Research Article |
Corresponding author: Naohiro Hasegawa ( uuuuu-hasegawa@eis.hokudai.ac.jp ) Academic editor: Pavel Stoev
© 2024 Naohiro Hasegawa, Natsumi Hookabe, Yoshihiro Fujiwara, Naoto Jimi, Hiroshi Kajihara.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hasegawa N, Hookabe N, Fujiwara Y, Jimi N, Kajihara H (2024) Supplemental re-description of a deep-sea ascidian, Fimbrora calsubia (Ascidiacea, Enterogona), with an inference of its phylogenetic position. Zoosystematics and Evolution 100(1): 129-140. https://doi.org/10.3897/zse.100.113132
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Fimbrora Monniot & Monniot, 1991, a macrophagous ascidian genus within the family Ascidiidae Adams & Adams, 1858, is currently monotypic, represented by F. calsubia Monniot & Monniot, 1991, a species previously recorded from the bottom of the South Pacific at depths of 1000–1860 m. The taxonomic status of Fimbrora has remained ambiguous because characteristics in its branchial papillae and neural-gland opening are incompletely known in previous studies, while these traits are essential for distinguishing other ascidiid genera. So far, no nucleotide sequence representing F. calsubia is available. In this study, we collected a single specimen of F. calsubia at a depth of 2027 m, about 400 km off the Pacific coast of Honshu, Japan. This is the deepest record, as well as the first report from the North Pacific, for the species. Our examination indicates that Fimbrora is morphologically similar to another ascidiid genus, Psammascidia Monniot, 1962, by having only secondary branchial papillae in the pharynx. Our phylogenetic analysis, based on the 18S ribosomal RNA and cytochrome c oxidase subunit I genes, along with those of 27 ascidian species available in public databases, showed that F. calsubia was more closely related to Ascidia zara Oka, 1935, Phallusia fumigata (Grube, 1864) and Phallusia mammilata (Cuvier, 1815) than to Ascidia ceratodes (Huntsman, 1912), Ascidiella aspersa (Müller, 1776) and Ascidiella scabra (Müller, 1776). Our results also indicated that acquisitions of macrophagous feeding by deep-sea members happened independently at least three times in the evolutionary history of the entire Ascidiacea.
bathyal zone, biogeography, Chordata, phylogeny, taxonomy, Tunicata, Urochordata
The ascidiid genus Fimbrora Monniot & Monniot, 1991a is currently monotypic, consisting of the deep-sea ascidian Fimbrora calsubia Monniot & Monniot, 1991a. The taxonomic identity of Fimbrora is not fully established because states of some characters used for distinguishing other ascidiid genera are not known for this taxon. Apart from Fimbrora, the family Ascidiidae Adams & Adams, 1858 also contains four genera: Ascidia Linnaeus, 1767; Ascidiella Roule, 1884; Phallusia Savigny, 1816; and Psammascidia Monniot, 1962. Fimbrora is supposed to be distinguished from the other ascidiid genera by having a combination of three characteristics: i) the large, cup-shaped oral siphon with thin, uniformly long, and soft lobes, ii) two large blood vessels running on the oral-siphon wall and iii) macrophagous feeding behaviour (cf.
While ascidians are generally suspension feeders that filter food particles, such as phytoplankton, from the surrounding seawater (
List of macrophagous species in Ascidiacea with information about family, species, depth, evidence for macrophagous feeding and references.
Family | Species | Depth (m) | Evidence for macrophagous feeding* | References |
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Ascidiidae | Fimbrora calsubia Monniot & Monniot, 1991 | 1000–2027 | m/c |
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Octacnemidae | Benthascidia michaelseni Ritter, 1907 | 399 | m |
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Cibacapsa gulosa Monniot & Monniot, 1983 | 567 | m/c |
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Cryptia planum Monniot & Monniot, 1985 | 4930 | m/c |
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Dicopia antirrhinum Monniot, 1972 | 600–4300 | m/c |
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Dicopia fimbriata Sluiter, 1905 | 1210 | m |
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Dicopia japonica Oka, 1913 | 4526–4609 | m |
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Kaikoja globosa Monniot, 1998 | 1978 | m |
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Kaikoja multitentaculata (Vinogradova, 1975) | 4485–4520 | m |
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Megalodicopia hians Oka, 1918 | 200–5325 | m/c |
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Megalodicopia rineharti (Monniot & Monniot, 1989) | 695–3970 | m |
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Myopegma melanesium Monniot & Monniot, 2003 | 445–472 | m/c |
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Myopegma midatlantica Monniot, 2011 | 2087 | m |
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Octacnemus alatus Monniot & Monniot, 1985 | 3344 | m |
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Octacnemus bythius Moseley, 1876 | 1957–4087 | m/c |
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Octacnemus ingolfi Madsen, 1947 | 640–4655 | m |
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Octacnemus kottae Sanamyan & Sanamyan, 2002 | 3700–3910 | m |
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Octacnemus vinogradovae Sanamyan & Sanamyan, 1999 | 5400 | m |
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Octacnemus zarcoi Monniot & Monniot, 1984 | 4260–4270 | m/c |
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Polyoctacnemus patagoniensis (Metcalf, 1893) | 1920 | m |
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Situla cuculli Monniot & Monniot, 1991 | 2040 | m |
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Situla galeata Monniot & Monniot, 1991 | 1395–4891 | m |
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Situla lanosa Monniot & Monniot, 1973 | 1800–4990 | m |
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Situla macdonaldi Monniot & Monniot, 1977 | 790 | m |
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Situla pelliculosa Vinogoradova, 1969 | 5035–8400 | m |
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Situla rebainsi Vinogradova, 1975 | 3700–5651 | m |
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Situla rineharti Monniot & Monniot, 1989 | 695–3680 | m |
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Molgulidae | Asajirus arcticus (Hartmeyer, 1923) | 905–1283 | m |
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Asajirus dichotomus (Monniot & Monniot, 1984) | 3550 | m |
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Asajirus eunuchus (Monniot & Monniot, 1976) | 2000–5000 | m |
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Asajirus gulosus (Monniot & Monniot, 1984) | 1800–2500 | m |
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Asajirus hemisphericus (Monniot & Monniot, 1990) | 3680–3740 | m |
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Asajirus indicus (Oka, 1913) | 800–5000 | m/c |
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Asajirus ledanoisi (Monniot & Monniot, 1990) | 720–4829 | m |
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Asajirus ovirarus (Monniot & Monniot, 1990) | 820–1900 | m |
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Oligotrema lyra (Monniot & Monniot, 1973) | 3360–4680 | m/c |
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Oligotrema psammatodes (Sluiter, 1905) | 1158 | m |
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Oligotrema psammites Bourne, 1903 | 90–4000 | m |
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Oligotrema sandersi (Monniot & Monniot, 1968) | 2200–5020 | m |
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Oligotrema unigonas (Monniot Monniot, 1974) | 2300–5500 | m |
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The taxonomy of macrophagous molgulids has experienced twists and turns. Historically, Asajirus and Oligotrema were once considered by
So far, F. calsubia has been known from the South Pacific bathyal zone in three publications, based on a total of 13 specimens: three specimens at a depth of 1865 m in New Caledonian waters (
A single specimen of F. calsubia was collected near the south of Hoei Seamount, about 400 km off the Pacific coast of Honshu, Japan (Fig.
Total DNA was extracted using a DNeasy Tissue Kit (Qiagen, Hilden, Germany). For amplification, KOD One PCR Master Mix (TOYOBO, Osaka, Japan) was used. Partial sequences of the 18S rRNA (18S) gene and the mitochondrial cytochrome c oxidase subunit I (COI) gene were PCR amplified from the total DNA; the primer pairs 1F/9R (
For phylogenetic analysis, 18S and COI sequences of 27 ascidian species and those of the lancelet Branchiostoma floridae Hubbs, 1922 were downloaded from GenBank (Table
The GenBank accession numbers of 18S and COI sequences of Fimbrora calsubia Monniot & Monniot, 1991a, as well as 27 ascidian species and the lancelet Branchiostoma floridae Hubbs, 1922, used for phylogenetic analysis in this study.
Species | 18S | COI |
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Ascidia ceratodes | L12378 | MW872268 |
Ascidia zara | LC547325 | KY235397 |
Ascidiella aspersa | LC547321 | KF886702 |
Ascidiella scabra | AB811928 | MN064599 |
Botrylloides violaceus | LC432326 | LC432331 |
Chelyosoma siboja | AF165821 | AB104867 |
Ciona robusta | AB013017 | MF479417 |
Ciona savignyi | LC547329 | MK512499 |
Clavelina lepadiformis | JN573225 | AY603104 |
Clavelina meridionalis | FM244840 | AM706470 |
Corella eumyota | FM244846 | KU299765 |
Ecteinascidia herdmanni | FM244847 | AY600968 |
Ecteinascidia turbinata | FM244848 | MT873564 |
Fimbrora calsubia | LC777587 | LC777585 |
Halocynthia roretzi | AB013016 | HM151268 |
Herdmania momus | AF165827 | KM411616 |
Megalodicopia hians | AB075543 | AB104866 |
Molgula manhattensis | L12426 | MT873565 |
Oligotrema lyra | JN565043 | – |
Perophora japonica | AB499607 | MN064600 |
Perophora viridis | FM244849 | OM912740 |
Phallusia fumigata | FM244844 | KF309548 |
Phallusia mammillata | AF236803 | MN064634 |
Pycnoclavella diminuta | KJ632948 | KC017435 |
Pyura mirabilis | LC432327 | LC432332 |
Styela clava | LC432329 | LC432334 |
Symplegma reptans | AF165826 | LS992553 |
Syncarpa composita | LC432325 | LC432330 |
Branchiostoma floridae | M97571 | AB478593 |
For constructing phylogenetic trees, Bayesian Inference (BI) and Maximum Likelihood (ML) analyses were performed; MrBayes ver. 3.2.6 (
Order Enterogona
Suborder Phlebobranchia
Family Ascidiidae Adams & Adams, 1858
Fimbrora calsubia
Monniot & Monniot, 1991a, p. 384, figs 1–6;
Yorifusa-boya, from yorifusa, an ornament for kimonos and Japanese accessories and boya, a phonological variant of hoya, meaning a sea squirt.
One individual, JAMSTEC No. 111618, collected by N. Hookabe on 26 September 2022, about 400 km off the Pacific coast of middle Honshu, Japan, 30°47.05'N, 138°44.72'E, at a depth of 2027 m (Fig.
Individual ca. 20 cm in length including oral siphon (Fig.
Fimbrora calsubia Monniot & Monniot, 1991a, photographs showing external appearance of JAMSTEC No. 111618. A. The individual in situ (white arrow), attaching to a dead sponge (yellow arrowhead) along with a euplectellid glass sponge (yellow arrow); B. Left view in life; C. Inner surface of the oral siphon in fixed state; D. Enlarged view of atrial siphon in life.
Body wall attached to tunic on oral siphon, heart and renal vesicles; irregular cavity existing between tunic and body wall; inner surface of tunic covered with epithelial tissue. Neural ganglion situated between oral siphon and atrial siphon. On base of oral siphon, 105 oral tentacles present, each being ca. 8 mm in length. Peripharyngeal band made of single lamina running in a short distance posterior to oral tentacles, forming V-shape posterior to neural gland aperture (Fig.
Fimbrora calsubia Monniot & Monniot, 1991a (JAMSTEC No. 111618). A. Drawing of dissected specimen, showing the shape of neural-gland aperture, peripharyngeal band and dorsal lamina; B. Photograph of dissected pharynx cut open from ventral side; C. Magnification of the rectangle on B, showing the arrangement of longitudinal vessels, transverse vessels, stigmata and secondary branchial papillae (indicated with arrows).
Digestive tract positioned on left side of body (Fig.
Fimbrora calsubia Monniot & Monniot, 1991a (JAMSTEC No. 111618), photographs of fixed specimen. A. Sinistero-posterior portion of body, viewed from outside, showing alimentary canal and reproductive system; B. Cross section of stomach, showing the prey crustacean (probably a copepod); arrows indicating stomach folds; C. Gonads; D. Magnification of the rectangle on C, showing an ovary containing multiple eggs.
Gonad situated proximally on intestinal loop (Fig.
The animal attached itself to a dead sponge in an area with accumulated sand and mud at a depth of 2027 m, where the water temperature was 1.93 °C (Fig.
The clade consisting of four genera in the family Ascidiidae, i.e. Ascidia, Ascidiella, Fimbrora and Phallusia, received high support values (97% bootstrap; 1.00 posterior probability) (Fig.
Phylogenetic relationship of 28 ascidian species; a Maximum-Likelihood tree, based on a concatenated dataset consisting of 18S rRNA (1676 bp) and COI (1136 bp) genes. Bootstrap values and posterior probabilities are indicated if they are higher than 60% and 0.70, respectively. Macrophagous species are indicated with an asterisk (*).
The three macrophagous ascidians included in this analysis—F. calsubia, Megalodicopia hians Oka, 1918 and Oligotrema lyra—were each positioned differently in the phylogenetic tree. As in previous analyses (
Previous studies posited that Fimbrora would belong to Ascidiidae (
While the convergent evolution of macrophagous feeding in Megalodicopia and Oligotrema has already been revealed by
The present study expanded the species’ known distribution range for about 4000 km northwards, representing the first record of the species from the North Pacific. Our material also represents the deepest record for the species with the known vertical distribution range being about 1000–2000 m (
We present the first report of F. calsubia from the North Pacific. Our molecular phylogenetic analysis suggested that macrophagous feeding was convergently acquired at least three times independently in Ascidiacea. Our morphological observation indicated a similarity of Fimbrora to Psammascidia in having secondary papillae and lacking primary and intermediate branchial papillae.
We extend our profound gratitude to the captain and crew of the support vessel Yokosuka, the commander and operation team of the human-occupied vehicle Shinkai 6500 and to both Takao Yoshida (JAMSTEC) and Hiroyuki Yokooka (IDEA Inc.) for their invaluable assistance in sample collection. Without the kind support from Kanta Ochiai and Misato Sako (Nagoya University, Sugashima Marine Biological Laboratory) for experimental work, this paper would not have materialised. We are indebted to all the people who donated to NHa through the academic crowd-funding site “academist”, especially to Shunji Furukuma, Naoki Hayashi, Miyuki Honda, Hitoki Horie, Sho Hosotani, Yoshiki Iwai, Nami Kenmotsu, Moe, Takehiro Nakamura, Ryoma Nishikawa, Yuichi Sasaki, Tatsuya Shimoyama, Makoto Taniguchi, Daiki Wakita, Takaaki Yonekura, amongst others. NHa received financial support from JST SPRING, Grant Number JPMASP2119. This research was partly performed by the Environment Research and Technology Development Fund (JPMEERF20S20700) of the Environmental Restoration and Conservation Agency Provided by the Ministry of Environment of Japan. The cruise YK22-17C of the R/V Yokosuka was funded by an MPA monitoring project outsourced by the Ministry of the Environment of Japan.
Video 1. A close encounter with the deep-sea ascidian
Data type: mov
Explanation note: Video of the moment the specimen was discovered at a depth of 2027 m.
Video 2. Grabbing the ascidian with the manipulator of Shinkai 6500
Data type: mov
Explanation note: Video of the moment the specimen used in this study was collected by Shinkai 6500.