Abstract
This paper represents a continuation of taxonomic publications on the benthic fauna of polymetallic nodule fields in the eastern Clarion-Clipperton Zone (CCZ) using material collected during baseline environmental survey work targeting two exploration contract areas (“UK-1” and “OMS”) and one Area of Particular Environmental Interest, “APEI-6.” Families Poecilochaetidae Hannerz, 1956 and Spionidae Grube, 1850 of the annelid suborder Spioniformia were studied here. Taxonomic data are presented for 25 species from 98 records as identified by a combination of morphological and genetic approaches. Although sub-optimal morphological condition can prevent new species being formally described, it is essential that morphological, molecular, and voucher data are made available for future surveys. Descriptions of two new species—Poecilochaetus brenkei sp. nov. and Laonice shulseae sp. nov.—increase the number of formally described new annelid species from the areas targeted in this study to 15 and CCZ-wide to 46. We also discuss the commonly reported “cosmopolitan” deep-sea spionid Aurospio dibranchiata Maciolek, 1981, which we show represents several genetically distinct species (three of these from CCZ area alone) but without reliable morphological characters to separate them. Molecular data provide evidence that 15 out of 25 species reported here have a wide distribution within the eastern CCZ and that Aurospio sp. “NHM_2186” and the known species Prionospio amarsupiata Neal & Altamira in Paterson et al. 2016 may be cosmopolitan. Lastly, the molecular data provide insights into relationships within Spioniformia, suggesting that both Poecilochaetidae and Trochochaetidae belong within Spionidae.
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Introduction
This publication presents results from an ongoing baseline survey of biodiversity in the Clarion-Clipperton Zone (CCZ) polymetallic nodule region. In recent decades, this vast area (~6 million km2) of the central abyssal Pacific has been targeted for exploration of deep-sea mineral resources (Gollner et al. 2017). Such exploration is managed through exploration licenses, regulated by the International Seabed Authority (ISA), which stipulates the need for baseline studies, environmental impact assessments and the establishment of area-based management tools such as preservation areas (Lodge et al. 2014). Here, we focus on areas in the eastern part of the CCZ—the UK Seabed Resources Ltd (UKSRL) exploration contract area “UK-1,” the Ocean Mineral Singapore exploration contract area “OMS,” and an Area of Particular Environmental Interest, “APEI-6.”
There is a particular interest in the knowledge of the biodiversity (including identity of species, abundance, and species richness) and distribution of benthic taxa found within areas of potential mining operations (e.g., Glover et al. 2018; Smith et al. 2011, 2021). Both biodiversity and species ranges in the deep sea remain poorly understood due to several factors, but mainly owing to under-sampling and the lack of comparable datasets produced by different research groups and contractors (e.g., Smith et al. 2011, 2021). The latter factor is greatly confounded by the lack of formal description of the fauna given that most represent species new to science. Recent sampling and subsequent analytical efforts have finally started to produce some (but still limited) taxonomic and biodiversity data from CCZ on various benthic taxa, employing molecular (e.g., Janssen et al. 2015) or morphological approach (e.g., Blake 2016; Kersken et al. 2018, 2019) or a combination of both (e.g., Bonifácio and Menot 2019; Dahlgren et al. 2016; Glover et al. 2016a; Kaiser et al. 2018; Lim et al. 2017; Wiklund et al. 2017; Wiklund et al. 2019).
The lack of knowledge is particularly acute for sediment infauna, a benthic component of the fauna that cannot be captured by video or camera surveys. In general, polychaete worms dominate the abyssal sediment macrofauna, constituting 50–75% of macrofaunal abundance and species richness, and are therefore considered a key component of benthic biodiversity (e.g., Glover et al. 2002; Smith et al. 2008). Polychaetes also exhibit a broad range of feeding types and life-history strategies and are frequently used to evaluate anthropogenic disturbance in shallow-water habitats (Dean 2008). Thus, evaluation of the diversity and species ranges of polychaete worms is critical to predicting and managing the impacts of manganese nodule mining in the CCZ.
Our main objective has been to provide taxonomic and genetic data on macrofaunal polychaetes collected as part of the Abyssal Baseline (ABYSSLINE) environmental survey cruises “AB01” and “AB02” to the polymetallic nodule exploration contract areas “UK-1,” “OMS” as well as an Area of Particular Environmental Interest, “APEI-6.” These data build on previous taxonomic work on polychaete worms from UK-1 area (Wiklund et al. 2019) as well as wider CCZ area (Janssen et al. 2015; Bonifácio and Menot 2019; Blake 2016) and ultimately provide further insights into polychaete species distribution in the deep sea. Up to this date, 43 new polychaete species have been formally described from CCZ, with the focus on families Spionidae (Paterson et al. 2016), Polynoidae (Bonifácio and Menot 2019), Cirratulidae (Blake 2016) and Opheliidae, Scalibregmatidae, and Travisiidae (Wiklund et al. 2019).
Spionidae Grube, 1850 represent one of the most species-rich annelid families with around 590 described species in 39 genera, although many taxa are in need of a revision (Blake et al. 2017). Spionidae are particularly abundant in soft-bottom environment from shallow waters to deep sea and are also commonly found in organically disturbed environments (e.g., Dean 2008). In the deep-sea sediments, Spionidae are well represented both in terms of abundance and species richness (e.g., Glover et al. 2002; Paterson et al. 2011), with species within the two closely related genera Prionospio Malmgren, 1867 and Aurospio Maciolek, 1981 particularly well represented (Paterson et al. 2016; Guggolz et al. 2019, 2020; Peixoto and Paiva 2019, 2020). On the other hand, the family Poecilochaetidae Hannerz, 1956 is rather species poor with 32 valid species confined to the single genus Poecilochaetus Claparède in Ehlers, 1875 and none known from the abyssal depths. Thus, targeting suborder Spioniformia in this study is likely to reveal a sizable and novel portion of benthic biodiversity within the areas samples in the CCZ.
Materials and methods
Fieldwork
The first UKSR ABYSSLINE cruise (AB01) took place in October 2013 onboard the RV Melville and targeted the UK-1 exploration contract area (Fig. 1). The second cruise (AB02) took place in February–March 2015 onboard the RV Thomas G. Thompson and sampled a wider area (Fig. 1), including UK-1 (depth ~4200 m) and OMS (depth ~ 4200 m) exploration contract areas and APEI-6 (depth ~4050 m), an area zoned by the ISA as a potential conservation zone.
Map over sampling sites. a UK-1 Stratum-A and b UK-1 Stratum-B study areas, both within the UK Seabed Resources UK-1 exploration contract area; c OMS Stratum-A study area, in the Ocean Mineral Singapore (OMS) polymetallic nodule exploration contract area; d Area of Particular Interest APEI-6. Inset map showing location of Clarion-Clipperton Fracture Zone. Bathymetric survey and sample localities from the AB01 2013 RV Melville survey cruise and AB02 2015 Thomas G. Thompson survey cruise, data courtesy Craig R. Smith (University of Hawaii), UK Seabed Resources Ltd and Seafloor Investigations, LLC
For a comprehensive description of the methodological pipeline, see Glover et al. (2016b). Briefly, specimens were collected using a range of benthic sampling gear including box corer and epibenthic sledge (EBS) (Brenke 2005). Geographic data from sampling activities were recorded on a central GIS database (Fig. 1). Live-sorting of specimen samples was carried out onboard both vessels in a “cold-chain” pipeline, with material maintained in chilled (2–4°C), filtered seawater. Specimens were assigned preliminarily identification and imaged live using stereo microscopes with attached digital cameras (Glover et al. 2016b). Specimens were then stored in individual microtube vials filled with aqueous solution of 80% non-denatured ethanol labeled appropriately and entered into a database. Samples were kept chilled throughout their transportation to the Natural History Museum, London, UK.
Morphological laboratory work
In the laboratory, preserved specimens were re-examined using stereo and compound microscopes. They were identified to morphospecies and the best-preserved examples (voucher specimens) were then used to provide informal descriptions with key morphological features photographed with digital camera. Shirlastain A was used during the morphological examination on some specimens, in order to better observe certain characters. Scanning electron microscopy (SEM) using a SEM FEI Quanta 650 was conducted on selected specimens, following graded ethanol dehydration, critical point drying, and gold coating. Figures were assembled using Adobe Photoshop CS6 software. In some instances, a fine line was used to outline and highlight particular morphological features where such features were unclear from images alone. Line drawings were made using camera lucida system.
Molecular laboratory work
Extraction of DNA was done with DNeasy Blood and Tissue Kit (Qiagen) using a Hamilton Microlab STAR Robotic Workstation. Approximately 1800 bp of 18S were amplified using the primers 18SA 5′-AYCTGGTTGATCCTGCCAGT-3′ (Medlin et al. 1988) and 18SB 5′-ACCTTGTTACGACTTTTACTTCCTC-3′ (Nygren and Sundberg 2003). Around 450 bp of 16S were amplified with the primers ann16Sf 5′-GCGGTATCCTGACCGTRCWAAGGTA-3′ (Sjölin et al. 2005) and 16SbrH 5′-CCGGTCTGAACTCAGATCACGT-3′ (Palumbi 1996), and around 650 bp of cytochrome c oxidase were amplified using LCO1490 5′-GGTCAACAAATCATAAAGATATTGG-3′ (Folmer et al. 1994) and COI-E 5′-TATACTTCTGGGTGTCCGAAGAATCA-3′ (Bely and Wray 2004). PCR mixtures contained 1 μl of each primer (10 μM), 2 μl template DNA, and 21 μl of Red Taq DNA Polymerase 1.1× MasterMix (VWR) in a mixture of total 25 μl. The PCR amplification profile for all gene fragments consisted of initial denaturation at 95°C for 5 min, 35 cycles of denaturation at 94°C for 45 s, annealing at 55°C for 45 s, extension at 72°C for 2 min, and a final extension at 72°C for 10 min. PCR products were purified using Millipore Multiscreen 96-well PCR Purification System, and sequencing was performed on an ABI 3730XL DNA Analyzer (Applied Biosystems) at The Natural History Museum Sequencing Facility, using the same primers as in the PCR reactions plus two internal primers for 18S, 620F 5′-TAAAGYTGYTGCAGTTAAA-3′ (Nygren and Sundberg 2003) and 1324R 5′-CGGCCATGCACCACC-3′ (Cohen et al. 1998). Overlapping sequence fragments were merged into consensus sequences using Geneious (Kearse et al. 2012) and aligned using MAFFT (Katoh et al. 2002) for 18S and 16S, and MUSCLE (Edgar 2004) for COI, both programs used as plugins in Geneious, with default settings. The program jModelTest (Posada 2008) was used to assess the best model for each partition with BIC, which suggested the MrBayes possible GTR+I+G as the best model for both genes. The data was partitioned into two genes (18S and 16S), and the evolutionary model mentioned above was applied to each partition. The parameters used for the partitions were unlinked. Bayesian phylogenetic analyses (BAs) were conducted with MrBayes ver. 3.2.6 (Ronquist et al. 2012). Analyses were run three times for 10,000,000 generations. Of these, the first 2,500,000 generations were discarded as burn-in. The tree files were interpreted with FigTree ver. 1.4.4 (available from http://tree.bio.ed.ac.uk/software/figtree/). Uncorrected “p” genetic distances within and between closely related species was calculated using Mesquite (Maddison and Maddison 2018).
Taxonomic assignments
Here, we use a phylogenetic species concept sensu Donoghue (1985) with species determined by DNA-based phylogenetic analysis. Poor morphological preservation of some of the collected specimens and the subsequent lack of morphological data hindered formal species descriptions for most species found. For these, we provide the lowest-level taxonomic name possible aided by phylogenetic information. In these cases, we use an informal naming system where the voucher specimen number for one representative individual is used as the informal species name. Therefore, Aurospio sp. (NHM_091) is the informal species name for all specimens that are the same species as the specimen number NHM_091. This avoids confusion with the use of sp. A, sp. B, sp. C etc. where confusing false synonymy can easily arise. Newly formalized species recovered from ABYSSLINE cruises were named in honor of the scientists, technicians, and crew of the two vessels used, with the names being randomly selected from a list of all on board.
Type material, DNA specimen vouchers, and DNA extractions are deposited at the Natural History Museum, London. A full list of all taxa including Natural History Museum Accession Numbers (NHMUK), NHMUK Molecular Collection Facility (NHMUK-MCF), and NCBI GenBank accession numbers is provided in Table 1.
Data handling
The field and laboratory work led to a series of databases and sample sets that were integrated into a “data-management pipeline.”. This included the transfer and management of data and samples between a central collections database, a molecular collections database, and external repositories (GenBank, WoRMS, OBIS, GBIF, GGBN, ZooBank) through DarwinCore (in Supplementary material 1) archives and usage of the GGBN data standard (Droege et al. 2014). This provides a robust data framework to support DNA taxonomy, in which openly available data and voucher material are key to quality data standards. A further elaboration of the data pipeline is published in Glover et al. (2016b).
Systematics section
Spioniformia sensu Fauchald, 1977
Poecilochaetidae Hannerz, 1956
Poecilochaetus Claparède in Ehlers, 1875
Type species: Poecilochaetus fulgoris Claparède in Ehlers, 1875
Diagnosis (modified after Blake and Maciolek 2017). Prostomium small, rounded, two pairs of eyespots; prominent facial tubercle projecting from dorsal lip of mouth; one to three tentaculiform nuchal organs extending posteriorly or nuchal organs reduced to short lobes or knobs. Two long, grooved palps present. First parapodia directed anteriorly, bearing elongated postchaetal lobes, with long chaetae forming cephalic cage. Chaetigers 2 to 3 or 4 or 5 with thick, usually curved spines in neuropodia. Ampullaceous postchaetal lobes present on some anterior parapodia from chaetigers 7 to 10 or 17. Thin, filiform, or branched branchiae on posterior sides of some middle and posterior parapodia or branchiae entirely absent. Simple chaetae of numerous types in middle and posterior parapodia: plumose, hispid, and knobbed with arista either simple or plumose. Last 20 or so parapodia modified, with notopodial spines.
Remarks. The majority of ~30 currently known species of Poecilochaetus have been described from shallow tropical waters, although the type species of the genus, Poecilochaetus fulgoris, is a deep-sea species. It was described from fragments collected by the 1868 Lightning expedition at 1170 m depth in the north-east Atlantic, west of the Faroe Islands (Claparède in Ehlers, 1875). Subsequently collected deep-sea specimens also assigned to P. fulgoris were specimens from 1300 m on the Celtic Slope (Ehlers 1875), and specimens from off New England (1000–5000 m) and north-eastern South America (770–805 m) (Hartman 1965). Later, an additional three species were described from the deep sea: Poecilochaetus bermudensis Hartman, 1965 from 1000 m off Bermuda; hadal Poecilochaetus vitjazi Levenstein, 1962 from Tonga Trench, 10,415–10,687 m; and lastly Poecilochaetus trachyderma Read, 1986 from 477 to 515 m off South Island, New Zealand.
Poecilochaetus fulgoris was poorly defined by Claparède (in Ehlers, 1875) and based on fragmented material. The subsequent re-description by Pilato and Cantone (1976) was based on specimens originally examined by Hartman (1965), without the specifications of their collection locality and perhaps more importantly, collection depth. Given that Hartman (1965) examined specimens collected over vast geographical and bathymetrical ranges, we are cautious of possible misidentifications and as a result also of the definition of P. fulgoris provided by Pilato and Cantone (1976). Therefore, P. fulgoris remains a poorly defined species, which complicates the efforts of describing any new species. Nevertheless, with support from molecular characters, a new species Poecilochaetus brenkei sp. nov. is formalized here from eastern CCZ material, becoming the first species with the type locality in abyssal (rather than bathyal or hadal) depths and only a fifth species described from the deep sea.
Poecilochaetus brenkei sp. nov. http://zoobank.org/0713EA14-6C72-425F-A33B-4F82EE0C73DC
Figs. 2a–h, 3a–e, 4a–f, 5a, 7a–b
Poecilochaetus brenkei sp. nov., holotype NHMUK.ANEA.2021.1 a specimen in dorsal view; b detail of anterior end with prostomium highlighted by line drawing; c postchaetal lobe from chaetiger 1; d neuropodial postchaetal lobe from chaetiger 2; e ampullacaeous postchaetal lobes; f unequal postchaetal lobes in chaetiger 11; g postchaetal lobes from chaetigers 12–16; h postchaetal lobe from chaetiger 30. Scale bars: a 1000 μm; c–h 250 μm
Poecilochaetus brenkei sp. nov., holotype NHMUK.ANEA.2021.1 a neuropodial spines in chaetiger 2-5, the slender spine on chaetiger 5 highlighted by arrow; b detail of spine from chaetiger 2; c detail of spine from chaetiger 3; d detail of spine from chaetiger 4; e detail of spine from chaetiger 5 shown by arrow. Scale bars: 100 μm
Poecilochaetus brenkei sp. nov., holotype NHMUK.ANEA.2021.1, line drawing representing the main types of capillaries a smooth; b hirsute (hairy); c plumose; d spinulose; e mixed hirsute-plumose, f mixed spinulose-plumose. Drawing not to scale
Poecilochaetus brenkei sp. nov., holotype NHMUK.ANEA.2021.1 a chaetae from chaetiger 1, with detail of ornamentation from the long chaetae of chaetiger 1; b example of hirsute chaetae; c bases on capillaries form chaetiger 3 showing a variable development of thickness and ornamentation from smooth to hirsute; d plumose chaeta from chaetiger 35; e mixed chaeta of basally spinose insert e1, distally plumose insert e2 type from chaetiger 35; f spinulose chaeta from chaetiger 35; g example of basally hirsute distally smooth chaeta; h–i mixed chaetae of basally hirsute and distally plumose type from chaetiger 35. Scale bars: a 100 μm; b, c, d, g, h, i 25 μm; e 50 μm
Material examined: holotype NHM_223, NHMUK ANEA.2021.1, coll. 15 Oct. 2013, collection method: Remotely Operated Vehicle, 13°57.7675, 116°33.0556, 4062 m.
Additional material of Poecilochaetus sp. examined: NHM_2526, NHMUK ANEA.2021.2, coll. 03 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°27.26N, 116°36.77W, 4137 m; NHM_1797B, NHMUK ANEA.2021.3, coll. 11 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°10.43N, 117°11.57W, 4045 m; NHM_1668A, NHMUK ANEA.2021.4, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m; NHM_1948A, NHMUK ANEA.2021.5, coll. 13 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°02.49N, 117°13.03W, 4094 m; NHM_2192, NHMUK ANEA.2021.6, coll. 26 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°06.93N, 117°09.87W, 4100 m.
Description (based on holotype, NHMUK ANEA.2021.1). Single specimen, represented by anterior fragment with 30 chaetigers, 7 mm long and 1.5 mm wide. Body, of near uniform width, covered with thin layer of sediment (Fig. 2a), when exposed pale yellow in ethanol.
Prostomium subquadrate anteriorly slightly widened and rounded with a shallow median notch (Fig. 2b). Eyes not observed. Nuchal lobes not observed. Facial tubercle dorsal to mouth, cirriform, short and smooth. Palps not observed. Dorsal chitinous plate on chaetiger 9 not observed. Interramal sensory papilla present, starting from chaetiger 1 and as large as in other anterior chaetigers; smaller from mid-body, distribution in the posterior part of the body uncertain. Branchiae absent. Interramal cirri absent.
Chaetiger 1 large, directed forward; neuropodial postchaetal lobes long, cirriform (Fig. 2c); notopodial postchaetal lobes absent. Postchaetal lobes present in both rami from chaetiger 2 (damaged in some chaetigers). On chaetiger 2 lobes short, robust with thickened base, relatively thick stalk and thickened distally (Fig. 2d); on chaetigers 3–6 resembling lobe of chaetiger 2 but getting progressively longer and more slender, approaching ampullaceous form; on chaetigers 7–11 lobes longest, thinnest, attaining distinct ampullaceous form, with globular base, long thin stalk, terminally enlarged (Fig. 2e). The size of postchaetal lobes on chaetiger 11 of unequal size with ventral lobe much shorter (Fig. 2f). In chaetigers 12 through to 18/19 both lobes short and thick, with distally enlarged tip (Fig. 2g); lobes getting thinner towards chaetigers 18/19. From around chaetiger 20, both lobes are thin, cirriform with base somewhat enlarged (Fig. 2h).
Neuropodial spines in chaetigers 2–5 (Fig. 3a); two spines on chaetigers 2–4 stout, distally curved (Fig. 3b–d); single spine on chaetiger 5 slender, only gently curved (Fig. 3e). Notopodial spines not observed in the posteriorly incomplete specimen. Capillary chaetae of 6 types present (Figs. 4a–f and 5a–i), differentiated by degree of ornamentation sensu Mackie (1990) as smooth (Figs. 4a and 5a), hirsute (Figs. 4b and 5b), plumose (Figs. 4c and 5d), spinose (Figs. 4d and 5f), and of mixed type (Figs. 4e–f and 5c, e, g, h, i); thickness of chaetal stems also variable (Fig. 5c).
Capillaries of chaetiger 1 directed forward in fan-shape arrangement, forming a cephalic cage (Figs. 2a–b and 5a). Notochaetae of chaetiger 1 as 6 long capillaries; stems smooth with some hirsutation along the distal half (Fig. 5a). Neurochaetae of chaetiger 1 all short; lower neurochaetae composed of two thickened hirsute capillaries with ornamentation along most of the length of shaft and three short slender smooth capillaries; upper neurochaetae as two hirsute capillaries, longer with ornamentation limited to distal half. Additionally, 5 very short chaetae present between notopodia and neuropodia of chaetiger 1.
Notochaetae of chaetiger 2 as 7 capillaries—3 long hirsute in distal half, 2 short and 2 long smooth capillaries. Neurochaetae of chaetiger 2 composed of single short lower hirsute capillary, 2 thick curved hirsute spines (Fig. 3a–b) and 2 slightly longer upper hirsute capillaries. Chaetigers 3–4 with similar chaetal arrangement to chaetiger 2, with capillaries longer than in chaetiger 2. Notochaetae of chaetiger 5 as five capillaries; short to long, proximal part of the shaft smooth, distal half hirsute. Neurochaetae of chaetiger 5 composed of single short lower hirsute capillary; single slender, almost straight hirsute spine (Fig. 3a, e); three shorter upper hirsute capillaries. Remaining parapodia composed of capillaries only. Until chaetiger 15 in notopodia and chaetiger 17 in neuropodia, capillaries mainly hirsute or spinose or smooth, differing in length and thickness of the shaft and the degree of ornamentation. Short, slender capillaries have ornamentation along most of the shaft, in longer and thicker capillaries ornamentation restricted to distal halt of the chaeta. Plumose capillaries (Figs. 4c and 5d) appear from chaetiger 15 in notopodia and chaetiger 17 in neuropodia, becoming a prevalent type in the remaining parapodia, although combination of all capillaries continues till end of fragment. Posterior chaetigers and pygidium unknown.
Molecular information. The 16S sequence of P. brenkei sp. nov. matches two sequences from another area (BGR) in the eastern CCZ labeled as Poecilochaetus sp. 18 PB (Bonifácio et al. 2020, GenBank accession numbers MK970939, MK971102). The uncorrected (p) values among the sequences range between 0.0 and 0.017, while the uncorrected (p) distance to two other Poecilochaetus species is 0.24. The COI sequence from the holotype of Poecilochaetus brenkei sp. nov. is similar to five already published sequences on GenBank from another CCZ study labeled as Poecilochaetus sp. NB (Janssen et al. 2015, GenBank accession numbers KJ736555–KJ736559), but differs from these with an uncorrected (p) distance of 0.07. The uncorrected (p) distance among the five published GenBank sequences range from 0.0 to 0.007. In the phylogenetic tree, the new species is basal in a clade of other Poecilochaetus sequences obtained from GenBank, but support for the Poecilochaetus clade is low (Fig. 6). The Poecilochaetus clade falls within Spionidae, although its position within the family is unresolved (Fig. 6).
Phylogenetic analysis of Spioniformia. 50% majority rule tree from the Bayesian analyses using 18S and 16S or CO1, with significant posterior probability values on nodes marked by asterisks. Sixty-five taxa from GenBank were included (clades of the genera Spio, Pygospio and Rhynchospio collapsed) with Cirratulidae as outgroup
Remarks. Six ABYSSLINE specimens assigned to the genus Poecilochaetus were examined for their morphology (Figs. 7a–h and 8a–b). The 16S molecular data showed only limited variation (see “Molecular information” section above) suggesting that specimens belong to the same species, while morphological investigation showed variation in size, color/sediment covering of body, shape of prostomium, and development of parapodial lobes on chaetiger 11 (Fig. 7a–h). If these differences should be considered of inter- or intra-specific variability remains unresolved. In the case of paucity of morphological data, the evidence from more variable genes such as COI could provide further insight, but such data are currently unavailable for some of the specimens. Chaetae, a very diverse and important character in Poecilochaetus (Mackie 1990, Santos and Mackie 2008), need to be observed in great detail, throughout the series of parapodial transections, leading to the destruction of the few fragile specimens available for this study, particularly as SEM observations may be necessary to fully understand the chaetal morphology. Additionally, some chaetae, such as notopodial spines, are limited to the posterior region only (if at all present) in Poecilochaetus and all ABYSSLINE specimens are posteriorly incomplete.
Images of preserved specimens of Poecilochaetus specimens examined from the ABYSSLINE collection, all specimens in dorsal view a holotype (NHMUK.ANEA.2021.1) of Poecilochaetus brenkei sp. nov.; b anterior end of holotype (NHMUK.ANEA.2021.1) of Poecilochaetus brenkei sp. nov., with line drawing of prostomium; c Poecilochaetus sp., specimen NHMUK.ANEA.2021.6; d Poecilochaetus sp., anterior end of specimen NHMUK.ANEA.2021.6, with line drawing of prostomium; e Poecilochaetus sp., specimen NHMUK.ANEA.2021.2; f Poecilochaetus sp., specimen NHMUK.ANEA.2021.5; g Poecilochaetus sp., specimen NHMUK.ANEA.2021.4; h Poecilochaetus sp., specimen NHMUK.ANEA.2021.3. Scale bars: 1000 μm
Poecilochaetus specimen NHMUK.ANEA.2021.5 a stereomicroscopy image, specimen in dorsal view; b SEM micrograph, anterior end with detail of prostomium. Scale bar: (a) 1000 μm
Interestingly, all ABYSSLINE Poecilochaetus specimens share one important character, which sets them apart from all known Poecilochaetus species, the presence of spines in neuropodia of chaetigers 2–5 (Figs. 3a–e and 9a, c, d), while all known species have such distribution confined to chaetigers 2–3 or 2–4, although the spine in chaetiger 5 differs in morphology to those from chaetigers 2–4 by being slenderer and straighter rather than robust and curved. However, as mentioned above, some morphological differences were observed, and having only 16S sequences available for species delimitation we currently cannot determine with certainty if more than one species sharing the same spinal character are present in our samples. In order to avoid future taxonomic confusion, we prefer to base the formal description solely on specimen NHMUK ANEA.2021.1 (holotype of P. brenkei sp. nov.), for which both 16S and COI data are available. The rest of the material is discussed in this section as Poecilochaetus sp.
Poecilochaetus sp. (specimen NHM_2192) is morphologically most aberrant as it is much bigger than the others (Fig. 7c, d). Thus, the observed morphological differences may be related to its size, given that this specimen shares the main character of P. brenkei sp. nov., the presence of spines in chaetigers 2–5. However, it also differs in the form of prostomium (Fig. 7d) and the size of lobes on chaetiger 11, which are equal, not unequal as in other specimens.
Poecilochaetus sp. (specimen NHM_1948A) differs from all other specimens in not being covered by sediment and being white (Fig. 7f). This specimen was also imaged using SEM (Fig. 8a–b) and confirmed the presence of neuropodial spines in chaetigers 2–5 (Fig. 9c–d).
Examples of neuropodial spines from Poecilochaetus sp. found in ABYSSLINE samples, unless stated otherwise a sequence of neuropodial spines from chaetigers 2–4 (spine on chaetiger 5 broken off, not imaged) of Poecilochaetus sp., specimen NHMUK.ANEA.2021.6; b neuropodial spine characteristic of chaetigers 2–4 of Poecilochaetus fulgoris (after Claparéde in Ehlers, 1875); c sequence of neuropodial spines from chaetigers 2–5 of Poecilochaetus sp., specimen NHMUK.ANEA.2021.5; d SEM micrograph of sequence of neuropodial spines from chaetigers 2–5 of Poecilochaetus sp., specimen NHMUK.ANEA.2021.5. Scale bars: a 100 μm; c 25 μm; d 50 μm
Poecilochaetus sp. (specimens NHM_2526, NHM_1668A, and NHM_1797B) are most similar to P. brenkei sp. nov. morphologically (Fig. 7e, g, h) in terms of size, sediment coverage, prostomium shape, and the length of the lobes. The presence of neuropodial spines has also been confirmed. However, all anterior fragments are less than 15 chaetigers long and often too damaged for a meaningful comparison with specimen NHMUK.ANEA.2021.1, assigned to P. brenkei sp. nov.
Of the known species Poecilochaetus brenkei sp. nov. is closest in morphology to bathyal P. fulgoris, a poorly known species described from a single fragmented specimen (see also earlier Remarks under genus Poecilochaetus). The new species differs from P. fulgoris in the distribution of anterior neurochaetal spines found in chaetiger 2–5 rather than 2–4 as well as the form of spines, which are more strongly hooked in P. fulgoris (Fig. 9b).
Distribution. Poecilochaetus brenkei sp. nov. has been found in the UK-1 area in the eastern CCZ. Other specimens assigned to Poecilochaetus sp. were found in the UK-1 area and OMS area in the eastern CCZ. Barcode data indicate that the species occur in additional exploration contract areas in the eastern CCZ.
Etymology. This species is named for Nils Brenke, who was responsible for deploying and recovering the epibenthic sledge on the first cruise (AB01) (see also Brenke 2005).
Spionidae Grube, 1850
Spionidae sp. NHM_017
Fig. 10a–d
Spionidae sp. NHM_017, specimen NHMUK.ANEA.2021.7 a fragmented preserved specimen with body segments (left) and anterior fragment with prostomium in dorsal view (right); b fascicle of neuropodial hooded hooks from body fragment, with secondary hood marked by arrow; c details of neuropodial hooded hooks; d slender neuropodial sabre chaeta. Scale bars: a 1000 μm; b, d 25 μm
Material examined: NHM_017, NHMUK ANEA.2021.7, coll. 9 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°50.232N, 116°33.506W, 4336 m.
Description: Single poorly preserved specimen, small and slender; now in two fragments—anterior fragment with 8 discernible chaetigers, 0.9 mm long and 0.25 mm wide and body fragment with about 7 discernible chaetigers. Color in alcohol pale yellow, without distinct pigmentation (Fig. 10a).
Prostomium anteriorly rounded, longer than wide, extending into blunt caruncle to beginning of chaetiger 2, without peaks. Eyes absent. Peristomium as narrow hood around prostomium, not forming lateral wings; dorsally not fused. Palps missing.
Parapodial lamellae and branchiae not observed, either missing or damaged.
Chaetae of three types: capillaries, hooded hooks (Fig. 10b, c) and slender sabre chaetae (Fig. 10d). Eight chaetiger long anterior fragment with capillaries only. Long, limbate and rather slender sabre chaetae observed in neuropodia of body fragment; granulation not detected. Multidentate hooded hooks observed in neuropodia of body fragment; up to 6 per fascicle. Hooded hooks long and slender, with several small teeth above the main fang as observed under light microscopy (Fig. 10b, c); with inflated, rounded, anteriorly somewhat truncated hood and rudimentary secondary hood (Fig. 10b). Notopodial hooded hooks not observed in available fragments. The rest of body and pygidium unknown.
Molecular information: The 16S sequence from this species does not match any sequences published on GenBank. In the phylogenetic tree (Fig. 6), this species falls in a low-support clade of mainly undescribed species assigned to Aurospio (including three morphospecies from this study) and Prionospio, and three known species—Aurospio foodbancsia Mincks, Dyal, Paterson, Smith & Glover, 2009 (in Mincks et al., 2009); Prionospio dubia Day, 1961; and Paraprionospio patients Yokoyama, 2007.
Remarks: The available fragment is in particularly poor morphological condition and cannot be morphologically compared with other species. Form of prostomium and the form and distribution of neuropodial hooded hooks suggest that this species may belong to Prionospio–Aurospio complex.
Distribution: This species is only known from UK-1 exploration area in the eastern CCZ.
Spionidae sp. NHM_564
Material examined: NHM_564, NHMUK ANEA.2019.10013, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_1507, NHMUK ANEA.2021.43, coll. 04 Mar. 2015, collection method: USNEL Box Core, 12°27.107N, 116°30.736W, 4196 m.
Description: Small, slender species represented by two very poorly preserved anterior fragments, consisting of anterior fragment with damaged prostomium and about 10 discernable damaged chaetigers; both fragments less than 1 mm in length.
Molecular data. The two 16S sequences from this species matches one sequence from another study labeled as Spionidae sp. 159-Ifr-0510 (Bonifácio et al. 2020, GenBank accession number MK970921), the uncorrected (p) distances among the three sequences are 0.0, extending this species distribution to the Ifremer exploration contract area in the eastern CCZ. This species falls into a well-supported clade of Prionospio, Aurospio, and Paraprionospio species (Fig. 6).
Remarks. Image of live specimen NHM_564 (Fig. 11) shows a relatively well-preserved about 20 chaetiger long anterior fragment. However, only limited morphological details of taxonomic value can be observed from this image and the current state of both specimens renders them of no value for morphological observations. Therefore, this species is represented best by its molecular data.
Live image of Spionidae sp. NHM_564, specimen NHMUK.ANEA.2019.10013
Distribution: This species is known from UK-1 and Ifremer exploration contract areas in the eastern CCZ.
Spionidae sp. NHM_1415
Fig. 12a–c
Spionidae sp. NHM_1415, specimen NHMUK.ANEA.2019.10039 a preserved specimen in dorso-lateral view; b neuropodial hooded hooks from chaetiger 18; c neuropodial sabre chaeta from chaetiger 15. Scale bars: a 1 mm; b 25 μm; c 50 μm
Material examined: NHM_520, NHMUK ANEA.2021.53, coll. 16 Feb. 2015, collection method: USNEL Box Core, 12°24.977N, 116°42.891W, 4127 m; NHM_1544, NHMUK ANEA.2019.10040, coll. 06 Mar. 2015, collection method: USNEL Box Core, 12°30.382N, 116°29.073W, 4244 m; NHM_1025C, NHMUK ANEA.2019.10029, coll. 24 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°08.02N, 117°17.52W, 4122 m; NHM_1415, NHMUK ANEA.2019.10039, coll. 02 Mar. 2015, collection method: USNEL Box Core, 12°27.066N, 116°35.661W, 4130 m.
Description: Small, slender species represented by four poorly preserved, posteriorly incomplete specimens. The best example, specimen NHM_1415, consisting of an anterior fragment with about 13 discernable chaetigers, 2.3 mm long and 0.25 mm wide and body fragment with about 10 chaetigers (Fig. 12a). Color in alcohol pale yellow.
Prostomium and peristomium not clearly observed. Parapodia mostly damaged or missing. Branchiae not observed, assumed missing.
Chaetae of three types: capillaries, hooded hooks (Fig. 12b), and sabre chaetae (Fig. 12c). The exact start of sabre chaetae and neuropodial hooded hooks unknown, first sabre chaeta observed in neuropodia of ca. chaetiger 15, first neuropodial hooks observed in neuropodia of ca. chaetiger 18. Sabre chaeta stout, curved, limbate. Hooded hooks, up to 5 per fascicle; long and slender, with large, blunt main fang and about 3 small teeth, observed under light microscopy (Fig. 12b); with rounded hood, secondary hood not observed (Fig. 12b). Notopodial hooded hooks not observed in available fragments. The rest of body and pygidium unknown.
Molecular information: The three 16S sequences from this species does not match any other sequences from the CCZ, the uncorrected (p) distances among the three sequences range from 0.002 to 0.009. In the phylogenetic tree (Fig. 6) this species falls into a clade containing Prionospio, Aurospio, and Paraprionospio species.
Remarks: This poorly preserved species cannot be morphologically compared with other species and is therefore best represented by the molecular data.
Distribution: This species is only known from UK-1 claim area in the eastern CCZ and OMS-1 area.
Spionidae sp. NHM_2123
Fig. 13a, b
Preserved specimen NHMUK.ANEA.2021.45 of Spionidae sp. NHM_2123 a specimen in dorsolateral view; b anterior end in dorsal view. Scale bar: 1 mm
Material examined: NHM_2123, NHMUK ANEA.2021.45, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m.
Description: Poorly preserved single specimen represented by anterior fragment consisting of ca. 20 discernible chaetigers, 3.2 mm long and 1.9 mm wide at the widest part. Body very broad and dorsoventrally flattened anteriorly (Fig. 13a, b), color in ethanol pale yellow, anterior half of prostomium with distinct reddish pigmentation (Fig. 13b). Prostomium narrow, oval, with rounded anterior margin and posteriorly narrowing into caruncle. Pair of short, thick, grooved palps attached (Fig. 13b). Branchiae mostly missing or damaged. Only capillary chaetae observed in available fragment.
Molecular information: The COI and 16S sequences from this species do not match any other sequences from the CCZ. In the combined 18S and 16S tree (Fig. 6), it sits basally to a clade with several spionid genera, with no affiliation to any specific genus.
Remarks: Specimen is too poorly preserved for further identification or comparison. Within the ABYSSLINE spionid collection, this species can be morphologically distinguished by its very broad and flattened body.
Distribution: This species is only known from APEI-6, an area preliminary designated as a preservation area.
Spionidae sp. NHM_2180
Fig. 14
Spionidae sp. NHM_2180, preserved specimen NHMUK.ANEA.2021.8 in dorsal view. Scale bar: 500 μm.
Material examined: NHM_2180, NHMUK ANEA.2021.8, coll. 21 Mar. 2015, collection method: USNEL Box Core, 19 27.998N, 120 00.172W, 4141 m.
Description: Single poorly preserved specimen, small and slender, 1.6 mm long and 0.25 mm wide, anterior fragment with about 13 discernable chaetigers. Color in alcohol pale yellow, with faint gold-brown pigmentation around caruncle (Fig. 14a). Prostomium anteriorly rounded, longer than wide, extending into blunt caruncle to beginning of chaetiger 2, without peaks. Eyes absent. Peristomium as narrow hood around prostomium, not forming lateral wings; dorsally not fused. Palps missing. Parapodial lamellae often damaged or missing, all lamellae relatively small, but large subtriangular notopodial lamellae observed on chaetiger 3. Anterior neuropodial lamellae rounded, largest on chaetiger 3. Only capillary chaetae observed in the available fragment, chaetae particularly long in chaetiger 3. Multidentate hooded hooks in notopodia or neuropodia and sabre chaetae not observed in the available fragment. The rest of body and pygidium unknown.
Molecular information: The COI and 16S sequences from this species do not match anything published on GenBank. This species falls into a well-supported clade of Prionospio, Aurospio, and Paraprionospio species (Fig. 6).
Remarks: The available fragment is in particularly poor morphological condition and cannot be meaningfully compared with other species.
Distribution: This species is only known from APEI-6.
Aurospio Maciolek, 1981
Type species: Aurospio dibranchiata Maciolek, 1981
Definition: Small and slender body. Prostomium anteriorly rounded, occipital antenna absent. Branchiae starting from chaetiger 3, small, maybe fused or free from notopodial lamellae or entirely absent. Neuropodial hooded hooks and sabre chaetae present.
Remarks: Definitions of Aurospio and closely related genus Prionospio are problematic and a matter of debate (e.g., Sigvaldadóttir 2002; Mincks et al. 2009; Paterson et al. 2016; Blake et al. 2017; Peixoto and Paiva 2019). It is generally agreed upon that the taxonomic reliance on number, form, and distribution of branchiae is problematic, particularly given the recent discoveries of abranchiate species (Paterson et al. 2016, Peixoto and Paiva 2019). While the initial definition of Aurospio by Maciolek (1981) is too restrictive (almost equaling the specific definition), subsequent authors expanded the definition to include species in which branchiae start from chaetiger 3 instead of 2 as in Prionospio (Sigvaldadóttir 2002; Mincks et al. 2009; Paterson et al. 2016) or display the ultimate branchial reduction by becoming abranchiate, but with large quadrate notopodial lamellae (Paterson et al. 2016). The most recent attempt at distinguishing Aurospio and Prionospio has been made by Blake et al. (2017), followed by Peixoto and Paiva (2019) who considered the fusion of branchiae to notopodial lamellae, the start of branchiae form chaetiger 3 and the absence of secondary hood in the hooks to be the defining characters of Aurospio. Currently there are six valid species of Aurospio, although Blake et al. (2017) argue that the genus is monotypic with Aurospio dibranchiata, its type species, the only valid species. Finally, the genetic data available so far suggest that there is no distinction between Aurospio and Prionospio (Fig. 6 this study; Guggolz et al. 2020), but currently no molecular data are available from the type localities, preventing firm conclusions.
Aurospio dibranchiata, the type species of genus Aurospio, is an often-reported deep-sea species. Although Maciolek (1981) designated the type specimens from Argentine Basin, SW Atlantic, depth range ca. 1600–2000 m, she considered the range of this species based on all material examined to be very large both geographically (pan-Atlantic) and bathymetrically (300–3600 m). Since the original publication this species has also been reported from the abyssal Pacific (e.g., Mincks et al. 2009) and Southern Oceans (e.g., Neal et al. 2018a). However, as our current (Fig. 6) and previously published (Neal et al. 2018b; Guggolz et al. 2020) molecular data suggest, the specimens identified as A. dibranchiata in fact represent genetically distinct species. Three of those species, Aurospio sp. NHM_091, Aurospio sp. NHM_2186, and Aurospio sp. NHM_2247, were collected from CCZ during ABYSSLINE cruises and will be further described in this publication.
Maciolek (1981) noted a remarkable consistency of taxonomic characters in A. dibranchiata over its wide geographic and bathymetric range. However, at the same time Maciolek (1981) reported some morphological variations, which were interpreted as within species, regional or preservation-related differences: the presence/absence of tiny prostomial peaks, the strength of pigmentation in the peristomium/first chaetiger, the variability in the start of neuropodial hooks over chaetigers 9–11, and the presence/absence of dorsal crests. While Maciolek (1981) elected the type specimens (those collected from Argentine Basin, SW Atlantic, depth range ca. 1600–2000 m), it appears that the original description is based on a collection of observations from all specimens in the material examined section, which may in fact belong to different species (for example, some specimens with 3 pairs of branchiae were considered an aberrant form of A. dibranchiata). This is further supported by our re-examination of A. dibranchiata paratypes (BMNHUK.1981.82-91) deposited at NHMUK London (see details below) as part of this study. Therefore, until A. dibranchiata is re-defined more restrictively with molecular data from the type locality, the recognition and subsequent description of new species will be problematic (see also discussion in Paterson et al. 2016; Peixoto and Paiva 2019).
Having examined the newly collected CCZ material and Maciolek’s paratypes (BMNH.1981.82-91), we investigated if variations reported by Maciolek (1981) as well as additionally observed characters could be considered of inter-specific importance. Based on our observations, the following characters were found to be variable within genetically defined species (comparative Fig. 15a–d) to the same degree as between genetically defined species (comparative Figs. 16a–d and 17a–d) and therefore cannot be considered as taxonomically informative. Prostomium shape, while generally best described as tear-shaped, differs in broadness and the abruptness of the narrowing into caruncle (Figs. 15a–d and 16a–d). Branchial size, although branchiae are always fused to notopodial lamellae and short (never longer than the corresponding notopodial lamellae), their size and the degree of fusion with the lamella can differ (Figs. 15a–d and 17a–d). The shape and size of parapodial lamellae are considered taxonomically informative in closely related genus Prionospio (e.g., Sigvaldadóttir 1998; Paterson et al. 2016; Peixoto and Paiva 2019), but the observations so far have proved problematic in A. dibranchiata as the size and shape of lamellae can vary (Figs. 15a–d and, 17a–d), sometimes even the left and right lamellae of the same chaetiger can differ (Neal pers. obs.). The presence/absence and development of dorsal crests also appear to be variable.
Aurospio sp. NHM_091 (aff. dibranchiata). Line drawings of sequences (top to bottom) of intraspecific variation in prostomial shapes and notopodial lamellae (ntl) from chaetigers (ch) 3–5, drawings omitted where no clear observation was possible a sequence of specimen NHMUK.ANEA.2019.10001 (prostomium omitted, too damaged): ntl from ch 3, ntl from ch 4, ntl from ch 5; b sequence of specimen NHMUK.ANEA.2019.10036: prostomium, ntl from ch 3, ntl from ch 4, ntl from ch 5; c prostomium of specimen NHMUK. ANEA.2019.10038, all ntl omitted; d sequence of specimen NHMUK.ANEA.2019.10049: prostomium, ntl from ch 3, ntl from ch 4, ntl from ch 5 omitted (not observed)
Interspecific variation in prostomial shapes of ABYSSLINE Aurospio dibranchiata-like species presented as line drawings (top row) and stereomicroscopy images, all specimens stained with Shirlastain (bottom row) a ABYSSLINE species Aurospio sp. NHM_ 91, specimen NHMUK. ANEA.2019.10036; b ABYSSLINE species Aurospio sp. NHM_2186, specimen NHMUK. ANEA.2019.10052; c ABYSSLINE species Aurospio sp. NHM_2247, specimen NHMUK.ANEA.2021.9; d Aurospio dibranchiata, one of paratypes BMNH.1981.82-91
Interspecific variation in shapes of notopodial branchiae carrying lamellae of ABYSSLINE-collected Aurospio dibranchiata-like species presented as line drawings—chaetiger 3 (top row) and chaetiger 4 (bottom row) a ABYSSLINE species Aurospio sp. 91, specimen NHMUK.ANEA.2019.10036; b ABYSSLINE species Aurospio sp. NHM_2186, specimen NHMUK. ANEA.2019.10052; c ABYSSLINE species Aurospio sp. NHMUK_2247, specimen NHMUK.ANEA.2021.9; d Aurospio dibranchiata, one of paratypes BMNH.1981.82-91, chaetiger 3 only
No differences were observed in the distribution of neuropodial hooks (Fig. 18a–c) from Maciolek paratypes and these hooks were consistently found from chaetiger 10, a most commonly reported chaetiger by Maciolek (1981). However, the secondary hood of the hooks, which absence of was considered a genus-level character by Maciolek (1981) (Fig. 18b) and recently by Blake et al. (2017) and Peixoto and Paiva (2019), has been detected in the re-examined paratypes (BMNH. 1981.82-91) (Fig. 18c). Such observation suggests that this character was either previously overlooked or that it is variable, possibly strengthening our hypothesis that several species were in fact present in the material ascribed by Maciolek (1981) to A. dibranchiata. It certainly shows that it cannot be used to define the genus Aurospio as suggested by Blake et al. (2017), further complicating the question: What is Aurospio?
Comparison of neuropodial hooded hooks a neuropodial hooded hooks and sabre chaeta from Aurospio sp. NHM_091, specimen NHMUK.ANEA.2019.10001; b drawing of neuropodial hooded hook of Aurospio dibranchiata (after Maciolek 1981), secondary hood absent; c hooks from paratypes of Aurospio dibranchiata BMNH.1981.82-91, with secondary hood present (arrow). Scale bars: a, c 25 μm
One character that may warrant further investigation is the development of peristomium, which can dorsally form a tight narrow hood (UKSR-1 specimens, Fig. 16a–c, lower row) or flare into lateral wings (Fig. 16d, lower row) as observed in some (but not all) Maciolek’s paratypes (BMNH.1981.82-91). The development of lateral wings in peristomium was neither reported, nor pictured by Maciolek (1981), although observed in this study of type material (Fig. 16d, lower row), further suggesting that the original description of A. dibranchiata may be problematic.
In the ABYSSLINE-collected material, three species similar to Aurospio dibranchiata in having tear-shaped prostomium and small branchiae fused to notopodial lamellae of chaetigers 3 and 4 were found. Further two species are assigned to genus Aurospio based on molecular and/or morphological similarity to Aurospio foodbancsia Mincks et al. (2009).
Aurospio sp. NHM_091
Figs. 15a–d, 16a, 17a, 18a, 19a–d, 20a–d, 22c–d
Selected examples of four specimens genetically identified as Aurospio sp. NHM_091 a live specimen NHMUK.ANEA.2019.10045 in dorsolateral view; b preserved specimen NHMUK.ANEA.2019.10036 in dorsal view; c preserved specimen NHMUK.ANEA.2019.10049 in dorsolateral view; d anterior end with prostomium of preserved specimen NHMUK.ANEA.2019.10038 in dorsal view. Scale bar: c 1000 μm
Intraspecific variation in prostomial shapes and parapodial lamellae in Aurospio sp. NHM_091, all specimens stained with Shirlastain a specimen NHMUK. ANEA.2019.10001 in dorsal view (prostomium not clearly visible); b specimen NHMUK.ANEA.2019.10036 in dorsal view; c specimen NHMUK.ANEA.2019.10038 in dorsal view; d specimen NHMUK.ANEA.2019.10049 in dorso-lateral view
Material examined: NHM_091, NHMUK ANEA.2019.10001, coll. 10 Oct. 2013, collection method: Multi Corer, 13°50.792N, 116°37.590W, 4079 m; NHM_323, NHMUK ANEA.2019.10010, coll. 18 Oct. 2013, collection method: USNEL Box Core, 13°45.001N, 116°30.799W, 4036 m; NHM_322, NHMUK ANEA.2019.10009, coll. 18 Oct. 2013, collection method: USNEL Box Core, 13°45.001N, 116°30.799W, 4036 m;
NHM_134, NHMUK ANEA.2019.10002, coll. 11 Oct. 2013, collection method: Brenke Epibenthic Sledge 02, 13°45.500N, 116°41.911W, 4080 m; NHM_957C, NHMUK ANEA.2019.10026, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m; NHM_1668C, NHMUK ANEA.2019.10044, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m;
NHM_1768, NHMUK ANEA.2019.10045, coll. 11 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°10.43N, 117°11.57W, 4045 m; NHM_1025A, NHMUK ANEA.2019.10028, coll. 24 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°08.02N, 117°17.52W, 4122 m; NHM_1351D, NHMUK ANEA.2019.10036, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m;
NHM_1797J, NHMUK ANEA.2019.10047, coll. 11 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°10.43N, 117°11.57W, 4045 m; NHM_1347G, NHMUK ANEA.2019.10035, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m; NHM_1351F, NHMUK ANEA.2019.10037, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m; NHM_1390A, NHMUK ANEA.2019.10038, coll. 02 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°08.695N, 117°19.526W, 4044 m; NHM_2020, NHMUK ANEA.2019.10049, coll. 16 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°03.03N, 117°24.28W, 4235 m; NHM_2151, NHMUK ANEA.2019.10050, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m; NHM_2152, NHMUK ANEA.2019.10051, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m; NHM_176, NHMUK ANEA.2019.10004, coll. 13 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°56.089N, 116°33.011W, 4082 m.
Description (based on specimens NHM_091, NHM_1390A, NHM_2020 and NHM_1351D [SEM specimen]) (Fig. 19a–d). Small slender species represented by 17 posteriorly incomplete specimens, measuring up to 2.8 mm long and up to 0.4 mm wide for max. of 15 discernible chaetigers (specimen NHM_091 composed of three fragments: anterior fragment with 12 chaetigers and two body fragments of 8 and 10 chaetigers, respectively). Live specimens tanned with distinct orange gut from around chaetiger 10 (Fig. 20a); the color in alcohol pale yellow to tanned (Fig. 20b, c), with reddish pigmentation concentrated near the anterior margin of prostomium and peristomium (best observed in specimen NHM_1390A (Fig. 20d), now blueish due to retention of Shirlastain, but pigmentation still visible).
Prostomium rounded, widest medially, broadly rounded anteriorly, posteriorly narrowing into caruncle to the end of chaetiger 1, with some variability observed to overall width, abruptness of narrowing into caruncle and robustness of caruncle (Figs. 15b–d and 20a–d). Eyes not observed. Peristomium forms a narrow hood around prostomium, not forming lateral wings. Palps missing. Pharynx an eversible soft pouch (Fig. 20b).
Branchiae present on chaetigers 3–4 only; both short, smooth, cirriform and basally fused to the corresponding notopodial lamellae (Figs. 15a, b, d and 20a, b, d). Branchiae on chaetiger 3 longer, approaching the length of corresponding notopodial lamellae; branchiae on chaetiger 4 short, stubby, reaching max. 2/3 length of corresponding notopodial lamellae. Cilia not observed.
Parapodial lamellae morphologically plastic, particularly in anterior chaetigers in size and shape (see comparative Fig. 15a, b, d and Fig. 20a–d). In specimens NHM_091 and NHM_1351D anterior notopodial lamellae large, almost covering dorsum (Fig. 20a, b), in specimens NHM_1390A and NHM_2020 small, with dorsum well exposed (Fig. 20c, d). As a general trend, notopodium of chaetiger l reduced to a small rounded lamella. Notopodial lamellae best developed on chaetigers 2–4 (to chaetiger 7 in specimen NHM_091), with those on chaetiger 3 largest and those on chaetigers 2 and 4 (or 4–7) smaller of similar size (Fig. 20a). Notopodial lamellae on chaetiger 2 subquadrate to broadly rounded (Fig. 20a). Notopodial lamellae on chaetiger 3 broad and foliaceous, with the medial edge prolonged over the dorsum, tip blunt or pronounced (Fig. 15a, b, d and Fig. 20a). Notopodial lamellae on chaetiger 4 broad to subquadrate with short blunt tip (Fig. 15a, b, d and Fig. 20a). Neuropodium of chaetiger l reduced to a small rounded lamella. On chaetiger 2, it is a small auricular lobe which becomes larger on chaetiger 3 and then again smaller on chaetiger 4. In general, from chaetiger 5, both noto- and neuropodial lamellae as broadly rounded lobes, getting progressively smaller and lower, with notolamellae being larger in anterior chaetigers (Fig. 20a). Dorsal crests not consistently detected, at best appearing low from chaetiger 5 or 6 but integument often damaged to some degree. Form of parapodia not established past chaetiger 15 (end of the longest fragment).
Chaetae consist of 3 types: capillaries, ventral sabre chaetae (Fig. 18a), and multidentate hooded hooks (Figs. 18a and 22c–d). Anterior chaetae arranged in 2 rows of longer and shorter limbate capillaries; chaetae particularly long in neuropodia of chaetiger 2. A single heavily granulated and ventral sabre chaeta present from chaetiger 10 (Fig. 18a). Neuropodial hooded hooks first observed in chaetiger 10, with six hooks per fascicle accompanied by two capillaries (in body segments of specimen NHM_091 up to 12 hooks per fascicle observed). Neuropodial hooks with squarish primary hood, secondary hood not observed; with four slender teeth of unequal size in lateral view (Figs. 18a and 22c–d). Notopodial hooks not observed in available fragments. Mid to posterior chaetigers and pygidium not observed.
Molecular information. Seventeen 16S sequences obtained for Aurospio sp. NHM_091 form a well-supported clade (Fig. 6). The 16S sequences from specimens within this species match 15 sequences of Aurospio sp. ‘20 PB’ reported from other areas (GSR, Ifremer and IOM) in the eastern CCZ (Bonifácio et al. 2020). The uncorrected (p) values among all 32 sequences range between 0.0 and 0.01, while the lowest uncorrected (p) distance considered inter-specific (with Aurospio sp. NHM_2247 being the closest species) is 0.08.
Remarks. Aurospio sp. NHM_091 is the first of three CCZ collected species so far that correspond well to Aurospio dibranchiata based on following characters, the shape of prostomium, two pairs of small branchiae partially fused to notopodial lamellae of chaetigers 3 and 4 and neuropodial hooded hooks from chaetiger 10.
Differentiation of commonly encountered species similar to Aurospio dibranchiata is important in order not to overestimate the range of A. dibranchiata by lumping similar species together. This information is in turn crucial to the future conservation efforts. However, as already discussed earlier, the problematic definition of A. dibranchiata makes comparisons difficult. Such effort is further compounded by the lack of molecular data from the type locality, the plasticity of certain characters as observed in this study and paucity of well-preserved material from the CCZ and deep sea in general. Therefore, we assign these specimens to morphospecies only and identify it primarily by molecular data (Fig. 6). Two other morphologically similar but genetically distinct species have been found in ABYSSLINE samples (see Remarks under Aurospio sp. NHM_2186 and Aurospio sp. NHM_2247).
Distribution. Molecular evidence based on 16S suggests that Aurospio sp. NHM_091 is a widely distributed species within the eastern CCZ as it was found in the UKSR-1, OMS-1, GSR, Ifremer, and IOM exploration areas and APEI-6 region.
Aurospio sp. NHM_2186
Aurospio sp. NHM_2186 a live; and b preserved body fragments genetically identified as Aurospio sp. NHM_2186; c anterior end in dorsal view, specimen NHMUK. ANEA.2019.10052 stained with Shirlastain; d dorsolateral view of anterior parapodial lamellae, specimen stained with Shirlastain; e neuropodial hooded hooks; f close-up of neuropodial hooded hook. Images g–k all line drawings of specimen NHMUK. ANEA.2019.10052 (g) prostomium; h notopodial lamella from chaetiger 2; i notopodial lamella from chaetiger 3; j notopodial lamellae from chaetiger 4, left (L.H.) and right-hand side (R.H.); k notopodial lamella from chaetiger 5. Scale bars: a 500 μm; e 25 μm
Comparison of neuropodial hooded hooks (from chaetiger 10–11) of ABBYSLINE-collected Aurospio dibranchiata-like species as seen under light microscopy a line drawing of Aurospio dibranchiata with quadridentate hooks, without secondary hood after Maciolek (1981); b hooks from paratypes of Aurospio dibranchiata BMNH.1981.82-91, with secondary hood (arrow); c-d ABYSSLINE species Aurospio sp. NHM_091 with quadridentate hooks, without discernible secondary hood; e–f ABYSSLINE species Aurospio sp. NHM_2186 with tridentate hooks, with secondary hood (marked by arrow); g–h ABYSSLINE species Aurospio sp. NHM_2247, hooks dentition not clearly observed, secondary hood may be present. Scale bar: 25 μm
Material examined: NHM_513, NHMUK ANEA.2019.10012, coll. 16 Feb. 2015, collection method: USNEL Box Core, 12°24.977N, 116°42.891W, 4127 m; NHM_2186, NHMUK ANEA.2019.10052, coll. 22 Mar. 2015, collection method: USNEL Box Core, 19 28.342N, 120 11.495W, 4115 m.
Description. Small slender species represented by a posteriorly incomplete specimen (NHM_2186), now split into anterior fragment 1.3 mm long and 0.3 mm wide for 10 discernible chaetigers and about 7 discernible chaetigers long body fragment; in addition, another example (NHM_513) represented by around 10 discernible chaetigers long body fragment was observed. Live example observed as tanned body fragment with distinct orange gut (Fig. 21a), the color in alcohol pale yellow (Fig. 21b), pigmentation not observed.
Prostomium rounded, widest medially, broadly rounded anteriorly, posteriorly narrowing into slender caruncle to the end of chaetiger 1 (Figs. 16b and 21c, g). Two pairs of well separated tiny red eyes observed. Peristomium forms a narrow hood around prostomium, not forming lateral wings. Palps missing. Pharynx an eversible soft pouch.
Branchiae present on chaetigers 3–4 only; both short, smooth, cirriform and basally fused to the corresponding notopodial lamellae (Figs. 17b and 21i–j). Branchiae on chaetiger 3 longer, approaching the length of corresponding notopodial lamellae; branchiae on chaetiger 4 short, slender, reaching about 1/2 length of corresponding notopodial lamellae. Cilia not observed. Notopodium of chaetiger l rudimentary. Notopodial lamellae best developed on chaetigers 2–5 (Fig. 21d, h–k), with those on chaetiger 3 largest; almost meeting medially, leaving only a part of dorsum exposed. Notopodial lamellae on chaetiger 2 as broadly rounded to subquadrate lobe. Notopodial lamellae on chaetiger 3 broad subquadrate with the medial edge prolonged over the dorsum into elongated produced tip (Figs. 16b and 21i). Notopodial lamellae on chaetiger 4 either broadly conical not produced into short tip (L.H. side, Fig. 21j) or broadly rounded to subquadrate with short produced tip directed medially over dorsum (R.H. side, Fig. 21j). Neuropodium of chaetiger l rudimentary; on chaetiger 2 as a small broadly rounded lobe which becomes larger on chaetiger 3 and then again smaller on chaetiger 4. On chaetiger 5, notolamellae remain well developed, as broadly subtriangular lobes (Fig. 21k), with neuropodial lamellae as low broadly rounded lobes. From chaetiger 6, both noto- and neuropodial lamellae as broadly rounded lobes, getting progressively smaller and lower, with notolamellae being larger in anterior chaetigers. On chaetigers 6–7, a very low dorsal crest detected, becoming high and well developed in chaetigers 9–12.
Chaetae consist of 3 types: narrowly bilimbate capillaries, ventral sabre chaetae, and multidentate hooded hooks. Anterior chaetae arranged in 2 rows of longer and shorter limbate capillaries; chaetae particularly long in neuropodia of chaetiger 2. A single heavily granulated and ventral sabre chaeta present from chaetiger 10. Neuropodial hooded hooks first observed in chaetiger 10, with six hooks per fascicle accompanied by few capillaries. Neuropodial hooks with rounded primary hood and detectable secondary hood, with 3 teeth in lateral view (Figs. 21e–f and 22e–f). Notopodial hooks not observed in available fragments. The rest of body and pygidium unknown.
Molecular information. The two 16S sequences from specimens of this species match with 14 published sequences of Aurospio sp. ‘249 PB’ from other eastern CCZ areas (GSR, Ifremer, IOM) (Bonifácio et al. 2020). The uncorrected (p) distances among the 16 sequences range between 0.0 and 0.017. It also matches an already published sequence labeled Aurospio dibranchiata KP342 with GenBank accession number EU340087 (Mincks et al. 2009) collected from the CCZ during the Kaplan project and another sequence labeled Aurospio cf. dibranchiata PAP with GenBank accession number MH379971 collected from the Porcupine Abyssal Plain, NE Atlantic (Neal et al. 2018b). The uncorrected (p) distances to published sequences were 0.009 and 0.004, respectively.
Remarks. Aurospio sp. NHM_2186 is the second of three CCZ collected species so far that corresponds well to Aurospio dibranchiata based on characters such as the shape of prostomium, two pairs of small branchiae partially fused to notopodial lamellae of chaetigers 3 and 4 and neuropodial hooded hooks from chaetiger 10. However, as already discussed, reliable taxonomic characters have not been found during the examination of the available material. This may change in the future, should better preserved material become available, but currently DNA identification appears to be the best tool available.
One character of note in the case of Aurospio sp. NHM_2186 is the form of neuropodial hooks (see comparative Fig. 22a–h). These differ from both Maciolek type material (BMNH.1981.82-91) and Aurospio sp. NHM_091 in being tridentate (Fig. 22f), rather than quadridentate (Fig. 22a–d). Also, the hooks are overall more slender and higher magnification is necessary to achieve a similar detailed view to Aurospio sp. NHM_091. Form of neuropodial hooks in the third ABYSSLINE species—Aurospio sp. NHM_2247—cannot be established with certainty, as these hooks have proved particularly difficult to observe with necessary detail (Fig. 22g, h).
Distribution. Molecular evidence based on 16S suggests that Aurospio sp. NHM_2186 is a widely distributed species as it was found in the UKSR-1, GSR, Ifremer, and IOM exploration areas in the eastern CCZ, Kaplan site CCZ, and Porcupine Abyssal Plain in NE Atlantic (Neal et al. 2018b).
Aurospio sp. NHM_2247
Figs. 16c, 17c, 22g–h, 23a–f, 24a–e
Aurospio sp. NHM_2247 a preserved specimen NHMUK.ANEA.2021.9 in dorsal view, with peristomial pigmentation visible; b specimen in dorsal view stained with Shirlastain, with dorsal crests visible; c detail of anterior end in dorsal view, specimen stained with Shirlastain; d detail of branchial chaetigers 3 and 4, specimen stained with Shirlastain; e close-up image of dorsal crests; f neuropodial hooded hooks. Scale bars: a 1000 μm; e 250 μm; f 25 μm
Line drawings of Aurospio sp. NHM_2247, specimen NHMUK.ANEA.2021.9 a prostomium; b notopodial lamella from chaetiger 3 (ch3); c notopodial lamella from chaetiger 4 (ch4); d notopodial lamella from chaetiger 5 (ch5); e notopodial lamella from chaetiger 6 (ch6)
Material examined: NHM_2247, NHMUK ANEA.2021.9, coll. 01 Mar. 2015, collection code: EB06, 12°15.44N, 117°18.13W, 4302 m.
Description. Small slender species represented by a single posteriorly incomplete specimen, 2.1 mm long and 0.4 mm wide for 12 discernible chaetigers (Fig. 23a–b). Live specimens not observed; the color in alcohol tanned with very strong reddish pigmentation dorsally on peristomium (Fig. 23a).
Prostomium rounded, posteriorly narrowing into relatively thick caruncle to the end of chaetiger 1 (Figs. 16c, 23c, 24a). Eyes not observed. Peristomium forms a narrow hood around prostomium, not forming lateral wings (Fig. 23c). Palps missing.
Branchiae present on chaetigers 3–4 only; both short, smooth, cirriform, and basally fused to the corresponding notopodial lamellae (Figs. 17c, 23c–d, 24b–c). Branchiae on chaetiger 3 longer, approaching the length of corresponding notopodial lamellae; branchiae on chaetiger 4 very short, stubby, only reaching about 1/3 length of corresponding notopodial lamellae.
Notopodium of chaetiger l rudimentary. Notopodial lamellae best developed on chaetigers 2–6, with those on chaetiger 3 largest; not meeting medially, leaving part of dorsum exposed (Fig. 23c). Notopodial lamellae on chaetiger 2 approaching rhomboid shape. Notopodial lamellae on chaetiger 3 broad, subquadrate with the medial edge prolonged over the dorsum into blunt tip (Figs. 17c and 24b). Notopodial lamellae on chaetiger 4 broadly subquadrate with short blunt tip (Figs. 17c and24c). Neuropodium of chaetiger l rudimentary; on chaetiger 2 as a small broadly rounded lobe which becomes larger on chaetiger 3 and then again smaller on chaetiger 4. From chaetiger 5, both noto- and neuropodial lamellae as broadly rounded lobes, getting progressively smaller and lower, with notolamellae being larger in anterior chaetigers (Fig. 24d–e). On chaetigers 6–7, a low dorsal crest detected, becoming very high and well developed in chaetigers 9–12 (end of the fragment) (Fig. 23e). Form of parapodia not established past chaetiger 12 (end of the longest fragment).
Chaetae consist of 3 types: capillaries, ventral sabre chaetae and multidentate hooded hooks. Anterior chaetae arranged in 2 rows of longer and shorter limbate capillaries; chaetae particularly long in neuropodia of chaetiger 2. A single heavily granulated and ventral sabre chaeta present from chaetiger 10, but mostly broken off. Neuropodial hooded hooks first observed in chaetiger 10, with six hooks per fascicle accompanied by few capillaries. Neuropodial hooks with squarish primary hood, secondary hood not confirmed, with several minute teeth in lateral view (Figs. 22g–h and 23f). Notopodial hooks not observed in available fragments. The rest of body and pygidium unknown.
Molecular information. The 16S sequence from this species matches four sequences from Aurospio sp. ‘80 PB’ (Bonifácio et al. 2020), with the uncorrected (p) distances ranging from 0.0 to 0.005 among the five sequences. Interestingly, Aurospio sp. NHM_2247 falls out as sister taxon to species found in bathyal (1000–1600 m) East and West Atlantic rather than CCZ abyssal species (Fig. 6).
Remarks. This is the third species morphologically consistent with Aurospio dibranchiata found in the ABYSSLINE material. It is of interest to report that Aurospio sp. NHM_2247 has the best developed dorsal lamellae of any ABYSSLINE-collected specimens, but often this character cannot be established with certainty due to integument damage and Aurospio sp. NHM_2247 is represented by a single specimen only.
Distribution. This species has been found in OMS-1, GSR, and Ifremer exploration areas.
Aurospio sp. NHM_776
Material examined: NHM_776, NHMUK ANEA.2019.10020, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m.
Description: Single poorly preserved specimen, small and slender, 2.5 mm long and 0.25 mm wide, anterior fragment with about 14 discernible chaetigers. Color in alcohol pale yellow, without distinct pigmentation (Fig. 25).
Preserved specimen NHMUK.ANEA.2019.10020 of Aurospio sp. NHM_776. Scale bar: 1000 μm
Prostomium anteriorly rounded, longer than wide, extending into blunt caruncle to beginning of chaetiger 2, without peaks. Eyes absent. Peristomium as narrow hood around prostomium, not forming lateral wings; dorsally not fused. Palps missing.
Parapodial lamellae often damaged or missing, but large foliaceous to subtriangular notopodial lamellae observed on chaetiger 3, these arch medially over dorsum. Single pair of branchiae only on chaetiger 3, other branchiae absent; smooth and cirriform branchial pair, about the same length as notopodial lamellae on chaetiger 3. Neuropodial lamellae on chaetiger 3 also greatly enlarged, rounded.
Only capillary chaetae observed in the available fragment, chaetae particularly long in chaetiger 3. Multidentate hooded hooks in notopodia or neuropodia and sabre chaetae not observed in the available fragment. The rest of body and pygidium unknown.
Molecular information: The 16S sequence from this species matches one spionid sequence from another study (Bonifácio et al. 2020) with collection locality in Ifremer exploration contract area and accession number MK971061, the uncorrected (p) distance between the two sequences is 0.005.
Remarks: Although this single specimen is in rather poor condition, the shape of prostomium and the presence of single branchial pair on chaetiger 3, accompanied by greatly enlarged notopodial lamellae suggest similarities to Aurospio foodbancsia Mincks et al., 2009. This species was described from the Bellingshausen Sea, the Southern Ocean, depths of around 500 m, where it was particularly abundant (Mincks et al. 2009). Due to poor preservation of the ABYSSLINE specimen, meaningful comparison is difficult. It appears that no sabre chaetae or hooded hooks are present in Aurospio sp. NHM_776 in first 14 chaetigers, while these were detected from chaetiger 10 and 11, respectively, in the known species. However, it is not currently clear if this is a true absence of hooks and sabre chaetae, or true posterior distribution or absence. Another species collected from ABYSSLINE samples also share these characters (see Remarks under Aurospio sp. 1661).
Distribution: This species is known from UK-1 and Ifremer exploration contract areas in the eastern CCZ.
Aurospio sp. NHM_1661
Fig. 26a–c
Aurospio sp. NHM_1661 a preserved specimen NHMUK.ANEA.2019.10043 in lateral view; b fascicle of neuropodial hooded hooks; c neuropodial sabre chaeta. Scale bars: a 250 μm; b-c 25 μm
Material examined: NHM_1661, NHMUK ANEA.2019.10043, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m.
Description: Single poorly preserved specimen, small and slender, 1.9 mm long and 0.25 mm wide, anterior fragment with 15 chaetigers (Fig. 26a).
Prostomium anteriorly rounded, longer than wide, extending into blunt caruncle to beginning of chaetiger 2, without peaks. Eyes absent. Peristomium as narrow hood around prostomium, not forming lateral wings; dorsally not fused. Palps missing.
Parapodial lamellae relatively small, rudimentary on chaetiger 1; notopodial lamellae enlarged and foliaceous to subtriangular on chaetiger 3. Single pair of branchiae only on chaetiger 3, other branchiae absent; smooth and cirriform branchial pair, slightly longer than notopodial lamellae on chaetiger 3. Neuropodial lamellae on chaetiger 3 also enlarged, rounded.
Chaetae of three types: capillaries, hooded hooks (Fig. 26b) and sabre chaetae (Fig. 26c). First 9 chaetigers with capillaries only. Stout, curved, limbate and distally granulated sabre chaeta from chaetiger 10. Multidentate hooded hooks observed in neuropodia from chaetiger 11 where 4 per fascicle, up to 6 per fascicle in subsequent chaetigers. Hooded hooks long and slender, with several about 4 small teeth above main fang as observed under light microscopy (Fig. 26b); with inflated, rounded hood; secondary hood not observed. Notopodial hooded hooks not observed in available fragments. The rest of body and pygidium unknown.
Molecular information: The 16S sequence from this species matches five sequences from another CCZ study labeled as Spionidae sp. (Bonifácio et al. 2020, GenBank accession numbers MK970880, MK970987, MK971006, MK971016, MK971114), with the uncorrected (p) distances ranging from 0.0 to 0.005 among the six sequences. The COI sequence from this species has a 100% match with a polychaete sequence from the Belgian (GSR) contract area in CCZ submitted to GenBank by Janssen et al. (2015) and labeled as Polychaeta sp. NB-Po304, accession number KJ736487.1. Interestingly, in the phylogenetic tree (Fig. 6), the sister taxon of Aurospio sp. NHM_1661 is the Southern Ocean species A. foodbancsia, with which it also shares morphological similarities.
Remarks: This species corresponds well to Aurospio foodbancsia from the Southern Ocean as already discussed in Remarks of Aurospio sp. NHM_776. It agrees in the shape of prostomium, form and distribution of branchiae and lamellae on chaetiger 3 as well as distribution of sabre chaetae and neuropodial multidentate hooks on chaetigers 10 and 11, respectively. However, the single incomplete specimen cannot be meaningfully differentiated from the known species beyond observation that parapodial lamellae are rather small.
Distribution: This species is known from UK-1, GSR, and IOM exploration areas in the eastern CCZ.
Laonice Malmgren, 1867
Type species: Laonice cirrata Malmgren, 1867
Diagnosis: Prostomium anteriorly rounded or T-shaped, maybe free from peristomium or dorsally or completely fused with peristomium. Occipital tentacle present or absent. Caruncle followed by nuchal organs on dorsal surface along several anterior chaetigers. Palps without sheath at base. Peristomium not fused to chaetiger 1. Branchiae present from chaetiger 2. Neuropodial inferior fascicles with sabre chaetae and usually bidentate (in lateral view) hooded hooks starting in the anterior part of the body. Genital pouches present. Pygidium terminal, with two small ventral papilliform cirri and several pairs of comparatively long dorsal cirri.
Remarks: Genus Laonice consists of 38 described species with many more not formalized especially from deep sea environments, in part reflecting the problematic taxonomy of this group (e.g., Sikorski et al. 2017; Bogantes et al. 2018). Laonice has recently been divided into four subgenera: Laonice, Sarsiana, Appelloefia, and Norgensia by Sikorski et al. (2017), based on characters such as fusion of prostomium and peristomium, development of nuchal organs, presence of notopodial hooks, number of rows of capillaries in anterior chaetigers, and the distribution of branchiae and genital pouches. This division has not been based on a phylogenetic approach and is not followed here also due to the fact that necessary diagnostic characters could not be observed in the ABYSSLINE specimens owing to their poor preservation.
Although Laonice is commonly encountered in deep-sea samples (Guggolz et al. 2019), currently only 11 species of Laonice have been described from waters deeper than 400 m (Sikorski et al. 2017; Sikorski et al. 2021). In ABYSSLINE material, seven species of Laonice have been recognized based on morphology and molecular data. Six species are represented by poorly preserved specimens. The other species, although represented by incomplete specimens possesses unique “easy to recognize” characters that distinguish them from all know Laonice and thus decision has been made to formally described it as new species—Laonice shulseae sp. nov.
Our phylogenetic analysis recovered the species assigned to Laonice in a well-supported clade (Fig. 6), although its position within Spionidae was unresolved.
Laonice sp. NHM_2111
Material examined: NHM_2111, NHMUK ANEA.2021.10, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m.
Description: Poorly preserved single specimen consisting of damaged prostomium and about 10 discernable chaetigers long anterior fragment, about 0.9 mm long.
Molecular information: The 16S sequence from this species does not match any other available sequences from the CCZ, but it falls into a well-supported Laonice clade (Fig. 6).
Remarks: The available anterior fragment is in particularly poor morphological condition and cannot be meaningfully compared with other species.
Distribution: This species is only known from APEI-6.
Laonice sp. NHM_1662.
Laonice sp. NHM_1662 NHMUK ANEA.2021.11, in images d–e specimen stained with Shirlastain a–b anterior end in dorsal view showing the stout chaetae; c specimen in ventral view with prostomium and palps in antero-dorsal view; d detail of prostomium in antero-dorsal view with one remaining palp attached and small antenna (arrow); e–f remaining notopodial lamellae and branchiae on chaetigers 3–6 marked by arrows, ntps—notopodial lamellae, br—branchiae. Scale bars: b 250 μm; c, e, f 1 mm
Laonice sp. NHM_1662, NHMUK ANEA.2021.11 a capillaries from anterior chaetigers; b capillaries from chaetiger 9; c sabre chaetae d neuropodial hooded hooks; e detail of dentition of neuropodial hooks. Scale bars: a, b, c 50 μm; e 25 μm; d 20 μm
Material examined: NHM_1662, NHMUK ANEA.2021.11, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m.
Description: Single specimen consisting of 16 chaetigers long anterior fragment, 1.5 mm long and 0.4 mm wide. Preserved specimens pale yellow in ethanol (Fig. 27a, c), with some reddish pigmentation near the anterior margin of prostomium. Body narrow and cylindrical, not anteriorly expanded. Anterior chaetae very well developed, stout and long, almost forming a cephalic cage (Fig. 27b).
Prostomium narrow, anteriorly rounded (Fig. 27c–d); dorsally free from peristomium; no eyes observed; with very slender cirriform antenna (Fig. 27d). Pair of short, thick grooved palps attached (one lost during the examination) reaching to chaetiger 3 (Fig. 27c–d). Caruncle not clearly detected. Branchiae often missing, but still attached in some chaetigers, including chaetiger 2, branchiae very slender and cirriform, long (about twice the length of corresponding notopodial lamellae) (Fig. 27e–f).
Parapodial lamellae of chaetiger 1 well developed, but smaller than those on subsequent chaetigers; notopodial lamellae, slender elongated conical; neuropodial lamellae foliaceous, widened basally, distally produce into rounded tip. Parapodial lamellae of chaetiger 2 similar to those in chaetiger 1, but larger. Notopodial lamellae largest on chaetigers 3–5 with those in chaetiger 3 largest; foliaceous with their produced tips bent medially towards dorsum (Fig. 27e-f). Neuropodial lamellae of chaetigers 3–6 wide rounded lobes. Parapodial lamellae past chaetiger 7 mostly missing/damaged. Genital pouches not observed in 16 chaetiger long fragment.
Notochaetae capillaries, arranged in two rows, in first 12 chaetigers notochaetae shorter and very stout (Fig. 28a) than those in subsequent chaetigers, which are very long, silky in appearance, very slender and narrowly bilimbate (Fig. 28b). Neurochaetae in first 12 chaetigers very stout, shorter than notochaetae. Sabre chaetae first observed on chaetiger 9, two per fascicle, relatively slender, granulated and non-limbate (Fig. 28c). Neuropodial hooded hooks first clearly observed on chaetiger 13, up to 8 per fascicle (Fig. 28d), accompanied by few thin capillaries; all hooks bidentate, with main fang and slender secondary tooth well separated (Fig. 28e); with tight fitting, somewhat anteriorly truncated hood. The rest of the body unknown.
Molecular information. The 16S sequence from this species matches one sequence from another study (Bonifácio et al. 2020) with collection locality in GSR exploration area labeled as Laonice sp. 381 PB and GenBank accession number MK971107; the uncorrected (p) distance between the two sequences is 0.002. The sequence from the CCZ specimen falls into a well-supported Laonice clade (Fig. 6).
Remarks. Although the description is based on a single, incomplete specimen and not all characters could have been observed, the following combination of the characters is unique to this specimen, suggesting it belongs to a new species: the narrow form of prostomium, the anterior start of neuropodial hooks (chaetiger 13) and the marked change in the form of capillary chaetae throughout the body, with anterior chaetae creating an effect of “cephalic cage.” However, as the species cannot be meaningfully compared with other species due to poor preservation we ascribe this specimen to morphospecies only.
Distribution. This species is known from UK-1 and GSR exploration areas in the eastern CCZ.
Laonice sp. NHM_131
Fig. 29a–b
Laonice species from the ABYSSLINE samples a live image of Laonice sp. NHM_131 in dorsal view, prostomium not visible except for small antenna (arrow) showing enlarged parapodial lamellae; b preserved specimen of Laonice sp. NHM_131 in anterior-dorsal view showing prostomium and parapodial lamellae of chaetiger 1; c Laonice sp. 016 specimen NHMUK.ANEA.2021.15 in in antero-dorsal view, showing prostomium and parapodial lamellae of chaetigers 1–3, specimen stained with Shirlastain; d Laonice sp. 048 with prostomium in dorsal view, showing antenna (arrow), specimen stained with Shirlastain. All scale bars: 1 mm
Material examined: NHM_131, NHMUK ANEA.2021.17, coll. 11 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°45.500N, 116°41.911W, 4080 m; NHM_577, NHMUK ANEA.2021.18, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_586, NHMUK ANEA.2021.19, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_1510, NHMUK ANEA.2021.20, coll. 05 Mar. 2015, collection method: Multi Corer, 12°27.125N, 116°30.736W, 4199 m; NHM_2117, NHMUK ANEA.2021.21, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m; NHM_1581, NHMUK ANEA.2021.22, coll. 07 Mar. 2015, collection method: USNEL Box Core, 12°25.195N, 116°37.477W, 4136 m.
Description: Six poorly preserved specimens, consisting of body fragments or short anterior fragments only. Preserved specimens pale yellow in ethanol. The best-preserved specimen (NHM_2117) 1.2 mm long and 0.4 mm wide for 8 chaetigers (Fig. 29a). Prostomium anteriorly somewhat truncated, only slightly expanded without obvious lateral horns; dorsally free from peristomium (Fig. 29b); no eyes observed; with large triangular antenna (Fig. 29a). Caruncle not detected. Branchiae mostly missing, but still attached in few chaetigers, including chaetiger 2 (Fig. 29b), slightly longer than corresponding notopodial lamellae.
First notopodial and neuropodial lamellae well developed only slightly smaller than in subsequent chaetigers. Notopodial lamellae on chaetiger 1 elongated (Fig. 29b), similar in anterior most chaetigers, soon becoming very large rounded (Fig. 29a) and remaining as such till end of fragment. Neuropodial lamellae on chaetiger 1 auricular to rounded (Fig. 29b), getting progressively larger on chaetigers 2–4 and then remaining well developed, rounded till end of the fragment (Fig. 29a). Neuropodial genital pouches not detected in the available fragments. Capillary chaetae in first chaetiger stouter and shorter and granulated, in subsequent chaetiger capillaries more slender and longer, neurochaetae with some granulation, notochaetae smooth and narrowly bi-limbate. Sabre chaetae and hooded hooks not observed in the available fragments. The rest of the body unknown.
Remarks. This species appears to have particularly large and rounded parapodial lamellae in comparison to other UKSR-1 species.
Molecular information. The 16S sequences from the specimens within this species group matches sequences from Laonice sp. ‘349 PB’ from other areas in the eastern CCZ (Bonifácio et al. 2020), extending its distribution from the UK1 area to BGR, GSR and Ifremer exploration contract areas in the Eastern part of CCZ. The uncorrected (p) distances among the in total 15 sequences range between 0.0 and 0.013.
Distribution: This species is known from UK-1, BGR, GSR, and Ifremer exploration contract areas in the eastern CCZ.
Laonice sp. NHM_016
Fig. 29c
Material examined: NHM_016, NHMUK ANEA.2021.12, coll. 9 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°50.232N, 116°33.506W, 4336 m; NHM_685, NHMUK ANEA.2021.13, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_882, NHMUK ANEA.2021.14, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m;
NHM_1243, NHMUK ANEA.2021.15, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m; NHM_1425, NHMUK ANEA.2021.16, coll. 03 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°27.26N, 116°36.77W, 4137 m.
Description: Five poorly preserved specimens, consisting of 12–18 chaetigers long anterior fragments, 1.5–2.3 mm long and 0.7–1 mm wide. Preserved specimens pale yellow in ethanol. Prostomium narrow, anteriorly only slightly expanded and rounded; dorsally fused to peristomium; with a pair of tiny faint red eyes positioned medially; with very small triangular antenna (maybe scar?) observed in specimens NHM_882 and NHM_1243 upon staining with Shirlastain (Fig. 29c). Caruncle not detected. Branchiae all missing. Notopodial lamellae very small on chaetiger 1 where broadly conical (Fig. 29c), becoming larger and more elongated in chaetiger 2 and largest over chaetiger 3 where tips bent medially over dorsum; then remaining well developed till chaetiger 18 (the last observed chaetiger). Neuropodial lamellae very small on chaetiger 1, round to auricular (Fig. 29c), then getting larger and elongated on chaetiger 2 and becoming best developed on chaetigers 3–5, then getting progressively smaller, but remaining well developed. Neuropodial genital pouches present, first observed between chaetigers 14 to 15, then detected till rest of the fragment. Capillary chaetae in anterior chaetigers stouter, shorter and granulated, becoming very long, smooth and threadlike towards the end of the fragment. Sabre chaetae and hooded hooks not observed in 18 chaetigers long fragment. The rest of the body unknown.
Molecular information: The five 16S sequences from this species does not match any other sequences on GenBank, the uncorrected (p) distances within the species range between 0.0 and 0.009. The COI sequence matches six sequences from CCZ submitted to GenBank by Janssen et al. (2015) and labeled as Polychaeta sp. (accession numbers KJ736571-KJ736576); the uncorrected (p) distances among these seven sequences range between 0.004 and 0.02.
Remarks. As with other species of Laonice collected from UK-1, several taxonomically informative characters cannot be observed due to poor preservation. This species is therefore assigned to morphospecies only, accompanied by DNA sequences.
Distribution: This species is known from UK-1 and BGR claim areas in the eastern CCZ.
Laonice sp. NHM_048
Material examined: NHM_048, NHMUK ANEA.2021.23, coll. 9 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°50.232N, 116°33.506W, 4336 m; NHM_538, NHMUK ANEA.2021.24, coll. 17 Feb. 2015, collection method: USNEL Box Core, 12°22.020N, 116°31.017W, 4158 m; NHM_563, NHMUK ANEA.2021.25, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_591, NHMUK ANEA.2021.26, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_592, NHMUK ANEA.2021.27, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_706, NHMUK ANEA.2021.28, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_741, NHMUK ANEA.2021.29, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_944, NHMUK ANEA.2021.30, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m; NHM_781, NHMUK ANEA.2021.31, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_1676, NHMUK ANEA.2021.32, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m; NHM_1335, NHMUK ANEA.2021.33, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m; NHM_1451, NHMUK ANEA.2021.34, coll. 03 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°27.26N, 116°36.77W, 4137 m; NHM_1663, NHMUK ANEA.2021.35, coll. 10 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°21.81N, 116°40.86W, 4233 m; NHM_1992, NHMUK ANEA.2021.36, coll. 15 Mar. 2015, collection method: USNEL Box Core, 12°00.559N, 117°22.818W, 4141 m; NHM_2120, NHMUK ANEA.2021.37, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m; NHM_1018, NHMUK ANEA.2021.38X, coll. 24 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°08.02N, 117°17.52W, 4122 m.
Description: Sixteen poorly preserved specimens, consisting of very short anterior fragments. Preserved specimens pale yellow in ethanol. The best-preserved specimen (NHMUK_048) anterior fragment with 12 chaetigers, 2 mm long and 0.85 mm wide. Prostomium anteriorly somewhat truncated, expanded into short, but distinct rounded lateral horns (Fig. 29d); dorsally free from peristomium; no eyes observed; with large triangular antenna (Fig. 29d). Caruncle not detected. Branchiae all missing. First notopodial and neuropodial lamellae well developed only slightly smaller than in chaetiger 2; notopodial lamellae elongated, conical; neuropodial lamellae broad, somewhat triangular; the rest of parapodial lamellae missing or damaged (12 chaetiger long fragment). Neuropodial genital pouches in the available fragments. Capillary chaetae in anterior chaetigers stouter, shorter, and granulated, becoming long and smooth towards the end of the fragment. Sabre chaetae first detected in neuropodia of chaetiger 10, up to per fascicle, slender, heavily granulated and uni-limbate. Hooded hooks not detected in the available fragments. The rest of the body unknown.
Molecular information. The 16S sequences from this species matches seven sequences from Laonice sp. ‘361 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the sequences range between 0.0 and 0.007, extending this species distribution to the BGR, GSR, and Ifremer exploration contract areas in the Eastern CCZ. The COI sequences matches four sequences from CCZ submitted to GenBank by Janssen et al. (2015) and labeled as Laonice sp. with accession numbers KJ736564, KJ736566, KJ736567, and KJ736570, and three sequences from another study (Bonifácio unpubl. data), the uncorrected (p) distances among these 13 sequences range between 0.0 and 0.009.
Remarks. Due to poor preservation of available material this species is assigned to morphospecies only, accompanied by DNA sequences.
Distribution: This species is known from UK-1, BGR, GSR, and Ifremer exploration contract areas in the eastern CCZ.
Laonice sp. NHM_2076
Fig. 30a–d
Laonice sp. NHM_2076, specimen NHMUK.ANEA.2021.39 a–b preserved specimen in lateral view, c anterior end in antero-dorsal view, specimen stained with Shirlastain; d diagrammatic line drawing of prostomium and anterior dorsal lamellae; e neuropodial hooded hooks from chaetiger 18. Scale bars: a 500 μm; b 250 μm; e 25 μm
Material examined: NHM_2076, NHMUK ANEA.2021.39, coll. 17 Mar. 2015, collection method: USNEL Box Core, 12°01.643N, 117°19.512W, 4139 m.
Description: Anterior fragment of specimen consisting of ca. 20 discernable chaetigers (ca. 0.8 mm long) and damaged body region. Body narrow and cylindrical. Preserved specimen white in ethanol (Fig. 30a, b).
Prostomium anteriorly rounded, appearing free from peristomium (Fig. 30c, d); no eyes observed; antenna not confirmed. Branchiae mostly missing or damaged. Parapodial lamellae overall small, best developed over the first 5 chaetigers. Genital pouches not confirmed likely due to poor preservation. Observed capillaries slender and lightly granulated. Sabre chaetae not detected. Neuropodial hooded hooks observed from chaetiger 18 (Fig. 30e), hooks very slender and sigmoid, with 2 small teeth in profile and narrow primary hood. The rest of the body unknown.
Molecular Information. The 16S sequence from this species matches three sequences from Laonice sp. ‘334 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the four sequences are 0.0, extending this species distribution to the GSR, Ifremer, and IOM exploration contract areas in the eastern CCZ.
Remarks. This single anterior fragment appears atypical of Laonice species in having rather narrow cylindrical body and small parapodial lamellae.
Distribution: This species is known from OMS-1, GSR, Ifremer, and IOM exploration contract areas.
Laonice shulseae sp. nov. http://zoobank.org/02AF55D7-4F41-44FB-B9A4-49E34F99715E
Laonice shulseae sp. nov., holotype NHMUK.ANEA.2021.50, in images d–e specimen with retained Shirlastain a preserved specimen in dorsal view; b–d anterior part in dorsal view, with image c anterior end in dorsal view represented as diagrammatic line drawing; d anterior end in lateral view, showing separation of prostomium and peristomium. Scale bars: a 1000 μm; b, d 500 μm
Laonice shulseae sp. nov., holotype NHMUK.ANEA.2021.50 a spines from chaetiger 1; b capillary chaetae from chaetiger 1; c capillary chaetae from ch 7 (typical for chaetigers 4-8); d detail of capillary chaetae from ch 4 (typical for chaetigers 4–7); e hairy tips from chaetiger 7; f capillaries from chaetiger 9; g sabre chaeta; h detail of sabre chaeta; i neuropodial hooks. Scale bars: a, b, d, e, i 10 μm; c, f, g 25 μm
Material examined: holotype NHM_2182, NHMUK ANEA.2021.50, coll. 21 Mar. 2015, collection method: USNEL Box Core, 19 27.998N, 120 00.172W, 4141 m; NHM_2098, NHMUK ANEA.2021.48, coll. 20 Mar. 2015, collection method: Brenke Epibenthic Sledge, 19 27.874 N, 120 01.525W, 4026 m; NHM_2181, NHMUK ANEA.2021.49, coll. 21 Mar. 2015, collection method: USNEL Box Core, 19 27.998N, 120 00.172W, 4141 m.
Description: Three posteriorly incomplete specimens; the best-preserved specimen (holotype NHM_2182) now in two fragments, anterior fragment 11.5 mm long for ca. 100 chaetigers and 1.25 mm at the widest region and body fragment with ca. 40 chaetigers (Fig. 31a). Anterior 10 chaetigers widest, flattened dorso-ventrally; following chaetiger gradually narrowing (Fig. 31a-d). Body pale yellow in alcohol (Fig. 31a).
Prostomium bell-shaped (Fig. 31b, c), anterior margin with shallow median incision, with slender cirriform occipital antenna present at the anterior end of the caruncle (Fig. 31c–e). Eyes absent. Peristomium moderately developed and appearing separated from the prostomium dorsally and laterally (Fig. 31e). Palps missing. Nuchal organ as pair of thick short loops extending past the anterior margin of chaetiger 2 (Fig. 31b–d), with light brown pigmentation.
Notopodial postchaetal lamellae overall well developed, smallest in chaetiger 1; large, fleshy and triangular (Fig. 31b–d) in the widest anterior part of the body (chaetigers 2–10); damaged or missing in the rest of the body but occasionally elongated triangular lamellae with blunt distal tip observed. Neuropodial postchaetal lamellae similar in development, with the smallest lamella in chaetiger 1 and largest lamellae in chaetigers 2–10; all lamellae broadly oval (Fig. 31e). Neuropodial pouches could not be confirmed. Branchiae missing.
Chaetal types undergoing marked change between chaetigers 2 and 3 and then 8 and 9. Chaetigers 1 and 2 with eight stout spine-like chaetae in a fan-shaped arrangement (Fig. 31a–d), spines abruptly curved, extending into very long slender tip and covered with fine hair when observed under high magnification (Fig. 32a); few slender, smooth narrowly bi-limbate capillaries also present (Fig. 32b). In chaetigers 3–8, chaetae arrange in four rows, chaetae broadly limbate capillaries (Fig. 32c), broadest in the middle (Fig. 32d), and abruptly extending into long slender tips, covered with fine hair when observed under high magnification (Fig. 32e). From chaetiger 9 capillaries long and slender, narrowly bi-limbate without granulations and hair (Fig. 32f). Sabre chaetae first detected from chaetiger 9, one or two per neuropodium, long, stout, and granulated (Fig. 32g, h). Neuropodial hooded hooks present (Fig. 32i), their start uncertain due to damage (~chaetiger 25); hooks very long and slender, about three per fascicle; bidentate in lateral view, both teeth minute without obvious main fang, with very short and narrow hood and appearing aristate under high magnification. Most of the body past chaetiger 10 too damaged, pygidium unknown.
Molecular information. In our phylogenetic analysis (Fig. 6), Laonice shulseae sp. nov. has been recovered within a well-supported clade containing other species in the genus Laonice. The three 16S sequences from this species did not match any other sequences from the CCZ, the uncorrected (p) distances between the sequences range between 0.0 and 0.005.
Remarks. Laonice shulseae sp. nov. possess an unusual character among known Laonice species—the spines in chaetigers 1 and 2 (Fig. 32a). Only one recently described species from the bathyal Atlantic, Laonice plumisetosa Bogantes, Halanych and Meißner, 2018 possesses similar chaetae that Bogantes et al. (2018) described as “stout capillaries with plush-like texture.” However, L. shulseae sp. nov. can be easily distinguished from the known species by the following characters. New species has a different body shape, with the anterior chaetigers distinctly broadened (Fig. 31a, b, c). Although both species share the looped nuchal organs (also rare in Laonice), these are much shorter in the known species, not exceeding chaetiger 1, while they surpass the anterior margin of chaetiger 2 in L. shulseae sp. nov. (Fig. 31b, c). Furthermore, the two species can be differentiated based on the morphology of hooded hooks, which are tri-dentate with distinct main fang in the known species, but in L. shulseae sp. nov. they have a very small bidentate distal dentition, without obvious main fang (Fig. 3i).
While it is clear that ABYSSLINE specimens represent a new species, many other characters of taxonomic importance among species of Laonice cannot be ascertained due to poor morphological preservation (e.g., missing branchiae). Nevertheless, we formalize new species Laonice shulseae sp. nov. despite limitations of the material as unique morphological and molecular characters are available and allow for easy identification (see also Bogantes et al. 2018). Should better preserved specimens be found in the future, the current morphological description can be amended.
Distribution: This species has only been found in CCZ APEI-6, an area assigned for preservation.
Etymology. This species is named for Dr. Christine Shulse, a scientist that participated in the first ABYSSLINE cruise in 2013.
Prionospio Malmgren, 1867
Type species: Prionospio steenstrupi Malmgren, 1867
Diagnosis (emended from Peixoto and Paiva, 2019). Prostomium without occipital antenna. Peristomium at least partially fused with chaetiger 1. Parapodia of chaetiger 1 reduced. Noto- and neuropodial lamellae largest in branchial region. Branchiae from chaetiger 2 or rarely absent. Branchiae limited to anterior chaetigers, can be all apinnate, all pinnate, or various combinations of both; free from dorsal lamellae. Dorsal crests present or absent. Interparapodial pouches present or absent. Anterior chaetae limbate capillaries; posterior noto- and neuropodial hooded hooks present, bi-, tri-, or multidentate, with secondary hood. Neuropodial sabre chaetae present or absent. Pygidium with long dorsomedial cirrus and two shorter ventrolateral cirri, all sometimes fused.
Remarks. The Prionospio-complex represents one of the most morphologically diverse and species rich groups within the Spionidae, although it is currently poorly defined. The arrangements of branchial diversity were used in the past to inform systematics of Prionospio (e.g., Foster 1971; Sigvaldadóttir 1998), a problem highlighted by recent discoveries of abranchiate species (Paterson et al. 2016; Peixoto and Paiva 2019). Our phylogenetic analyses (Fig. 6) recovered species assigned to Prionospio in a clade with strong support, but this clade also contain species assigned to Aurospio and Paraprionospio.
Prionospio sp. NHM_135
Fig. 33a–c
Prionospio sp. NHM_135 a preserved specimen in dorsal view; b anterior end in dorsal view; c neuropodial hooded hooks from chaetiger 11. Scale bar: a 500 μm; b 250 μm; c 25 μm
Material examined: NHM_135, NHMUK ANEA.2021.40, coll. 11 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°45.500N, 116°41.911W, 4080 m; NHM_1413, NHMUK ANEA.2021.41, coll. 02 Mar. 2015, collection method: USNEL Box Core, 12°27.066N, 116°35.661W, 4130 m; NHM_1347B, NHMUK ANEA.2019.10034, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m; NHM_783G, NHMUK ANEA.2019.10021, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_701, NHMUK ANEA.2019.10018, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m.
Description: This small and slender species is represented by five poorly preserved specimens; the best example is specimen NHMUK_135, an anterior fragment 0.95 mm long and 0.22 mm wide for about 11 discernible chaetigers. Color in alcohol pale yellow (Fig. 33a).
Prostomium anteriorly rounded, posteriorly elongated into slender caruncle reaching the anterior margin of chaetiger 2. Eyes absent. Peristomium forming a narrow hood around prostomium, not pronounced into distinct lateral wings (Fig. 33a, b).
Parapodial lamellae mostly missing or damaged. Branchiae not observed, assumed missing.
Chaetae of three types: capillaries, hooded hooks and sabre chaetae. First 9 chaetigers with capillaries only, which are granulated and narrowly bi-limbate. Sabre chaeta in neuropodia from chaetiger 10; stout, curved, limbate. Single multidentate hooded hook observed in neuropodia of chaetiger 11 (the last available chaetiger). Hooded hook long and slender, multidentate observed under light microscopy; with inflated, rounded hood; secondary hood not observed (Fig. 33c). Notopodial hooded hooks not observed in available fragments.
The rest of body and pygidium unknown.
Molecular Information: The 16S sequences from this species matches four sequences from Prionospio sp. ‘73 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the sequences range between 0.0 and 0.01, extending this species distribution to the BGR, GSR, Ifremer, and IOM exploration contract areas in the Eastern CCZ.
Remarks: Due to poor preservation (the loss of branchiae in particular), this species cannot be meaningfully compared with either known Prionospio species or other Prionospio species found in the ABYSSLINE samples.
Distribution: This species is only known from the eastern CCZ: UK-1, OMS-1, BGR, GSR, Ifremer and IOM exploration contract areas.
Prionospio sp. NHM_471
Fig. 34a–c
Prionospio sp. NHM_471 a preserved specimen in dorsal view, faint Shirlastain still retained, anterior prostomial pigmentation visible; b anterior end in dorso-lateral view, showing notopodial lamellae and branchiae of chaetiger 2; c prostomium with caruncle and peristomium in dorsolateral view. Scale bars: a 1000 μm; c 100 μm
Material examined: NHM_471, NHMUK ANEA.2019.10011, coll. 22 Oct. 2013, collection method: USNEL Box Core, 13°43.597N, 116°40.200W, 4160 m; NHM_646, NHMUK ANEA.2019.10016, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_1930, NHMUK ANEA.2019.10048, coll. 13 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°02.49N, 117°13.03W, 4094 m; NHM_698, NHMUK ANEA.2019.10017, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m.
Description: Small, slender species represented by four posteriorly incomplete specimens. The best example, specimen NHM_471, an anterior fragment with 16 discernible chaetigers, 1.5 mm long and 0.25 mm wide (Fig. 34a). Preserved specimen whitish in color (Fig. 34a).
Prostomium anteriorly truncated, with anterior margin lightly pigmented (Fig. 34b), longer than wide, extending into slender caruncle to beginning of chaetiger 2, without peaks. Eyes absent. Peristomium not developed into lateral wings (Fig. 34b); dorsally not fused. Palps missing.
Parapodial lamellae rudimentary on chaetiger 1, best developed on branchial chaetigers, then getting smaller in postbranchial chaetigers. Notopodial lamellae largest on chaetiger 3, foliaceous to subtriangular with blunt rounded tip, arching medially over dorsum (Fig. 34c); notopodial lamellae on chaetiger 2 about half the size and similar in shape to those in chaetiger 3; notopodial lamellae on chaetiger 4 smaller and much more slender than those on chaetiger 3. Neuropodial lamellae largest on chaetigers 2–4; particularly large on chaetiger 3, blunt and oval. Three pairs of branchiae observed on chaetigers 2–4; all smooth, slender cirriform; first pair of branchiae (= chaetiger 2) longest, surpassing the length of corresponding notopodial lamellae (Fig. 34c); the second pair of branchiae very small, about half the size of corresponding notopodial lamellae; the third pair of branchiae extremely small, stubby. Dorsal ridge not confirmed.
Capillary chaetae only observed in 16 chaetiger long fragment. The presence and distribution of sabre chaetae, noto- and neuropodial hooded hooks unknown. The rest of body unknown.
Molecular information: The four 16S sequences from this species match five sequences from Prionospio sp. ‘268 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the nine sequences range between 0.0 and 0.01, extending this species distribution to the BGR, GSR and IOM exploration contract areas in the Eastern CCZ. The COI sequences match three sequences from CCZ submitted to GenBank by Janssen et al. (2015) and labeled as Prionospio sp. with accession numbers KJ736506, KJ736507 and KJ736509.
Remarks: Although this species could not be described in great detailed with characters such as hooded hooks missing, it appears that this species belongs to a group of deep-sea Prionospio species with reduced number of branchiae (Paterson et al. 2016) and relatively posterior start of neuropodial hooks. The fact that hooded hooks were not observed in the16 chaetiger long anterior fragment of Prionospio sp. NHM_471 suggests their more posterior distribution. Three pairs of branchiae of similar form were also recorded in the species Prionospio sp. NHM_914 and previously in Prionospio branchilucida Altamira, Glover & Paterson in Paterson et al. (2016) also described from CCZ (see Paterson et al. 2016 for details). Further comparison with known species is hampered by poor preservation of ABYSSLINE-collected specimens.
Distribution: This species is only known from CCZ: UK-1, OMS-1, BGR, GSR, and IOM exploration contract areas in the eastern CCZ.
Prionospio sp. NHM_914
Prionospio sp. NHM_914 a preserved specimen in lateral view and b specimen stained with Shirlastain; c preserved specimen in dorsal view; d specimen stained with Shirlastain; e detail of anterior end in antero-dorsal view, showing prostomium and peristomium, first pair of branchiae and enlarged notopodial lamellae of chaetiger 3. Scale bars: 1000 μm
Prionospio sp. NHM_914 a detail of enlarged notopodial lamellae; b neuropodial lamellae of chaetigers 2–4; c neuropodial sabre chaeta (arrow) from chaetiger 19; d neuropodial hooded hooks from chaetiger 19. Scale bars: a 250 μm; b 100 μm; d 50 μm
Material examined: NHM_914, NHMUK ANEA.2019.10024, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m; NHM_1002, NHMUK ANEA.2019.10027, coll. 24 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°08.02N, 117°17.52W, 4122 m; NHM_1099, NHMUK ANEA.2019.10030, coll. 26 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°06.93N, 117°09.87W, 4100 m; NHM_1545, NHMUK ANEA.2019.10041, coll. 06 Mar. 2015, collection method: USNEL Box Core, 12°30.382N, 116°29.073W, 4244 m; NHM_1174A, NHMUK ANEA.2019.10031, coll. 26 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°06.93N, 117°09.87W, 4100 m; NHM_1600, NHMUK ANEA.2021.42, coll. 08 Mar. 2015, collection method: USNEL Box Core, 12°31.273N, 116°41.889W, 4237 m.
Description: Small, slender species represented by six posteriorly incomplete specimens. The best example, specimen NHM_914, an anterior fragment with 19 discernible chaetigers, 2.6 mm long and 0.35 mm wide (Fig. 35a–d). Preserved specimen pale yellow (Fig. 35a, c).
Prostomium anteriorly truncated, longer than wide, extending into slender caruncle to beginning of chaetiger 2, without peaks (Fig. 35e). Eyes absent. Peristomium forming slightly developed lateral wings (Fig. 35e). Palps missing.
Parapodial lamellae rudimentary on chaetiger 1, best developed on branchial chaetigers, then getting smaller in postbranchial chaetigers. Notopodial lamellae largest on chaetiger 3, foliaceous to subtriangular with blunt rounded tip, arching medially over dorsum (Figs 34e, 35a); notopodial lamellae on chaetiger 2 about half the size and similar in shape to those in chaetiger 3, notopodial lamellae on chaetiger 4 smaller and much more slender than those on chaetiger 3, approaching bottle-shape. Neuropodial lamellae largest on chaetigers 2–4; particularly large, blunt and oval on chaetiger 3 (Fig. 36b); on chaetiger 2 about half the size of those on chaetiger 3, squarish to rounded; on chaetiger 4 smaller than those on chaetiger 3, rounded.
Three pairs of branchiae observed on chaetigers 2–4; all smooth and cirriform; first pair of branchiae (= chaetiger 2) longest, surpassing the length of corresponding notopodial lamellae (Fig. 35e); the second and third pairs of branchiae extremely small, stubby. Dorsal ridges not confirmed.
Chaetae of three types: capillaries hooded hooks and sabre chaetae. Capillaries slender, narrowly bi-limbate and lightly granulated. The exact start of sabre chaetae uncertain, with first sabre chaeta observed in neuropodia of chaetiger 19; relatively slender with aristate tip, curved, limbate, granulation not observed (Fig. 36c). Hooded hooks singly from chaetiger 18; with 5 per fascicle in chaetiger 19; hooks with main fang and several small teeth, observed under light microscopy (Fig. 36d); with tight-fitting rounded hood and rudimentary secondary hood (Fig. 36d). Notopodial hooded hooks not observed in available fragments.
The rest of body and pygidium unknown.
Molecular information: Six 16S sequences from this species match five sequences from Prionospio sp. ‘29 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the 11 sequences range between 0.0 and 0.002, thus extending this species distribution to the GSR, Ifremer and IOM exploration areas in the Eastern CCZ. COI sequences match eight sequences from CCZ submitted to GenBank by Janssen et al. (2015) and labeled as Prionospio sp. with accession numbers KJ736496-KJ736500 and KJ736502-KJ736504.
Remarks: Although this species cannot be described in great detail and the consistency of the characters reported above is currently uncertain, it appears that this species belong to group of deep-sea Prionospio species with reduced number of branchiae (Paterson et al. 2016) and relatively posterior start of neuropodial hooks. Three pairs of branchiae of similar form were also recorded in ABYSSLINE species Prionospio sp. NHM_471 and in Prionospio branchilucida Altamira, Glover & Paterson in Paterson et al. (2016) previously described from CCZ and collected during Kaplan project. See also Remarks under Prionospio sp. NHM_471.
Distribution: This species is known from UK-1, OMS-1, GSR, Ifremer, and IOM exploration contract areas in the eastern CCZ.
Prionospio sp. NHM_266
Fig. 37a–e
Prionospio sp. NHM_266, specimen NHMUK.ANEA.2019.10007. a Fragmented preserved specimen, anterior fragment in dorsal view, specimen retaining faint Shirlastain; b anterior end in dorsal view; c detail of notopodial lamellae on chaetigers 2–5, with short branchiae on chaetigers 3–4 and dorsal crest on chaetiger 5 visible; d specimen in lateral view, showing parapodial lamellae of chaetigers 5–7; e neuropodial hooded hooks. Scale bars: a, b 1 mm
Material examined: NHM_227, NHMUK ANEA.2019.10005, coll. 15 Oct. 2013, collection method: Remotely Operated Vehicle, 13°57.880N, 116°32.993W, 4072 m; NHM_301, NHMUK ANEA.2019.10007, coll. 17 Oct. 2013, collection method: USNEL Box Core, 13°45.726N, 116°27.825W, 4110 m; NHM_302, NHMUK ANEA.2021.44, coll. 17 Oct. 2013, collection method: USNEL Box Core, 13°45.726N, 116°27.825W, 4110 m; NHM_266, NHMUK ANEA.2019.10006, coll. 17 Oct. 2013, collection method: Brenke Epibenthic Sledge, 13°45.21N, 116°29.12W, 4128 m; NHM_582, NHMUK ANEA.2019.10014, coll. 17 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°23.17456N, 116°32.92021W, 4202 m; NHM_1797F, NHMUK ANEA.2019.10046, coll. 11 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°10.43N, 117°11.57W, 4045 m; NHM_886, NHMUK ANEA.2019.10023, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m; NHM_1343, NHMUK ANEA.2019.10033, coll. 01 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°15.44N, 117°18.13W, 4302 m.
Description. Medium-sized species represented by four posteriorly incomplete specimens and several body fragments. The best example is specimen NHM_301, now in three fragments (Fig. 37a): anterior fragment with 10 chaetigers measuring 3.7 mm long, 0.9 wide (at chaetiger 1) and two body fragments with 20 and approximately 10 discernable chaetigers respectively. Preserved specimens whitish in alcohol, with faint brown pigmentation around prostomial caruncle (Fig. 37b). Prostomium long, bottle-shaped with broadly rounded anterior margin (Fig. 37b); slender caruncle extending to anterior margin of chaetiger 2. Eyes not observed. Peristomium well developed, encircling prostomium closely like a collar, partially fused to chaetiger 1, forming low lateral wings (Fig. 37b).
Four pairs of branchiae present on chaetigers 2–5, with first and fourth pair lost in all available specimens. Branchial pairs 2 and 3 short, fleshy, triangular and laterally ciliated; both pairs slightly shorter than accompanying notopodial lamellae, in dorsal view both pairs covered by enlarged notopodial lamellae (Fig. 37c).
Anterior notopodial lamellae well developed, particularly enlarged in branchial chaetigers and largest on chaetigers 3 and 4 (Fig. 37c); triangular and elongated; from chaetiger 6 increasingly smaller and wider (Fig. 37d), becoming subquadrate with somewhat produced dorsal tip; in the available 20 chaetiger long body fragment notopodial lamellae low, flattened. Low dorsal crests from chaetiger 5 (Fig. 37b, c), till end of anterior fragment and also observed on most chaetigers of the 20 chaetiger long body fragment. Neuropodial lamellae small on chaetiger 1, largest on branchial chaetigers, then gradually becoming reduced in size; lamellae on chaetigers 2–4 fan-shaped (rhomboid) with rounded corners to slightly developed blunt ventral tip; then becoming progressively smaller and low (form not known from around chaetiger 30 due to damage of specimen). Interparapodial pouches absent.
Both notopodia and neuropodia in anterior region with capillaries arranged in three to four irregular rows. Capillaries slender, smooth and narrowly bi-limbate. Sabre chaetae and neuropodial hooks start around chaetiger 18 (observed on body fragments only, none found in 10 chaetiger long anterior fragment). Sabre chaetae long, slender, gently curved, with distal half lightly granulated, up to 2 per fascicle. Neuropodial hooks up to 8 per fascicle; long, slender, with angular, inflated primary hood and striated secondary hood; shaft very constricted just below multidentate “head”, with several small teeth, without particularly pronounced main fang (Fig. 37e). Notopodial hooks not present in available fragments. The mid body, posterior chaetigers and pygidium unknown.
Molecular information. Ten 16S sequences from this species match four sequences from Prionospio sp. ‘14 PB’ (Bonifácio et al. 2020), the uncorrected (p) distances among the 14 sequences range between 0.0 and 0.006. This group of sequences is very similar to its sister taxon (Fig. 6), Prionospio sp. NHM_884, with uncorrected (p) distances in 16S ranging between 0.028 and 0.03. In the phylogenetic tree (Fig. 6), the clade with these two taxa also contains Prionospio cf. amarsupiata, and the uncorrected (p) distance to this taxon is equally low, 0.028.
Molecular data suggest close relationship of ABYSSLINE collected specimens to Prionospio cf. amarsupiata. It is important to note that the published sequences linked to P. amarsupiata by Paterson et al. (2016) were obtained from Crozet Island (abyssal South Atlantic) specimens and not from type locality (Setubal Canyon, NE Atlantic, 4482 m). Thus, we suggest here that Crozet Island specimens are assigned to Prionospio cf. amarsupiata rather than Prionospio amarsupiata. However, as supported by both molecular (this study; Guggolz et al. 2020) and morphological observations (this study, Paterson et al. 2016), P. cf. amarsupiata appears to be widely distributed in the abyss.
Remarks. Specimens collected from CCZ during Kaplan project were morphologically considered to belong to P. amarsupiata by Neal & Altamira in Paterson et al. (2016). ABYSSLINE specimens correspond well to P. amarsupiata in shape of prostomium, form of anterior parapodial lamellae, relatively late start of hooded hooks and their form, the presence of low dorsal crest from chaetiger 5 and lack of neuropodial genital pouches (see also discussion of P. amarsupiata in Paterson et al. 2016). However, one of the main diagnostic characters – the form of branchiae, cannot be compared as first and fourth pairs of branchiae have been lost in all ABYSSLINE-collected specimens. Therefore, as a precaution we assigned these specimens to Prionospio. cf. amarsupiata till better preserved specimens become available (see also Molecular information).
In addition, another ABYSSLINE collected species—Prionospio sp. NHM_884—has shown both morphological and molecular affinities to P. amarsupiata. For further details, see Remarks section of Prionospio sp. NHM_884.
Distribution: This species has here been recorded from the eastern CCZ (UK-1, OMS-1, GSR and Ifremer areas). Previously this species has been reported from wider CCZ (Kaplan project).
Prionospio sp. NHM_884
Prionospio sp. NHM_884, showing specimen NHMUK.ANEA.2019.10022 unless stated otherwise a preserved specimen in dorsal view; b detail of anterior end, showing the pigmentation; e–g live, preserved and stained with Shirlastain specimen NHMUK.ANEA.2019.10019 in dorsal view. Scale bars: 1 mm
Comparison of neuropodial hooded hooks a neuropodial hooded hooks of Prionospio sp. NHM_884; b neuropodial hooded hooks of Prionospio amarsupiata from Paterson et al. (2016); c neuropodial sabre chaetae of Prionospio sp. NHM_884. Scale bars: a, c 25 μm; b 10 μm
Material examined: NHM_736, NHMUK ANEA.2019.10019, coll. 20 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°32.23N, 116°36.25W, 4425 m; NHM_884, NHMUK ANEA.2019.10022, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m; NHM_943, NHMUK ANEA.2019.10025, coll. 23 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°34.28N, 116°36.63W, 4198 m.
Description: small species represented by three posteriorly incomplete specimens. The best example is specimen NHM_844, measuring 2.2 mm long, 0.7 mm wide (at chaetiger 1) for 17 chaetigers (Fig. 38a–c). Live specimens (NHM_736) observed, 3.1 mm long, 0.5 mm wide for about 20 discernable chaetigers) translucent, with pale blue hues, distinct rusty pigmentation around prostomial caruncle, with orange to brown gut (Fig. 38e); preserved specimens pale yellow in alcohol, with distinct dark rusty pigmentation around prostomial caruncle (Fig. 38a, b, f). Prostomium angular, anteriorly truncated (Fig. 38b), with slender caruncle extending to anterior margin of chaetiger 2. Eyes not observed. Peristomium well developed, encircling prostomium closely like a collar, partially fused to chaetiger 1, forming low lateral wings (Fig. 38b).
Four pairs of branchiae present on chaetigers 2–5, with first and fourth pair lost in all specimens. Branchial pairs 2 and 3 short, somewhat stubby, cirriform (Fig. 38c, g).
Anterior notopodial lamellae well-developed in all observed chaetigers, but particularly enlarged in branchial chaetigers and largest on chaetigers 3 and 4 (Fig. 38c, d, g); triangular and elongated, from chaetiger 6 increasingly smaller, wider, conical with broadly rounded tip. Low dorsal crests from chaetiger 6 (Fig. 38g), till end of the fragment. Neuropodial lamellae small on chaetiger 1, largest on branchial chaetigers, then gradually becoming reduced in size; lamellae on chaetiger 2–4 fan shaped with rounded corners to slightly developed blunt ventral tip; then becoming rounded and smaller, particularly low past chaetiger 15. Interparapodial pouches absent.
Both notopodia and neuropodia in anterior region with capillaries arranged in two rows of longer and short chaetae. Capillaries slender, smooth and narrowly bi-limbate. Sabre chaetae and neuropodial hooks start on chaetiger 17. Sabre chaetae stout, gently curved and heavily granulated, up to 2 per fascicle (Fig. 39c). Neuropodial hooks long, slender, with angular, primary hood (Fig. 39a); the presence of secondary hood uncertain; shaft very constricted just below very small multidentate “head” (difficult to observe even under high magnification), with several very small teeth, no main fang detected (Fig.38a); five per fascicle observed. Notopodial hooks not present in available anterior fragments. The mid body, posterior chaetigers, and pygidium unknown.
Molecular information. Three 16S sequences obtained from this species do not match any other sequences, the uncorrected (p) distance among the three sequences range from 0.0 to 0.002. However, this group of sequences is very similar to its sister taxa in the tree (Fig. 6), Prionospio sp. NHM_266, with uncorrected (p) distances in 16S ranging between 0.028 and 0.03. In the tree (Fig. 6), the clade with these two taxa also contains Prionospio cf. amarsupiata, and the uncorrected (p) distance to this taxon is equally low, 0.028.
Remarks. Molecular data suggest close relationship of Prionospio sp. NHM_884 with Prionospio amarsupiata as well as another ABYSSLINE collected specimens assigned to Prionospio sp. NHM_266 (= cf. amarsupiata) (Fig. 6). Morphologically, these species are similar in the shape of anterior parapodial lamellae, relatively posterior start of hooded hooks and their form (Figs 36e, 38a, b), the presence of low dorsal crest and lack of neuropodial genital pouches (see also discussion of P. amarsupiata in Paterson et al. 2016). The main differences observed are the shape of prostomium, which is anteriorly rounded and bottle shaped in P. amarsupiata and Prionospio sp. NHM_226 (Fig. 37b) but distinctly truncated in Prionospio sp. NHM_884 (Fig. 38b) and possession of four, not two rows of capillaries in anterior notopodia in P. amarsupiata. However, the main diagnostic characters—the form of branchiae, cannot be compared as first and fourth pairs of branchiae have been lost in all ABYSSLINE specimens.
Distribution. This species is only known from UK-1 exploration contract area in the eastern CCZ.
Spiophanes Grube, 1860
Spiophanes sp. NHM_1897
Fig. 40a–d
Preserved specimens of Spiophanes sp. NHM_1897, specimen NHMUK. ANEA.2021.46 in a lateral view and b dorsal view; c–d specimen NHMUK.ANEA.2021.47 in dorsal view. Scale bars: 1000 μm
Material examined: NHM_1897, NHMUK ANEA.2021.46, coll. 13 Mar. 2015, collection method: Brenke Epibenthic Sledge, 12°02.49N, 117°13.03W, 4094 m; NHM_3186, NHMUK ANEA.2021.47, coll. 24 Feb. 2015, collection method: Brenke Epibenthic Sledge, 12°08.02N, 117°17.52W, 4122 m.
Description: This species is represented by two anterior fragments (Fig. 40a–d), consistent with genus Spiophanes due to presence of modified hooks in chaetiger 1 and absence of branchiae.
Molecular information: The 16S sequences from this species did not match any other available sequences. The COI sequence from this species matched five previously published sequences from the CCZ and labeled as Spiophanes sp. (Janssen et al. 2015, GenBank accession numbers KJ736657–KJ736661), with uncorrected (p) values ranging from 0.0 to 0.02. The COI sequence also matches a recently described species from the Adriatic Sea, Spiophanes adriaticus, D'Alessandro, Castriota, et al. (2020) (GenBank accession number MT177912) with uncorrected (p) value between the species of 0.017.
Remarks: This species is currently studied by Karin Meissner (Meissner pers. comm.). Therefore, we only report this species as present in ABYSSLINE material for the completeness of Spioniformia species checklist.
Distribution: This species is known from the eastern CCZ and was found in the OMS-1 contract area and previously also in the BGR contract area (Janssen et al. 2015).
Discussion
This study has added 25 annelid species, two of those formalized, and 98 records to the knowledge of the benthic annelid macrofauna of the CCZ, bringing a published record from the ABYSSLINE (UK-1 and OMS) investigated areas to 48 polychaete species, with 15 formalized (see also Wiklund et al. 2019; Drennan et al. 2021). Additional studies to either provide taxonomic data for or to formalize remaining ABYSSLINE polychaetes are currently underway by the authors.
It is well known that Spionidae are well represented in sediment infauna, both in terms of abundance and species richness in shallow water and deep sea, including the CCZ area (e.g., Glover et al. 2002; Paterson et al. 2011, 2016). Although Spionidae represent a species rich group within Annelida, interestingly, its ca. 40 genera tend to be reduced to only four, commonly encountered in the deep-sea samples—Aurospio, Prionospio, Laonice, and Spiophanes (Neal pers. obs.)—as also mirrored in this study. Of those, Prionospio and the allied Aurospio tend to be particularly abundant and species rich in the deep sea (e.g., Paterson et al. 2016; Guggolz et al. 2020; Peixoto and Paiva 2020). Unfortunately, the discovery and description of this great diversity tends to be compromised by two problems, a poor definition of Prionospio and related taxa and the poor preservation and easy fragmentation of available specimens. Such issues were also encountered here preventing a formal description of several new species. Furthermore, as already observed by Paterson et al. (2016) the main diagnostic character of Prionospio—the branchiae not only tend to be lost due to damage in deep-sea specimens, but even if observed, they tend to have reduced morphology compared to shallow waters species (i.e., <4 branchial pairs or even absence of branchiae is commonly seen, pinnules are often absent etc.). Therefore, the search for characters that would reliably identify deep-sea Prionospio is greatly dependent on specimens in pristine condition, which are currently lacking.
Owing to the paucity and unreliability of morphological characters, molecular data gain even more importance for species identification and estimation of species ranges. Molecular data on Spionidae mimic the now well-established pattern of molecular data revealing the presence of more species than what can be established based on morphology alone, commonly known as cryptic diversity (Knowlton 1993). The diversity is not necessarily 100% cryptic, but careful examination of new material is needed to establish the presence of new and previously overlooked characters. We have highlighted some of these issues in the Remarks section of certain taxa, particularly Aurospio dibranchiata—long considered a deep-sea “cosmopolitan” species, a view now challenged by molecular data.
Studies of annelid species’ ranges in the deep sea in general and CCZ in particular as estimated from molecular data are still in their infancy. At present, many of abyssal annelid taxa, including those from CCZ appear to have a restricted distribution. Bonifácio et al. (2020) showed that 49% of CCZ polychaete species had their distribution limited to the single investigated area, a pattern also observed for CCZ tanaid crustaceans (Błazewicz et al. 2019). Nevertheless, such patterns may change with the increased future sampling and analytical efforts from other CCZ areas as well as other deep-sea regions. Only nine out of 25 species in this study have been found in a single area only and these were usually represented by singletons. Fifteen out of 25 species reported here have been found distributed across at least the eastern CCZ. Interestingly, two spionid species, Prionospio cf. amarsupiata and Aurospio sp. NHM_2186 (one of A. dibranchiata-like species), may truly be considered cosmopolitan, although more data is needed. Guggolz et al. (2020) analyzed a relatively large deep-sea molecular Prionospio and Auropsio dataset and reported that seven out of 21 lineages had pan-oceanic distributions, suggesting that high dispersal abilities may be due to free-swimming long-lived planktonic larval stages. Such findings are not unique to Spionidae though, with several other annelid taxa reported to have a wide distribution as supported by molecular data (Ahrens et al., 2013; Eilertsen et al. 2018; Georgieva et al. 2015; Neal et al. 2018). In fact, a recent review of genetic studies of deep-sea taxa revealed a general pattern of greater connectivity over long distances at similar depths, rather than across depth (Taylor and Roterman 2017). Contrary to this pattern, we found Spiophanes COI sequences from the CCZ matching a shallow water species from the Mediterranean (Spiophanes adriaticus). Such a result is difficult to explain, particularly as the two species are not morphologically similar and the validity of the Mediterranean species has been recently questioned (Jourde et al. 2020). Thus, distribution results based on single gene analyses must be scrutinized carefully. In our Spiophanes case, nine single base mutations among 593 bp resulted in five amino acids differences between the two species. This is an important result as it shows that using only COI sequences, as is common in, e.g., metabarcoding studies, could be potentially misleading.
Lastly, the molecular data presented here enable us to comment on phylogenetic relationships within Spioniformia (Fig. 6). Although both Poecilochaetidae and Trochochaetidae are currently considered valid (Read and Fauchald 2018, 2019), these spioniform monogeneric families have a confused history and their status is yet to be resolved. Their close relationship to Spionidae has long been recognized, even though Mesnil (1897) formed a separate family Disomidae to accommodate Disoma mulisetosum described by Örsted (1844). Problematic systematics of Disoma multisetosum (now Trochochaeta multisetosa) achieved some stabilization following the decision of Pettibone (1963) to establish the new family Trochochaetidae (see Radashevsky et al. 2018 for details). The family Poecilochaetidae was established by Hannerz (1956) for Poecilochaetus species due to larval differences, as it was argued that divergences in the formation of the prostomium and the peristomium and the prototroch differentiate Poecilochaetus from Disoma.
In recent decades, most works treated Poecilochaetidae and Trochochaetidae as two valid monogeneric families, although there were exceptions (Rouse and Pleijel 2006; Radashevsky et al. 2018). The phylogenetic approach to this question has so far been limited. Cladistic analysis of Blake and Arnofsky (1999) based on morphological and reproductive data suggested that the status of Trochochaetidae and Poecilochaetidae should be re-considered as these were recovered within Spionidae. Similarly, the inclusion of Trochochaetidae and Poecilochaetidae within Spionidae has been supported by Hausen (2007), due to presence and structure of light-sensitive organs within the prostomium. Eibye-Jacobsen’s (2005) cladistic analysis concentrated solely on the relationships within Poecilochaetidae, using Trochochaetidae and Apistobranchidae (but not Spionidae) as an outgroup. Molecular approaches that included Poecilochaetidae and Trochochaetidae to date have been of limited value, as these were higher level phylogenies, often including only one representative per family (e.g., Struck et al. 2007; Zrzavý et al. 2009) or family specific. Very recently, while investigating relationships of horned Spiophanes species, Radashevsky et al. (2020) recovered Trochochaeta as a sister group to Spiophanes. Our molecular results based on Bayesian analysis of 102 spioniform taxa and three genes (CO1, 16S, 18S) (Fig. 6, Table 1, Supplementary materials 1 and 2) are in agreement with those of Radashevsky et al. (2020). Therefore, our molecular data provide further support for the inclusion of both Poecilochaetidae and Trochochaetidae within Spionidae, although the position of Poecilochaetus within Spionidae was unresolved.
To summarize, despite the recent efforts, there are still few DNA sequences for benthic faunal groups from the CCZ available on GenBank, mainly restricted to echinoderms (Glover et al. 2016a), cnidarians (Dahlgren et al. 2016), molluscs (Wiklund et al. 2017), annelids (Bonifácio and Menot 2019; Janssen et al. 2015; Wiklund et al. 2019; Guggolz et al. 2020), Porifera (Lim et al. 2017), and crustaceans (Janssen et al. 2015). Although the morphological data presented here are limited for most species due to their poor condition, it is our hope that the accompanying molecular data may ease identification in future surveys and better-preserved specimens may become available with further sampling. The information presented here therefore represents a further step in improving our understanding of benthic fauna from the CCZ area, which in turn is essential for informing conservation efforts, as well as providing future practical identification guides to the fauna of this region.
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
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Acknowledgments
We thank the masters, crew, and technical staff on the RV Melville and RV Thomas G Thompson for their outstanding support. We acknowledge the expert leadership of the research cruises and ABYSSLINE project by Prof Craig R Smith, University of Hawaii. We acknowledge the continued support from the NHMUK Consultancy team (Harry Rousham, Robyn Fryer, Kate Rowland). We received help sorting and sieving samples at sea from Magdalena Georgieva and Madeleine Brasier, and the entire ABYSSLINE science team in successful deep-sea coring operations. Finally, we would like to thank to two anonymous reviewers who helped to improve this publication.
Funding
This study was funded by UK Seabed Resources Ltd, Contract No. SRD100200 (NHM) & Contract No. SRD100500 (NORCE) and Norwegian Research Council (JPIO MiningImpact2, Grant #290931).
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The first author, LN, led the morphological investigation of the specimens used in this study and led the publication. HW collected the specimens and was responsible for the molecular study of the specimens. MR collected the specimens and compiled the DarwinCore database. TGD and AGG conceptualized the research and collected the specimens. All authors contributed to the writing of the manuscript.
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AGG and TGD have received research grants from UK Seabed Resources Ltd, the Metals Company, NOAA and the Moore Foundation. AGG has received research grants from the Pew Foundation.
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All applicable international, national, and/or institutional guidelines for use of animals were followed by the authors.
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All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.
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Communicated by T. Horton
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Neal, L., Wiklund, H., Rabone, M. et al. Abyssal fauna of polymetallic nodule exploration areas, eastern Clarion-Clipperton Zone, central Pacific Ocean: Annelida: Spionidae and Poecilochaetidae. Mar. Biodivers. 52, 51 (2022). https://doi.org/10.1007/s12526-022-01277-1
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DOI: https://doi.org/10.1007/s12526-022-01277-1