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Dr. Chong CHEN

Dr. Chong CHEN

Deep-sea biologist. Malacologist. Evolutionary biologist. "Mollusc collector", photographer.

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Gallery of Publications

Our new paper on deep-sea true limpets in the enigmatic family Neolepetopsidae is now published in Zoological Journal of Linnean Society! In addition to describing three new species, we present the first molecular phylogeny that includes all genera in the family. This supported monophyly of the genera, and shed light on a potential ‘stepping-stone’ evolutionary pathway from organic falls to hot vents in the family. The paper is available here: https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zlab081/6408716<br />
Please let me know if you would like a PDF copy. <br />
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Abstract<br />
Neolepetopsidae is a family of true limpets restricted to deep-sea chemosynthesis-based ecosystems. It is a small and little-studied family with about a dozen species in three genera, namely Eulepetopsis, Neolepetopsis and Paralepetopsis, and all named species were from the Pacific or Atlantic Oceans. Here, we describe three new species from Indian Ocean vents, namely Eulepetopsis crystallina sp. nov. found across three ridges, Neolepetopsis ardua sp. nov. from the Southwest Indian Ridge and Neolepetopsis prismatica sp. nov. from the Carlsberg Ridge. Given that Neolepetopsis appears to specialize on inactive sulfide deposits, the apparent wider distribution of E. crystallina is probably attributable to bias in sampling effort at inactive chimneys. The molecular phylogeny of Patellogastropoda, reconstructed using the COI gene, supported the monophyly of Neolepetopsidae. These are the first molecular data available for Neolepetopsis, confirming that the three genera are genetically distinct. Eulepetopsis appears to be adapted to active vents, and its derived position compared with Paralepetopsis indicates a possible ‘stepping-stone’ evolutionary pathway from seeps and organic falls to vents. Our results provide new insights into this enigmatic family and highlight the importance of surveying the vent periphery, especially given that inactive vents are being eyed as a replacement for active ones in deep-sea mining.<br />
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Chen C*, Zhou Y*, Watanabe HK, Zhang R, Wang C (2021). Neolepetopsid true limpets (Gastropoda: Patellogastropoda) from Indian Ocean hot vents shed light on relationships among genera. Zoological Journal of the Linnean Society, zlab081. DOI: 10.1093/zoolinnean/zlab081
Our new paper in Molecular Biology and Evolution led by Ting Xu unravels demographic history and population connectivity of the deep-sea limpet Bathyacmaea nipponica across hot vents and cold seeps, using a genome-wide set of genetic markers consisting of nearly 10000 single nucleotide polymorphisms (SNPs) and supplemented by physical ocean modeling! The paper is *open access* and available for free here: https://doi.org/10.1093/molbev/msab278<br />
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Abstract: <br />
Hydrothermal vents and hydrocarbon seeps in the deep ocean are rare oases fueled by chemosynthesis. Biological communities inhabiting these ecosystems are often distributed in widely separated habitats, raising intriguing questions on how these organisms achieve connectivity and whether habitat types facilitate intraspecific divergence. The deep-sea patellogastropod limpet Bathyacmaea nipponica that colonizes both vents and seeps across ∼2,400 km in the Northwest Pacific is a feasible model to answer these questions. We analyzed 123 individuals from four vents and three seeps using a comprehensive method incorporating population genomics and physical ocean modeling. Genome survey sequencing and genotyping-by-sequencing resulted in 9,838 single-nucleotide polymorphisms for population genomic analyses. Genetic divergence and demographic analyses revealed four habitat-linked (i.e., three seep and one vent) genetic groups, with the vent genetic group established via the opportunistic invasion of a few limpet larvae from a nearby seep genetic group. TreeMix analysis uncovered three historical seep-to-vent migration events. ADMIXTURE and divMigrate analyses elucidated weak contemporary gene flow from a seep genetic group to the vent genetic group. Physical ocean modeling underlined the potential roles of seafloor topography and ocean currents in shaping the genetic connectivity, contemporary migration, and local hybridization of these deep-sea limpets. Our study highlighted the power of integrating genomic and oceanographic approaches in deciphering the demography and diversification of deep-sea organisms. Given the increasing anthropogenic activities (e.g., mining and gas hydrate extraction) affecting the deep ocean, our results have implications for the conservation of deep-sea biodiversity and establishment of marine protected areas.<br />
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Xu T, Wang Y, Sun J, Chen C, Watanabe HK, Chen J, Qian P-Y*, Qiu J-W* (2021). Hidden historical habitat-linked population divergence and contemporary gene flow in a deep-sea patellogastropod limpet. Molecular Biology and Evolution, Advance Article msab278. DOI: 10.1093/molbev/msab278
Ever wondered what the deep sea sounds like? Our new paper in Limnology and Oceanography presents results from analysing soundscapes from four deep-sea habitats including a hydrothermal vent and the abyssal plain, recorded using pressure-resistant hydrophones! OPEN ACCESS: https://aslopubs.onlinelibrary.wiley.com/doi/full/10.1002/lno.11911<br />
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All audio data used are freely available on Depositar: https://data.depositar.io/en/dataset/deep-sea-soundscapes-of-japan<br />
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Abstract: <br />
Underwater soundscapes, though invisible, are crucial in shaping the biodiversity of marine ecosystems by acting as habitat-specific settlement cues for larvae. The deep sea has received little attention in soundscape research, but it is being targeted for mineral extraction to feed the ever-growing needs of our society. Anthropogenic impacts on soundscapes influence the resilience of key shallow-water habitats, and the same likely applies to the deep. Japan is a forerunner in deep-sea mining, but virtually no deep soundscape baselines exist for Japanese waters. Here, we report baseline soundscapes from four deep-sea locations in Japan, including the Suiyo Seamount hydrothermal vent, the abyssal plain around the Minamitorishima Island home to manganese nodule fields and muds rich in rare-earth elements, twilight depths off Sanriku, as well as a typical bathyal system in Suruga Bay. Long-duration audio recordings were visualized and factorized by an unsupervised machine learning model, revealing differing characteristics among the habitats. Two locations near the coast are highly influenced by shipping noise. The Suiyo vent is characterized by low-frequency sounds from venting, and the abyssal Minamitorishima is quiet with a flat spectral shape. Noise from observation platforms is likely sufficient to alter soundscape characteristics, especially in offshore locations, suggesting offshore mining-targeted areas are susceptible to impacts from anthropogenic noise. We argue that the monitoring of soundscapes is an indispensable component for assessing potential mining impacts on deep-sea ecosystems. Our results establish reference points for future soundscape monitoring and assessment in Japanese waters as well as similar ecosystems globally.<br />
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Chen C# / Lin T-H#*, Watanabe HK, Akamatsu T, Kawagucci S (2021). Baseline soundscapes of deep-sea habitats reveal heterogeneity among ecosystems and sensitivity to anthropogenic impacts. Limnology and Oceanography, Early View: 1-14. DOI: 10.1002/lno.11911
In February 2021 we visited the deep seabed in Sagami Bay, Japan with a remotely operated vehicle, and here's a paper reporting some interesting (mollusc-related) finds from the cruise. Among other things, we report the first evidence for living naticid snails feeding on seep vesicomyid clams, previously only seen in fossils. Read for free here: https://rdcu.be/cpeeE<br />
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Abstract: <br />
Sagami Bay is among the most surveyed areas in Japan and the northwestern Pacific for marine biodiversity, partly owing to collecting efforts by the Showa Emperor, Hirohito. It was also here that the first chemosynthesis-based community was found in Japan, in the Off Hatsushima hydrocarbon seep site dominated by large vesicomyid clams. Nevertheless, new discoveries continue to be made in the deep. Here, we report observations of rare bathyal gastropods from unusual habitats. From the Off Hatsushima seep, the calliostomatid snail Otukaia kiheiziebisu was found living on tubeworm, the second record of the family from seeps. The cocculinid limpet Cocculina tenuitesta, previously only known from Suruga Bay, was found on a piece of branch-like plant debris inside the actively seeping clam field. This supports the step-wise evolutionary scenario from organic falls to hot vents recently suggested for this family. The predatory naticid snail Cryptonatica affinis represents the second record for the family at seeps, and we also show the first evidence for naticids feeding on chemosymbiotic clams—a phenomenon formerly only known from fossil seeps. We also found live individuals of Provanna stephanos, hitherto known from just two empty shells. Outside the seep area, the lepetid true limpet Sagamilepeta sagamiensis was found living on plastic debris, highlighting the function of plastic in the deep sea as settlement substrates among the muddy expanse. Our observations here have ecological and evolutionary implications, underscoring how much remains to be learned from the deep sea, even in well-studied areas like Sagami Bay.<br />
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Chen C*, Nomaki H (2021). Noteworthy observations and records of rare bathyal gastropods from unusual habitats in Sagami Bay, Japan. Marine Biodiversity, 51: 66. DOI: 10.1007/s12526-021-01212-w
Our new paper in Journal of Natural History presents Lirapex felix, a new species of peltospirid hydrothermal vent snail from the Indian Ocean! Only known from two specimens taken on a single chimney structure in the Longqi vent field despite considerable sampling efforts, it appears to be a rare species. The specific epithet 'felix' means 'lucky, happy, or blessed' in Latin, named in reference to the fortunate finding of a second specimen that allowed for a comprehensive description.  <br />
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Abstract: <br />
The biodiversity of deep-sea hydrothermal vents in the Indian Ocean remains poorly characterised compared with that of their Pacific and Atlantic counterparts. Although the Longqi hydrothermal vent field is the most extensively explored vent site on the ultra-slow-spreading Southwest Indian Ridge, it is still a source of new discoveries. Here, we report and formally describe a new peltospirid snail from Longqi – Lirapex felix sp. nov. Known from only two specimens, it differs from other named Lirapex species by a depressed spire and the lack of coil loosening on the body whorl. Examinations of the external anatomy and radular characteristics agree with its placement in Lirapex, which is also supported by a molecular phylogeny reconstructed using the barcoding fragment of the mitochondrial cytochrome c oxidase I (COI) gene. This is the fifth peltospirid snail known to inhabit the Longqi field, three of which (including Lirapex felix sp. nov.) have been found nowhere else. There is growing evidence that the Longqi field represents a biogeographically unique site among Indian Ocean vents. The discovery of Lirapex felix sp. nov. adds to the unique biodiversity of Longqi field, with implications for conservation in the light of potential deep-sea mining.<br />
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Chen C*, Han Y, Copley JT, Zhou Y* (2021). A new peltospirid snail (Gastropoda: Neomphalida) adds to the unique biodiversity of Longqi vent field, Southwest Indian Ridge. Journal of Natural History, 55 (13-14): 851-866. DOI: 10.1080/00222933.2021.1923851
Co-authored paper just published in Marine Pollution Bulletin reveals the main source of coral erosion in Hong Kong is grazing by sea urchins, through a two years deployment experiment of coral blocks followed 3D reconstruction and quantification. Read for free here: https://authors.elsevier.com/a/1d8VY,ash%7ER7k<br />
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Abstract: <br />
Erosion of coral substrate plays a crucial role in reef calcium carbonate budget, but little is known about erosion in subtropical corals. In a 2-year study of coral substrate erosion, we deployed Porites skeletal blocks at nine sites across subtropical Hong Kong waters. External erosion varied from 0.05 to 3.07 kg m−2 yr−1 and accounted for 23.4–99.2% of the total erosion. More than half of the study sites had substantial external erosion (> 1 kg m−2 yr−1), and the values were positively correlated with density of the sea urchin Diadema setosum. Excluding urchins from access to the skeletal blocks using cages reduced external erosion by more than 90%. Overall, our study revealed that external erosion caused by urchin grazing contributed predominantly to the total coral skeletal loss in Hong Kong waters. Control of sea urchin population is needed to reduce coral erosion in places with high urchin density. <br />
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Yeung YH# / Xie JY#, Zhao Y, Yu HY, Chen C, Lu WW, Qiu J-W* (2021). Rapid external erosion of coral substrate in subtropical Hong Kong waters. Marine Pollution Bulletin, 169: 112495. DOI: 10.1016/j.marpolbul.2021.112495
Evolutionary relationships among major molluscan lineages remain contested, yet the (small) pool of molluscan genomes made available to date presents a non-optimal dataset for phylogenomic inferences. Our article presenting a guide for selecting useful taxa in currently under-represented groups in order to better understand the molluscan tree of life, led by Julia Sigwart, is now out in Philosophical Transactions of the Royal Society B: Biological Sciences. Link to the article: https://royalsocietypublishing.org/doi/10.1098/rstb.2020.0161<br />
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This paper is part of a special issue arising from the Theo Murphy international scientific meeting “Pearls of wisdom: synergising leadership and expertise in molluscan genomics” organised by Dr Angus Davison and Dr Maurine Neiman in 2019, which we participated in: https://royalsociety.org/science-events-and-lectures/2019/09/pearls-of-wisdom/<br />
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Abstract: <br />
The extraordinary diversity in molluscan body plans, and the genomic mechanisms that enable it, remains one of the great questions of evolution. The eight distinct living taxonomic classes of molluscs are each unambiguously monophyletic; however, significant controversy remains about the phylogenetic relationships among those eight branches. Molluscs are the second-largest animal phylum, with over 100 000 living species with broad biological, economic and medical interest. To date, only around 53 genome assemblies have been accessioned to NCBI GenBank covering only four of the eight living molluscan classes. Furthermore, the molluscan taxa where partial or whole-genome assemblies are available are often aberrantly fast evolving or recently derived lineages. Characteristic adaptations provide interesting targets for whole-genome projects, in animals like the Scaly-foot Snail, or octopus, but without basal-branching lineages for comparison, the context of recently derived features cannot be assessed. The currently available genomes also create a non-optimal set of taxa for resolving deeper phylogenetic branches: they are a small sample representing a large group, and those that are available come primarily from a rarefied pool. Thoughtful selection of taxa for future projects should focus on the blank areas of the molluscan tree, which are ripe with opportunities to delve into peculiarities of genome evolution, and reveal the biology and evolutionary history of molluscs.<br />
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Sigwart JD*, Lindberg DR, Chen C, Sun J (2021). Molluscan phylogenomics requires strategically selected genomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 376 (1825): 20200161. DOI: 10.1098/rstb.2020.0161
Our paper just out in Philosophical Transactions of the Royal Society B: Biological Sciences led by Jin Sun benchmarks various genome assemblers based on Oxford Nanopore Technologies to test their efficiency in dealing with challenging molluscan genomes. This also resulted in much improved assemblies for the two genomes we used as models: Scaly-foot Snail Chrysomallon squamiferum and Hard-shelled Mussel Mytilus coruscus. Link to the article: https://royalsocietypublishing.org/doi/10.1098/rstb.2020.0160<br />
The accepted version is also available freely on bioRxiv: https://www.biorxiv.org/content/10.1101/2020.12.31.424979v1<br />
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This paper is part of a special issue arising from the Theo Murphy international scientific meeting “Pearls of wisdom: synergising leadership and expertise in molluscan genomics” organised by Dr Angus Davison and Dr Maurine Neiman in 2019, which we participated in: https://royalsociety.org/science-events-and-lectures/2019/09/pearls-of-wisdom/<br />
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Abstract: <br />
Choosing the optimum assembly approach is essential to achieving a high-quality genome assembly suitable for comparative and evolutionary genomic investigations. Significant recent progress in long-read sequencing technologies such as PacBio and Oxford Nanopore Technologies (ONT) has also brought about a large variety of assemblers. Although these have been extensively tested on model species such as Homo sapiens and Drosophila melanogaster, such benchmarking has not been done in Mollusca, which lacks widely adopted model species. Molluscan genomes are notoriously rich in repeats and are often highly heterozygous, making their assembly challenging. Here, we benchmarked 10 assemblers based on ONT raw reads from two published molluscan genomes of differing properties, the gastropod Chrysomallon squamiferum (356.6 Mb, 1.59% heterozygosity) and the bivalve Mytilus coruscus (1593 Mb, 1.94% heterozygosity). By optimizing the assembly pipeline, we greatly improved both genomes from previously published versions. Our results suggested that 40–50X of ONT reads are sufficient for high-quality genomes, with Flye being the recommended assembler for compact and less heterozygous genomes exemplified by C. squamiferum, while NextDenovo excelled for more repetitive and heterozygous molluscan genomes exemplified by M. coruscus. A phylogenomic analysis using the two updated genomes with 32 other published high-quality lophotrochozoan genomes resulted in maximum support across all nodes, and we show that improved genome quality also leads to more complete matrices for phylogenomic inferences. Our benchmarking will ensure efficiency in future assemblies for molluscs and perhaps also for other marine phyla with few genomes available.<br />
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Sun J, Li R, Chen C, Sigwart JD, Kocot K* (2021). Benchmarking Oxford Nanopore read assemblers for high-quality molluscan genomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 376 (1825): 20200160. DOI: 10.1098/rstb.2020.0160
Our revision of the sister-genera Chicomurex and Naquetia in Muricidae is now published in Novapex, as the 14th Special Issue (Hors Serie)! This includes a molecular phylogeny of Chicomurex, also providing genetic evidence to support some recently described species in the genus. A notable change in Naquetia is that we rehabilitate the name Naquetia annandalei (Preston, 1910), formally separating it from N. barclayi (Reeve, 1858). Many thanks go to Roland Houart and Chris Moe for involving me in this work. Please let me know if you would like to have a PDF copy of this paper. <br />
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Abstract:<br />
Twenty-four species of Muricidae are reviewed, 15 assigned to Chicomurex Arakawa, 1964 and 9 to Naquetia Jousseaume, 1880, two closely related genera. Each species is listed with the author's name(s), the date of description, the synonymy, the chresonymy, the distribution, the description and some comments; the chresonymy is only cited for misidentified figures in recent publications dealing with Muricidae. Each species is illustrated in colour with many specimens, while scanning electron micrographs are provided for the radulae. Photos of the protoconch are provided for most of the species as well as the spiral cord morphology. The type locality and the type material (holotype only) are noted for each name. In addition, a molecular phylogeny of Chicomurex is reconstructed from eight species using three mitochondrial genes (cytochrome oxidase c subunit I, 12S rRNA, and 16S rRNA). The phylogeny revealed three well supported clades within the monophyletic Chicomurex, the grouping of species being congruent with morphology (C. laciniatus complex, C. superbus complex, and C. gloriosus complex). Species sampled includes three recently described species C. lani Houart, Moe & Chen, 2014, C. globus Houart, Moe & Chen, 2015, and C. pseudosuperbus Houart, Moe & Chen, 2015; the specific status of these were assessed and found to be supported by genetic data.<br />
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Houart R*, Moe CO, Chen C* (2021). Living species of the genera Chicomurex Arakawa, 1964 and Naquetia Jousseaume, 1880 (Gastropoda: Muricidae) in the Indo-West Pacific. Novapex, 22 (HS14): 1-52.
Excited to present high-quality genomes of the deep-sea hot vent snail Gigantopelta aegis and its two symbiotic bacteria in our new paper, just out in Nature Communications! Gigantopelta, which I described in 2015, was previously thought to have only one symbiont. We have seen some signs of a potential second symbiont for a few years but without definitive evidence – now we finally pinned it down. Thanks go to the lead author Yi Lan and all co-authors, especially Jin Sun. The paper is Open Access: https://www.nature.com/articles/s41467-021-21450-7<br />
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Abstract:<br />
Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulphur oxidiser and a methane oxidiser. We assembled high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses revealed mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodelled its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulphur-oxidising gammaproteobacterial endosymbiont, showed that their sulphur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulphur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.<br />
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Lan Y, Sun J, Chen C, Sun Y, Zhou Y, Yang Y, Zhang W, Li R, Zhou K, Wong WC, Kwan YH, Cheng A, Bougouffa S, Van Dover CL, Qiu J-W, Qian P-Y* (2021). Dual symbiosis in the deep-sea hot vent snail Gigantopelta aegis revealed by its hologenome. Nature Communications, 12: 1165. DOI: 10.1038/s41467-021-21092-9 [Preprint available on bioRxiv, DOI: 10.1101/2020.09.23.308304]
New co-authored paper on deep-sea parchment worms (genus Phyllochaetopterus) inhabiting the Shinkai Seep Field – a 5700 m deep chemosynthesis-based ecosystem in the Mariana Trench – led by Hiromi Watanabe-Kayama is now published in Plankton and Benthos Research! We found three (apparently) cryptic lineages closely related to the Atlantic P. polus co-occurring in the same site, forming bushes on carbonate chimney structures. This paper is Open Access: https://www.jstage.jst.go.jp/article/pbr/16/1/16_B160103/_article/-char/en<br />
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Abstract:<br />
Phyllochaetopterus (Annelida: Chaetopteridae) is a diverse genus of tube-dwelling polychaetes found in a wide range of marine environments from subtidal to abyssal depths, including chemosynthesis-based ecosystems. The Shinkai Seep Field (SSF) is a serpentinite-hosted system in the Mariana Trench, where the deepest-known Phyllochaetopterus polychaetes inhabit the surfaces of brucite/carbonate chimneys. Despite all specimens collected from SSF being morphologically consistent with P. polus originally described from a deep-sea hot vent on the Mid-Atlantic Ridge, molecular barcoding using the mitochondrial cytochrome c oxidase subunit I (COI) gene revealed at least three cryptic lineages, none of which corresponded to P. polus. Phylogenetic reconstruction recovered P. polus embedded among the three SSF lineages, confirming their close relationship. These results warrant careful examination of Phyllochaetopterus from other regions using integrative taxonomy in order to understand its true diversity and pinpoint further taxonomically informative morphological characters.<br />
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Watanabe HK*, Chen C, Nishi E, Ohara Y (2021). Cryptic diversity of the tube-dwelling polychaete Phyllochaetopterus in the Shinkai Seep Field, Mariana Trench. Plankton and Benthos Research, 16(1): 73-77. DOI: 10.3800/pbr.16.73
Meet Vulcanolepas verenae, a new deep-sea stalked barnacle from a hydrothermal vent in the Mariana Trough and named in honour of the deep-sea biologist Verena Tunnicliffe! Our paper led by Hiromi Watanabe-Kayama and published in Marine Biodiversity describes this new species and discusses the feeding ecology of species currently assigned to genus Vulcanolepas. Read the paper for free here: https://rdcu.be/cdtgH<br />
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Abstract:<br />
A new species of deep-sea neolepadid stalked barnacle, Vulcanolepas verenae sp. nov., is described from Hafa Adai hydrothermal vent field in the Mariana back-arc basin, northwest Pacific. Vulcanolepas verenae sp. nov. is differentiated from other described species in the family morphologically by a mandible with a very small first tooth and small, non-protruding peduncular scales. Its gross external morphology exhibits a range of plasticity, similar to those previously reported from other neolepadid stalked barnacles. This is the first report of the genus Vulcanolepas in the northern hemisphere, and we discuss the phylogeography of Neolepadidae with a phylogenetic reconstruction based on the cytochrome c oxidase subunit I gene. We also discuss the relationship between key morphological characteristics and the feeding habits in the family, showing that, a number of Vulcanolepas species including Vulcanolepas verenae sp. nov. are specialized in culturing filamentous bacteria on their cirri.<br />
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Watanabe HK*, Chen C, Chan BKK* (2020). A new deep-sea hot vent stalked barnacle from the Mariana Trough with notes on the feeding ecology of Vulcanolepas. Marine Biodiversity, 51(1): 9. DOI: 10.1007/s12526-020-01144-x
Our paper just published in Zoological Journal of the Linnean Society revises two enigmatic genera of buccinid whelks, Enigmaticolus and Thermosipho that appear to specialise in deep-sea hot vents and cold seeps. We examined both new materials and the type specimens, combined with molecular phylogenetics to clear up confusions surrounding validity of names, generic assignments, and taxonomically informative characters. You can read the paper for free here: https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlaa134/6038916?guestAccessKey=ded4f2d5-cdbc-49b4-bd33-52d8a8b7b712<br />
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Abstract: <br />
Whelks in the sister genera Enigmaticolus and Thermosipho (Buccinidae) commonly inhabit deep water hydrothermal vents and hydrocarbon seeps. Thermosipho desbruyeresi, originally described from the Lau Basin, was thought to occur in vents across the western Pacific, with Eosipho desbruyeresi nipponensis described from the Okinawa Trough treated as its junior synonym. New materials collected from the Okinawa Trough vents and South China Sea seeps, however, exhibited key characteristics of Enigmaticolus. Re-examination of the types revealed that Eosipho d. nipponensis is actually morphologically distinct from Thermosipho desbruyeresi. A molecular phylogeny reconstructed using the cytochrome c oxidase subunit I (COI) gene confirmed the placement of both in Enigmaticolus and supported their distinctiveness at the species level. We therefore rehabilitate E. d. nipponensis as Enigmaticolus nipponensis comb. nov. and transfer T. desbruyeresi to the same genus, as Enigmaticolus desbruyeresi comb. nov. Our phylogeny also revealed that Enigmaticolus monnieri described from east Africa and E. inflatus described from the South China Sea are conspecific with E. nipponensis. We discuss the distribution and biogeography, as well as morphological variability of Enigmaticolus. Thermosipho is then left with only its type species, T. auzendei. We revised the diagnosis for the two genera, as well as the relevant species. <br />
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Chen C*, Xu T, Fraussen K, Qiu J-W (2020). Integrative taxonomy of enigmatic deep-sea true whelks in the sister genera Enigmaticolus and Thermosipho (Gastropoda: Buccinidae). Zoological Journal of the Linnean Society, Online First. DOI: 10.1093/zoolinnean/zlaa134
A co-authored paper published in the Journal of Eukaryotic Microbiology reports an abundance of chitinous structures in Chilostomella ovoidea, a deep-sea benthic foraminifera. Such structures have not been found in any other foraminifera. We revealed the distribution of these structures within an entire individual using 3D reconstruction (over 400 slices at 500 nm thick each!), and discussed their potential functions. The paper is OPEN ACCESS: https://onlinelibrary.wiley.com/doi/10.1111/jeu.12828 <br />
Thanks to all co-authors, including Masashi Tsuchiya!<br />
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Abstract<br />
Benthic foraminifera, members of Rhizaria, inhabit a broad range of marine environments and are particularly common in hypoxic sediments. The biology of benthic foraminifera is key to understanding benthic ecosystems and relevant biogeochemical cycles, especially in hypoxic environments. Chilostomella is a foraminiferal genus commonly found in hypoxic deep‐sea sediments and has poorly understood ecological characteristics. For example, the carbon isotopic compositions of their lipids are substantially different from other co‐occurring genera, probably reflecting unique features of its metabolism. Here, we investigated the cytoplasmic and ultrastructural features of Chilostomella ovoidea from bathyal sediments of Sagami Bay, Japan, based on serial semi‐thin sections examined using an optical microscope followed by a three‐dimensional reconstruction, combined with TEM observations of ultra‐thin sections. Observations by TEM revealed the presence of abundant electron‐dense structures dividing the cytoplasm. Based on histochemical staining, these structures are shown to be composed of chitin. Our 3D reconstruction revealed chitinous structures in the final seven chambers. These exhibited a plate‐like morphology in the final chambers but became rolled up in earlier chambers (toward the proloculus). These chitinous, plate‐like structures may function to partition the cytoplasm in a chamber to increase the surface/volume ratio and/or act as a reactive site for some metabolic functions.<br />
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Nomaki H*, Chen C, Oda K, Tsuchiya M, Tame A, Uematsu K, Isobe N (2020). Abundant chitinous structures in Chilostomella (Foraminifera, Rhizaria) and their potential functions. Journal of Eukaryotic Microbiology, Early View. DOI: 10.1111/jeu.12828
The first vesicomyid clam genome! We present a high-quality, chromosome-level genome assembly of the chemosymbiotic deep-sea cold seep clam Archivesica marissinica, as well as the genome of its endosymbiont. Analysing the two genomes together provided new insights on the co-evolution and genomic integration in this holobiont. This co-authored paper is now published online in Molecular Biology and Evolution and it is Open Access: https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msaa241/5909661<br />
Thanks to all collaborators, including Ting Xu and Jin Sun! <br />
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Abstract: <br />
Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.<br />
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Ip JC-H, Xu T, Sun J, Li R, Chen C, Lan Y, Han Z, Zhang H, Wei J, Wang H, Tao J, Cai Z, Qian P-Y, Qiu J-W* (2020). Host-endosymbiont genome integration in a deep-sea chemosymbiotic clam. Molecular Biology and Evolution, msaa241. DOI: 10.1093/molbev/msaa241
Paper documenting a case of extreme shell morphology variation in a vetigastropod limpet has been published in Marine Biodiversity! We found a new deep-sea hot vent site in the Okinawa Trough where Lepetodrilus nux (Vetigastropoda: Lepetodrilidae) lived on three substrate types, the shell morphology shifting according to the substrate shape. Previously, this level of intraspecific variation was well-known from true limpets, but this example adds to the existing evidence that any of the 54 independently-evolved limpet lineages may exhibit similar variation. The new vent site, “Ghibli Site”, is named after Studio Ghibli and includes structures such as “Laputa Chimney” and “Howl’s Castle”. Read the paper for free here: https://rdcu.be/caNYQ<br />
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Abstract: <br />
Having a non-coiled, limpet-like shell is a characteristic shared by numerous gastropod molluscs, including many lineages outside the true limpets (Patellogastropoda) where it has evolved convergently. The shell shape of limpet-formed gastropods has often been used as a key taxonomic character, and although studies have shown that it can vary depending on the substrate morphology these have mostly been examples from true limpets. Over a dozen origins of limpet-form are known in Vetigastropoda, and these limpets are still generally assumed to have rather stable shell forms that are useful for taxonomy and species identification. Here, we show that the vetigastropod limpet Lepetodrilus nux (Okutani, Fujikura & Sasaki, 1993) from a deep-sea hot vent in the Okinawa Trough develop distinct shell forms when living on different substrate types. Sequences of the barcoding region of the mitochondrial cytochrome c oxidase subunit I gene among the three forms only differed by 0.31–0.63% (K2P distance) in a 637 bp alignment, in line with the differences in shell morphology being intraspecific. The extent of shell form shift seen in this species is likely the largest reported for a vetigastropod limpet and provide further evidence that such plasticity is not phylogenetically constrained but is an intrinsic part of having a limpet-like shell. <br />
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Chen C, Watanabe-Kayama H (2020). Substrate-dependent shell morphology in a deep-sea vetigastropod limpet. Marine Biodiversity, 50(6): 104. DOI: 10.1007/s12526-020-01135-y
Co-authored paper examining genetic connectivity and differences in gene expression patterns between a hot vent and a cold seep population of deep-sea squat lobster Shinkaia crosnieri now published in Frontiers in Marine Science! A collaboration with colleagues including Ting Xu and Jin Sun. The paper is Open Access and can be freely accessed here: https://www.frontiersin.org/articles/10.3389/fmars.2020.587686<br />
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Abstract: <br />
Shinkaia crosnieri (Decapoda: Munidopsidae) is a squat lobster that dominates both deep-sea hydrothermal vent and methane seep communities in the Western Pacific. Previous studies comparing S. crosnieri living in these two types of habitats have suffered from methodological and/or sample size limits. Here, using transcriptome-wide single nucleotide polymorphisms (SNPs) markers from 44 individuals of S. crosnieri, we reveal the extent of genetic connectivity between a methane seep population in the South China Sea and a hydrothermal vent population in the Okinawa Trough, as well as their signatures of local adaptation. Analysis of differentially expressed genes (DEGs) between these two populations and population-specific genes (PSGs) revealed that a large number of unigenes, such as cytochrome P450 (CYP), glutathione S-transferase (GST) and peroxiredoxin 6 (Prdx6) related to oxidoreductase, and sulfur dioxygenase (ETHE1) and chondroitin 4-sulfotransferase 11 (CHST11) related to sulfur metabolism, showed opposite expression patterns in these two populations. Data subsampling in this study revealed that at least five individuals of S. crosnieri per site are required to generate reliable results from the differential gene expression analysis. Population genetic analyses based on 32,452 SNPs revealed clear genetic differentiation between these two populations with an FST value of 0.07 (p < 0.0005), and physical oceanographic modeling of the ocean currents in middle and deep layers also suggests a weak connection between these two sites. Analysis of outlier SNPs revealed 345 unigenes potentially under positive selection, such as sarcosine oxidase/L-pipecolate oxidase (PIPOX), alanineglyoxylate transaminase/serine-glyoxylate transaminase/serine-pyruvate transaminase (AGXT), and Cu-Zn superoxide dismutase (SOD1). Among the differentially expressed genes and genes with amino acid substitutions between the two sites are those related to oxidation resistance and xenobiotic detoxification, indicating local adaptation to the specific environmental conditions of each site. Overall, exploring the population structure of S. crosnieri using transcriptome-wide SNP markers resulted in an improved understanding of its molecular adaptation and expression plasticity in vent and seep ecosystems.<br />
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Xiao Y# / Xu T#, Sun J, Wong WC, Kwan YH, Chen C, Qiu J-W*, Qian P-Y* (2020). Population genetic structure and gene expression plasticity of the deep-sea vent and seep squat lobster Shinkaia crosnieri. Frontiers in Marine Science, 7: 587686. DOI: 10.3389/fmars.2020.587686
A co-authored paper describing two deep-sea polychaete worms in the genus Hesiolyra has been published online in Deep-Sea Research Part I! Previously, only one species was recognised in Hesiolyra and it was thought to be cosmopolitan, but our results show that this genus is in fact more diverse. The two newly named worms are from Indian Ocean hot vents, with H. longqiensis from the Southwest Indian Ridge and H. heteropoda n. sp. from Central Indian and Carlsberg ridges. Many thanks to collaborators including Ting Xu, Yanjie Zhang, Hiromi Watanabe-Kayama, among others! Link: https://doi.org/10.1016/j.dsr.2020.103401<br />
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Abstract:<br />
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Although many deep-sea species are considered to have transoceanic distribution, this assumption has rarely been critically tested. Using Hesiolyra (Hesionidae) as a case study, we show that careful molecular and morphological analyses are required for refuting/accepting claims about such wide distribution. Hesiolyra is a genus of polychaetes commonly found in hydrothermal vents of the Eastern Pacific, Atlantic and Indian Ocean. Nevertheless, H. bergi Blake, 1985, a species originally described from the Eastern Pacific Rise (EPR), is the only recognized species in this genus. Phylogenetic analyses based on the COI and 16 S rRNA genes revealed two monophyletic clades that were distinct from a clade consisting of H. bergi sequences. We erected two new species of Hesiolyra, herein named as H. longqiensis n. sp. from the Southwest Indian Ridge (SWIR) and H. heteropoda n. sp. from the Central Indian Ridge (CIR) and the Carlsberg Ridge (CR). Among them, H. longqiensis n. sp. is more closely related to H. bergi than to H. heteropoda n. sp. . Morphologically, the two newly described species can be easily distinguished from H. bergi. The notopodia and neuropodia of H. bergi and H. longqiensis n. sp., are of similar sizes, but the morphology of their lyrate chaetae and their dorsal cirri alternation patterns are different. In H. heteropoda n. sp., the notopodia are remarkably slimmer than the neuropodia, and it lacks lyrate chaetae. Overall, in this report two new species of Hesiolyra from the Indian Ocean ridges and show that the distribution of H. bergi is restricted to the Eastern Pacific Rise. Future exploration of other mid-ocean ridges is required to discover the true diversity of this genus of polychaetes inhabiting hydrothermal vent fields.<br />
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Wang Z, Xu T, Zhang Y, Zhou Y, Liu Z, Chen C, Watanabe HK, Qiu J-W* (2020). Molecular phylogenetics and morphological analyses of the ‘monospecific’ Hesiolyra (Annelida: Hesionidae) reveal two new species. Deep-Sea Research Part I: Oceanographic Research Papers, 103401. DOI: 10.1016/j.dsr.2020.103401
Co-authored paper led by Hiromi Watanabe-Kayama has been published in Journal of Crustacean Biology! We show that the deep-sea hot vent crab Gandalfus yunohana has high genetic connectivity across its known range with the gene-flow on the Izu-Bonin-Mariana Arc being predominantly southwards. For the first time we confirm that the Gandalfus from Okinawa Trough is indeed G. yunohana, as previously speculated. The article is OPEN ACCESS: https://doi.org/10.1093/jcbiol/ruaa045<br />
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Abstract: <br />
Genetic connectivity provides a basis for evaluating the resilience of animal communities by elucidating gene flow and serves as a proxy for realized dispersal through planktonic larval dispersal, settlement, and reproductive success. Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) is a brachyuran crab endemic to deep-sea hydrothermal vents in the northwestern Pacific. Although an iconic and often dominant species, the connectivity among its populations is yet to be examined. We obtained barcoding sequences of the mitochondrial COI gene of G. yunohana from four vent fields including two on the Izu Arc, one on the northern Mariana Arc, and one in the Okinawa Trough. Genetic diversity of populations on the Izu and northern Mariana arcs were similar and shared the dominant haplotypes, showing no genetic subdivision regardless of the habitat depth. The Okinawa Trough population, for which only one specimen was available, was not genetically different from specimens from the Izu/Mariana arc populations. Estimation of the number of immigrants among populations suggests that the migration from north to south is higher than in the reverse direction. Our results resonate with previous laboratory-culture experiments, suggesting a high dispersal capability for G. yunohana. Visual observations and sampling, however, suggest that G. yunohana is exceedingly rare in the Okinawa Trough. This perhaps results from a lack of sufficient larval supply from the Izu-Bonin-Mariana Arc vents, and there may not be a reproductive population in the Okinawa Trough.<br />
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Watanabe HK*, Chen C, Kojima S, Kato S, Yamamoto H (2020). Population connectivity of the crab Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) (Decapoda, Brachyura: Bythograeidae) from deep-sea hydrothermal vents in the northwestern Pacific. Journal of Crustacean Biology, Advance Access. DOI: 10.1093/jcbiol/ruaa045
Our paper on an endosymbiont-hosting vesicomyid clam from Antarctica has been published in Polar Biology! We show that all live pliocardiine clams so far found in vents and seeps around Antarctica are Archivesica puertodeseadoi, which was previously only known from off Argentina. We show using in situ observations and experimental respirometry that these clams are quite flexible in their ecophysiology, allowing them to thrive in a range of chemosynthesis-based ecosystems. The paper is OPEN ACCESS: https://link.springer.com/article/10.1007/s00300-020-02717-z<br />
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Abstract: <br />
Geothermal energy provides an important resource in Antarctic marine ecosystems, exemplified by the recent discovery of large-sized chemosymbiotic vesicomyid bivalves (subfamily Pliocardiinae) in the Southern Ocean. These clams, which we identified as Archivesica s.l. puertodeseadoi, have been reported as dead shells in areas previously covered by Larsen A and B ice shelves (eastern Antarctic Peninsula) and as live animals from active hydrothermal sites in the Kemp Caldera (South Sandwich Arc) at depths of 852–1487 m. Before, A. puertodeseadoi was known only from its type locality in the Argentine Sea, so we considerably extend the range of the species. Observations taken by remotely operated vehicle (ROV) footage show that the clams can live buried in sediment, or epilithically on the surface of rocks in diffuse geothermal flow. Experimental respirometry was conducted at surface pressure on individual bivalves acclimated to either their habitat temperature (4 °C) or elevated temperature (10 °C). The range of standard metabolic rates, from 3.13 to 6.59 (MO2, μmol O2 h−1 g−1 dry tissue mass), is similar to rates measured ex situ for other species in this clade, and rates did not differ significantly between temperature groups. Taken together, these data indicate a range of ecophysiological flexibility for A. puertodeseadoi. Although adapted to a specialist mode of life, this bivalve exploits a relatively broad range of habitats in the Southern Ocean: within sulphidic sediments, epilithically in the presence of diffuse sulphidic flow, or in deep methane-enriched seawater trapped under ice. <br />
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Linse K, Sigwart JD*, Chen C, Krylova EM (2020). Ecophysiology and ecological limits of symbiotrophic vesicomyid bivalves (Pliocardiinae) in the Southern Ocean. Polar Biology, Online First. DOI: 10.1007/s00300-020-02717-z
Our paper just published in Marine Biology finds shell microstructure to be a useful taxonomic character in deep-sea vent/seep pectinodontid limpets, in which shell form and radula are extremely variable intraspecifically and cannot reliably separate species. This provides a basis for taxonomy and species identification in future studies on this group. Furthermore, the limpets seem to shift their aragonite:calcite ratio in response to the environment. The paper: https://link.springer.com/article/10.1007/s00227-020-03692-z<br />
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Abstract: <br />
Pectinodontid limpets of the genus Bathyacmaea are endemic to hot vents and cold seeps and exhibit greatly variable shell and radular macro-morphologies, rendering reliable species-level identification challenging. Here, we analyzed shell microstructures of western Pacific vent/seep Bathyacmaea limpets using scanning electron microscopy and Raman spectrophotometry to test its usefulness in providing phylogenetic signals. Bathyacmaea shells comprised of two forms of calcitic microstructure including irregular spherulitic prismatic type-A (ISP type-A) and semi-foliated (SF), as well as the aragonitic crossed lamellar (CL) microstructure. Despite marked differences in macroscopic shell morphologies once leading them to be classified into different species or even genera, six morphotypes of Bathyacmaea nipponica from different chemosynthetic localities and substrates shared an outermost ISP-A layer and alternating layers of SF and CL structures in their outer and inner shell layers. A genetically divergent lineage recovered from the South Chamorro Seamount, however, differed in having a simple three-layered shell composition consisting of ISP-A, SF, and CL structures, in that order, from the outside, and an unusually thin inner shell layer consisting of only CL structure. Moreover, the ratio of aragonite and calcite varied with habitat conditions, with calcite dominating in vents and aragonite dominating in seeps. These results suggest that the shell microstructure of pectinodontids is under phylogenetic constraints and provides useful taxonomic signals, while the mineral polymorphism in aragonite/calcite ratio varies according to environmental factors. Furthermore, microstructures of two ‘species’ from Cretaceous seeps confirmed the same patterns in fossil lineages. <br />
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Sato K*, Watanabe HK, Jenkins RG, Chen C (2020). Phylogenetic constraint and phenotypic plasticity in the shell microstructure of vent and seep pectinodontid limpets. Marine Biology, 167: 79. DOI: 10.1007/s00227-020-03692-z
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