae (Annelida: Polynoidae) from Indian Ocean hydrothermal vents with descriptions of four new species, Zoological Journal of the Linnean Society 201 (2), pp. 290-304 : 297-299

Branchinotogluma jiaolongae sp.nov.

( Fig. 5 )

ZooBank registration: urn:lsid:zoobank.org:act:B0F7F3C1-E3AF-470A-8C00-BDD3C56563C7 .

Polynoidae sp. 3— Zhou et al. 2018b.

Polynoidae indet. #3— Zhou et al. 2022.

Diagnosis: Medium-sized Branchinotogluma found in both CR and SWIR with oval prostomium, cylindrical anterior lobes, pharynx appendages including three dorsal papillae and two ventral papillae. Five pairs of ventral papillae on segments 11–15 on female, and four pairs of long ventral papillae on segments 12–15 followed by two pairs of ventral lamellae on male. Neuropodia on segment 21 on male elongated.

Type locality: Tiancheng vent field, SWIR .

Type material: Holotype ( RSIO35218 ): female, 11.50 mm in length, 4.58 mm in width, Tiancheng vent field (27.95°S, 63.53°E, 2682 m deep), SWIR, Dive 87, 23 December 2014 . Paratype 1 ( RSIO35215 ): male, 13.01 mm in length, 7.32 mm in width, same collecting data as the holotype . Paratype 2 ( RSIO38118 ): male, 9.89 mm in length, 2.38 mm in width, Wocan vent field (6.36°N, 60.53°E, 2920 m deep) Carlsberg Ridge, Dive 129, 14 March 2017 . Paratype 3 ( RSIO38128 ): female, 5.12 mm in length, 2.05 mm in width, same collecting data as paratype 2.

Description: Body short, 21 segments, somewhat tapered anteriorly and posteriorly ( Fig. 5A, B ). Elytra 10 pairs, present on 2, 4, 5, and following uneven segments until segment 19; elytra subreniform or oval, smooth ( Fig. 5C ), iridescent when fresh and pale white in ethanol, covering the dorsum. Branchiae arborescent, with short, terminal filaments, present on segments 3–21, larger on middle segments than on the anterior and posterior ones; branchiae separate into two clusters, one attached to lateral side of dorsal tubercle or elytrophore, the other basally to notopodia ( Fig. 5D ).

Prostomium oval and bilobed ( Fig. 5E ), cylindrical anterior lobes with tapering frontal filaments as long as anterior prostomium lobes ( Fig. 5E ). Middle antenna inserted in anterior notch with short, cylindrical ceratophore; style conical with long and slender terminal filament. Eyes absent ( Fig. 5E ). One pair of smooth, stout, tapering palps, lateral to prostomium ( Fig. 5F ). First segment, achaetous, fused to prostomium, indistinct ventrally; two pairs of tentacular cirri, slender, as long as palps, with short, cylindrical tentaculophores; styles with long, terminal filaments ( Fig. 5E—F ). Segment 2 with biramous parapodia bearing the first pair of elytra and bracts ( Fig. 5E ); ventral cirri basal to the neuropodia and much longer than ventral cirri on following segments ( Fig. 5F ). Mouth ventrally positioned between segments 1 and 2 ( Fig. 5F ). Pharynx with three dorsal papillae and two ventral papillae; two pairs of jaws, each with numerous teeth on the inner border ( Fig. 5G ).

Parapodia on the following segments biramous ( Fig. 5K–N ). Notopodia with acicular lobe on the ventral side ( Fig. 5K, L ); neuropodia longer than notopodia, with tapering acicular prechaetal lobes and rounded postchaetal lobes ( Fig. 5K, L ). Dorsal cirri long, extending beyond neurochaetae, with long, cylindrical cirrophores and slender filaments ( Fig. 5H ). Notochaetae in bundles, stout, straight ( Fig. 5K, L, N ), with two rows of inconspicuous and minute spines extending from the middle part to pointed tips ( Fig. 5O ). Neurochaetae numerous, slender, in fan-shaped bundles ( Fig. 5K, L, N ). Supraacicular neurochaetae straight, with two rows of widely-spaced spines beginning subdistally and extending to pointed tips ( Fig. 5P ). Upper subacircular neurochaetae with two rows of prominent spines distributing subdistally and more densely serrated spines at the tips ( Fig. 5Q ). Lower subacicular neurochaetae slender with two rows of feather-like spines on distal half parts ( Fig. 5R ).

On female, ventral papillae five pairs, tiny, round, present on segments 11–15 ( Fig. 5B ); pygidium rounded, anal cirri missing during collection ( Fig. 5A, B ).

On male, branchiae present on segments 3–18 ( Fig. 5H ). Ventral papillae four pairs, present on segments 12–15, long, tapering with slender tips ( Fig. 5I ) and followed by two pairs of ventral lamellae on segments 16 and 17. Segments 18 and 19 with ventral cirri longer than previous ones ( Fig. 5J ). Segments 20 and 21 fused and strongly modified ( Fig. 5H ); notopodial acicular lobes of segment 20 fused to dorsal cirriphores with few notochaetae ( Fig 5M ); neuropodia of segment 21 elongated, twice as long as that on segment 20 ( Fig. 5H, J ). Pygidium rounded with a pair of long and slender anal cirri ( Fig. 5H, J ).

Etymology: This species is named for HOV Jiaolong.

Distribution: The species has been found in hydrothermal vents in both SWIR and CR, including Tiancheng vent field, SWIR, and Wocan hydrothermal vent field, CR.

Remarks: Branchinotogluma jiaolongae sp. nov. is morphologically most similar to B. sandersi Pettibone, 1985 in the oval prostomium, cylindrical anterior lobes, pharyngeal appendages (three dorsal papillae and two ventral papillae), and five pairs of ventral papillae on segments 11–15 on female ( Pettibone 1985c). However, notochaetae decorated with two rows of spines in the new species is distinct from the smooth notochaetae in B. sandersi ( Pettibone 1985c) . In addition, some morphological characteristics on the male can also separate them from each other, including ventral lamellae (three pairs in B. sandersi vs. two pairs in B. jiaolongae sp. nov.) and neuropodia on segment 21 (short in B. sandersi vs. elongated in B. jiaolongae sp. nov.) ( Pettibone 1985c, Zhou et al. 2018b).

Molecular analyses

For Branchinotogluma , the interspecific pairwise distances ranged between 8.45% and 29.82%, much higher than the intraspecific distances (0–1.12%). The two new species from Indian Ocean, B. kaireiensis sp. nov. and B. jiaolongae sp. nov., exhibited lowest genetic divergence with B. pettiboneae Wu et al., 2019 (GTR distance 12.77%) from Manus Back-Arc Basin and an undescribed Atlantic Branchinotogluma sp. DC-2019 sensu Cowart et al., 2020 (GTR distance 15.45%), respectively (Supporting Information, Table S1). For Levensteiniella , the pairwise distances within species ranged between 0 and 1.00%, while interspecific distances ranged between 19.29 and 30.52%. The two Indian Ocean species, Levensteiniella pettiboneae sp. nov. and Levensteiniella longqiensis sp. nov. were recovered genetically closest to each other (GTR distance 19.29%) (Supporting Information, Table S2).

Phylogenetic relationships within Lepidonotopodinae were inferred using concatenated alignments of six genes (COI, 16S, 18S, 28S, Cytb,and H3)from58species(Supporting Information, Table S3), including 25 species of Branchinotogluma , 10 species of Branchipolynoe , eight species of Lepidonotopodium , six species of Levensteiniella , six species of Peinaleopolynoe , and one species from each of three genera, Branchiplicatus , Bathykurila , and Thermopolynoe . Both BI and ML analyses recovered topologies similar to Hatch et al. (2020), Jimi et al. (2022), and Wu et al. (2023). Branchiplicatus cupreus (Pettiboneae 1985b) was recovered in a basal position. Lepidonotopodium , Levensteiniella , Bathykurila , Thermopolynoe , and one Branchnotogluma species ( B. segonzaci Miura and Desbruyères, 1995 ) formed a main branch (BS/PP = 100/1) sister to another branch comprising of the remaining 24 Branchnotogluma species and all of the Branchipolynoe and Peinaleopolynoe species (BS/PP = 100/1). Lepidonotopodium was recovered as paraphyletic, with seven species forming a clade (BS/PP = 52/0.94), but the type species of the genus L. fimbriatum Pettibone, 1983 clustering with Thermopolynoe branchiata Miura, 1994 (BS/PP = 85/1). The six Leventseiniella species formed a well-supported clade (BS/ PP = 100/1). Its sister-relationship with the Lepidonotopodium clade received moderate support (BS/PP = 69/0.71). The two Indian Ocean Leventseiniella species were recovered as a species pair (BS/PP = 100/1) sister to Leventseiniella intermedia from the North-East Pacific (BS/PP = 100/0.94), and they formed a group with a well-supported sister-species pair, Leventseiniella iris (East Scotia Ridge)/ Leventseiniella undomarginata (Okinawa Trough) (BS/PP = 100/1). Leventseiniella manuensis (Manus Back–Arc Basin) was recovered in a basal position within the clade.

Branchnotogluma was recovered as paraphyletic with species divided into eight clades, each assigned a number (consistent with Hatch et al. 2020) in Figure 6 . Peinaleopolynoe and Branchipolynoe were recovered as monophyletic groups sister to clades5 and 8, respectively( Fig.6 ). The phylogenetic positions of the eight Branchnotogluma clades relative to each other, as well as to other genera, were poorly resolved, due to the low supporting values at some nodes. However, clades 2, 4, 6, and 8, together with Branchipolynoe , formed a group (BS/PP = 93/0.87) sister to clade 3 (BS/PP = 84/0.93). The three Indian Ocean species were separated into three clades, clades 3, 5, and 7. Within clade 3, Branchinotogluma jiaolongae sp. nov. was clustered with an undescribed Atlantic species, Branchinotogluma sp. DC-2019 sensu Cowart et al., 2020, forming a subclade (BS/PP = 84/0.89) sister to a species pair from the East Pacific ( B. sandersi / B. cf. sandersi ). Within clade 7, Branchinotogluma kaireiensis sp. nov. was recovered with high support (BS/PP = 100/1) as sister to B. pettiboneae (collected from the Manus Basin). They formed a well-supported group (BS/PP = 100/1) with Branchinotogluma robusta Wu et al., 2023 from the South China Sea, Branchinotogluma sp. nov. 2 and Branchinotogluma sp. nov. 3 [both sensu Goffredi et al. (2017)]. Like Zhou et al. (2018a) and Hatch et al. (2020), the previously reported Indian Ocean species B. bipapillata was recovered as sister to Branchinotogluma sp. nov. 1 [sensu Goffredi et al. (2017)] from the East Pacific.

Figures

Figure 5. Branchinotogluma jiaolongae sp. nov. Holotype (RSIO35218, female) in dorsal (A) and ventral views (B); C, right elytron from segment 5 of paratype RSIO35215 in dorsal view; branchiae and segments 1 and 14 in dorsal (D) view of holotype RSIO35218; head and anterior segment of paratype RSIO38118 in dorsal view (E) and ventral view (F). G, anterior view and dorsal view of pharynx with papillae indicated by white arrows on paratype RSIO38128; posterior segments on paratype RSIO35215 in dorsal view (H) and ventral view (J). I, ventral papillae on segments 12–15 of paratype RSIO35215.Posterior view (upper position) and anterior view (lower position) of right parapodia on segments 3 (K) and 9 (L) of holotype RSIO35218. M, left parapodia on segment 20 of paratype RSIO35215 in anterior view (upper position) and posterior view (lower position). N–R, holotype RSIO35218.N, posterior view of right parapodia on segment 9; O, notochaetae on segment 3 of holotype; P, tips of supracicular neurochaetae of segment 9 of holotype; Q, tips of subacicular neurochaetae on segment 9 with details of tips of supraacicular neurochaetae of holotype; R, upper subacicular neurochaetae on segment 3 of holotype. Scale bars:A, B = 2mm, C, D, F, H = 1mm, K, L = 0.5mm, E, G, M = 0.2mm, I, J = 0.5mm, N = 0.6mm, O = 20 μm, P = 25 μm, Q = 10 μm, 2μm in small window, R = 4 μm.

Figure 6. Phylogenetic reconstruction from the combined analysis using six genes (COI, 16S, 18S, 28S, Cytb, and H3). Numbers next to nodes are ML bootstrap percent/ Bayesian inference (BI) posterior probability.Abbreviations: * indicates 95% ultrafast bootstrap or greater and 0.95 posterior probability or greater; ~ indicates nodes not found; red marks the Indian Ocean, CIR = Central Indian Ridge, CR = Carlsberg Ridge, SWIR = South-West Indian Ridge.