Research Article |
Corresponding author: Hiroki Kise ( hkm11sea@yahoo.co.jp ) Academic editor: Bert W. Hoeksema
© 2021 Hiroki Kise, Masami Obuchi, James Davis Reimer.
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:
Kise H, Obuchi M, Reimer JD (2021) A new Antipathozoanthus species (Cnidaria, Hexacorallia, Zoantharia) from the northwest Pacific Ocean. ZooKeys 1040: 49-64. https://doi.org/10.3897/zookeys.1040.62309
|
A new species of zoantharian within the genus Antipathozoanthus is described based on specimens collected from the coast of mainland Japan, northwest Pacific Ocean. Antipathozoanthus tubus sp. nov. is characterized by its substrate (epibiotic on polychaete tube) and habitat (exposed rock). As well, the results of molecular phylogenetic analyses using concatenated multiple genetic markers also support the distinction between A. tubus sp. nov. and its congenerics. Antipathozoanthus tubus sp. nov. is the first species of Antipathozoanthus species reported to be epibiotic on polychaete tubes, and is the second species in the genus that is not associated with antipatharians.
molecular phylogeny, polychaete, Sagami Bay, symbiosis, zoantharians
The order Zoantharia Rafinesque, 1815 (Cnidaria: Anthozoa) consists of primarily colonial hexacorallians that are commonly found in most marine environments, including extreme environments such as intertidal zones and methane cold seeps in the deep sea (
Antipathozoanthus Sinniger, Reimer & Pawlowski, 2010 within the family Parazoanthidae Delage & Hérouard, 1901 is a genus that has been the subject of recent research in Japanese waters (
Recently, we collected two specimens in Japanese waters of an undescribed species belonging to the genus Antipathozoanthus, which were unexpectedly found as epibionts on an empty polychaete tube. Here, we formally describe this new species, Antipathozoanthus tubus sp. nov., utilizing morphological and phylogenetic data. With this addition, the entire Japanese zoantharian fauna now comprises 37 recorded species, representing 16 of the 28 currently-recognized genera across nine families (see also
The examined specimens were collected in shallow waters of Sagami Bay, Kanagawa, Japan on 2019 and 2020, by SCUBA (Table
Familiy | Species | Voucher number | Locality | Coordinates | Date | Depth | Collecter | GenBank accession numbers | |||||
18S–rDNA | ITS–rDNA | 28S–rDNA | COI | 12S–rDNA | 16S–rDNA | ||||||||
Parazoanthidae | Antipathozoanthus tubus sp. nov. | NSMT–Co 1742 | Iwa Beach, Sagami Bay, Kanagawa, Japan | 35°09'36"N, 139°08'36"E | 26 Jul 2019 | 13.6 | M. Obuchi | MW652773 | MW652765 | MW652768 | MW649812 | MW652761 | MW652770 |
NSMT–Co 1743 | Kotogahama, Sagami Bay, Kanagawa, Japan | 35°08'48"N, 139°09'05"E | 6 Jul 2020 | 14 | M. Obuchi | – | – | – | – | – | – | ||
A. hickmani | CMNH–ZG 05883 | Roca Onan, Pizon Island, Galapagos, Ecuador | 0°35'27.2"S, 90°41'09.6"W | 14 Mar 2007 | 27 | A. Chiriboga | MW652771 | MW652764 | – | – | MW652759 | MW652769 | |
A. cavernus | NSMT–Co 1604 | Sakurajima, Kagoshima, Japan | 31°35'23.5"N, 130°35.27.8"E | 20 Sep 2015 | 21 | JD. Reimer | – | MG384699 | MW652766 | MG384660 | MW652763 | MG384681 | |
A. remengesaui | NSMT–Co 1603 | Blue Hole, Palau | 7°8'29.4"N, 134°13'23.3"E | 15 Sep 2014 | 23 | JD. Reimer | MW652772 | MG384703 | MW652767 | MG384649 | MW652762 | MG384673 | |
A. obscurus | NSMT–Co 1602 | Cape Bise, Motobu, Okinawa–jima Island, Japan | 26°42'34.4"N, 127°52'49.2"E | 14 Aug 2014 | 5 | JD. Reimer | MW652774 | MG384691 | – | MG384644 | MW652760 | MG384685 |
We extracted genomic DNA from tissue of the holotype specimen preserved in 99.5% EtOH using a spin-column DNeasy Blood and Tissue Extraction Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol. PCR amplification using Hot Star Taq Plus Master Mix Kit (Qiagen, Hilden, Germany) was performed for each of COI (mitochondrial cytochrome oxidase subunit I), mt 12S-rDNA (mitochondrial 12S ribosomal DNA), mt 16S-rDNA (mitochondrial 16S ribosomal DNA), 18S-rDNA (nuclear 18S ribosomal DNA), ITS-rDNA (nuclear internal transcribed spacer region of ribosomal DNA), and 28S-rDNA (nuclear 28S ribosomal DNA) using published primers (
Forward and reverse sequences were assembled and edited in Geneious v10.2.3 (
Phylogenetic analyses were performed on the concatenated dataset using Maximum likelihood (ML) and Bayesian inference (BI). ModelTest-NG v0.1.6 (
Morphological data were collected from whole, dissected, and serial sections of the preserved specimens. Histological sections of 10–15 mm thickness were made using a RM-2125 RTS microtome (Leica, Germany) and were stained with hematoxylin and eosin after decalcification with a Morse solution for 48 h (1:1 vol; 20% citric acid: 50% formic acid). Classification of marginal muscle shapes followed
NSMT National Science Museum, Tsukuba, Ibaraki, Japan;
CMNH Coastal Branch of Natural History Museum and Institute, Chiba, Japan.
Suborder Macrocnemina Haddon & Shackleton, 1891
Family Parazoanthidae Delage & Hérouard, 1901
(revised from
Gerardia macaronesicus Ocaña & Brito, 2003, by original designation.
We herein modify the diagnosis of Antipathozoanthus, as A. tubus sp. nov. is clearly located within the clade of Antipathozoanthus with very high support in our molecular phylogenetic analyses. Skeletal secretion as has been reported in A. macaronesicus (Ocaña & Brito, 2003) was not found in any other Antipathozoanthus species, including A. tubus sp. nov.
Holotype. NSMT-Co 1742, collected from Iwa Beach, Sagami Bay, Kanagawa, Japan (35°09'36"N, 139°08'36"E) at a depth of 14 m by M. Obuchi, 26 July 2019, divided in two pieces, one portion fixed in 99.5% EtOH and the other in 5–10% saltwater formalin. Paratype. NSMT-Co 1743, collected from Kotogahama, Sagami Bay, Kanagawa, Japan (35°08'48"N, 139°09'05"E) at a depth of 14 m by M. Obuchi, 6 June 2020, divided in two pieces, one portion fixed in 99.5% EtOH and the other in 70% EtOH.
Images of external morphology of Antipathozoanthus tubus sp. nov. (holotype: NSMT-Co 1742) a colony on branched polychaete tubes in situ b close-up image of polyps in situ c colony on branched polychaete tubes in preserved condition d close-up image of closed polyp. Abbreviations: MT: marginal teeth, T: tube of polychaete. Scale bars: 10 mm (a, c), 5.0 mm (b), 0.5 mm (d).
Antipathozoanthus obscurus NSMT-Co1602 (holotype), collected from Cape Bise, Motobu, Okinawa-jima Island, Japan, by J.D. Reimer, 14 August 2014. Antipathozoanthus remengesaui NSMT-Co1603 (holotype), collected from Blue Hole, Palau, by J.D. Reimer, 15 September 2014. Antipathozoanthus cavernus NSMT-Co1604 (holotype), collected from Sakurajima, Kagoshima, Japan, by J.D. Reimer, 20 September 2015. Antipathozoanthus hickmani CMNH-ZG-05883 (paratype), collected from Roca Onan, Pinzon Island, Galapagos, Ecuador, by A. Chiriboga, 14 March 2007.
Iwa Beach, Sagami Bay, Kanagawa, Japan
External morphology. Colonial zoantharian, with cylindrical polyps connected by well-developed dark red colored coenenchyme (Fig.
Internal morphology. Azooxanthellete. Mesentery number 30–34, complete 15–17, incomplete 15–17. Mesenteries in macrocnemic arrangement (Fig.
Image of internal morphology of Antipathozoanthus tubus sp. nov. (holotype: NSMT-Co 1742) a longitudinal section of polyp b closed-up image of cteniform endodermal marginal muscle c, d cross-section of polyp. Abbreviations: A: actinopharynx, MF: mesenterial filament, CEMM: cteniform endodermal marginal muscle, DD: dorsal directives, VD: ventral directives, S: siphonoglyph, 5th: 5th mesentery from dorsal directives, M: mesoglea, CM: complete mesentery, IM: incomplete mesentery. Scale bars: 0.5 mm (a, c), 0.1 mm (b, d).
Cnidae. Basitrichs and microbasic b-mastigophores, microbasic p-mastigophores, holotrichs, and spirocysts (Fig.
Cnidae types and sizes observed in Antipathozoanthus tubus sp. nov. Frequency: relative abundance of cnidae type in decreasing order; numerous, common, occasional, rare (n = number of cnidae).
Tissue | Type of cnidae | Antipathozoanthus tubus sp. nov. | ||||
Length | Width | Mean±SD | Frequency | n | ||
(min-max) | (min-max) | (Length × Width) | ||||
Tentacles | Spirocysts | 8.0–19.0 | 1.0–4.0 | 15.6±2.0 × 2.1±0.5 | Numerous | 325 |
Bastrichs | 7.0–16.0 | 1.0–4.0 | 10.4±1.5 × 2.0±0.7 | Numerous | 37 | |
Holotrichs medium | 12.0–19.0 | 7.0–8.0 | 17.8±2.6 × 7.6±0.5 | Occasional | 6 | |
Holotrichs large | 20.0–22.0 | 8.0–11.0 | 20.7±0.6 × 9.4±0.8 | Occasional | 10 | |
Column | Special microbasic b-mastigophores | 12.0 | 6.0 | – | Rare | 1 |
Actinopharynx | Spirocysts | 10.0–16.0 | 1.0–3.0 | 12.7±1.6 × 2.4±0.7 | Occasional | 9 |
Bastrichs | 11.0–15.0 | 2.0–3.0 | 12.5±1.0 × 2.3±0.4 | Numerous | 37 | |
Microbasic b-mastigophores | 8.0–15.0 | 2.0–3.0 | 10.0±1.9 × 2.6±0.5 | Rare | 5 | |
Microbasic p-mastigophores | 9.0–11.0 | 3.0 | 10.0±0.8 × 3±0 | Rare | 3 | |
Holotrichs medium | 16.0–19.0 | 5.0–8.0 | 18.3±0.1 × 6.8±0.1 | Rare | 4 | |
Holotrichs large | 20.0–22.0 | 8.0–10.0 | 20.7±0.9 × 9.0±0.7 | Occasional | 15 | |
Mesenterial filaments | Microbasic b-mastigophores | 10.0–14.0 | 2.0–3.0 | 12.2±1.8 × 2.5±0.5 | Rare | 4 |
Microbasic p-mastigophores | 8.0–16.0 | 2.0–4.0 | 10.1±0.2 × 3.2±0.6 | Numerous | 60 | |
Holotrichs medium | 12.0–19.0 | 5.0–10.0 | 17.8±1.9 × 9.3±1.2 | Common | 23 | |
Holotrichs large | 20.0–25.0 | 10.0–12.0 | 21.1±1.2 × 10.7±0.5 | Numerous | 36 |
Cnidae in the tentacles, column, actinopharynx, and mesenterial filaments of holotype of Antipathozoanthus tubus sp. nov. Abbreviations: HL: holotrich large, HM: holotrich medium, B: basitrichs, BM: microbasic b-mastigophores, SBM: special microbasic b-mastigophores, PM: microbasic p-mastigophores, S: spriocysts.
Northwestern Pacific Ocean: Sagami Bay, Kanagawa, Japan at depths < 14 m.
We could not identify host polychaete species as there were no polychaetes in the tubes. However, the tubes that Antipathozoanthus tubus sp. nov. was attached to may belong to species within the genus Eunice, as polychaete species that build parchment-like branched tubes have been reported from this genus (e.g.,
Both ML and BI phylogenetic analyses showed similar topologies as indicated in Fig.
Antipathozoanthus tubus sp. nov. can be easily distinguished from A. remengesaui
Antipathozoanthus is a circumglobally distributed genus, as species have reported from the Indian, Pacific, and Atlantic Oceans (
Within Parazoanthidae, until now, Isozoanthus altisulcatus Carlgren, 1939 is the only species described as living on the tubes of polychaetes. However, several morphological differences exist between A. tubus sp. nov. and I. altisulcatus. Capitular ridges are developed and conspicuous in I. altisulcatus, whereas they are indiscernible in A. tubus sp. nov. The marginal teeth on the capitulum found in A. tubus sp. nov. were not observed in I. altisulcatus. Although
Genetic distances of COI sequence between A. tubus sp. nov. and other Antipathozoanthus species can be considered as intra-generic differences based on previous comparisons of genetic distances (
Antipathozoanthus tubus sp. nov. is named from the Latin tuba, as this species is found on polychaete tubes. The Japanese name is ‘Iwa-tsuno-sunaginchaku’.
Japanese waters are composed of a wide variety of physical, geographical, and topographical environments due to the latitudinal extension of Japan spanning from the near-tropics of Okinawa to the near-subarctic Hokkaido, and also to the dynamic geology of the region, and thus, Japanese waters have high marine species diversity levels (
We would like to thank Tetsuaki Tabata, Yodai Tano, Marie Chiba, and Masaru Furuya (Iwa Diving Center). We are also grateful to Dr. Kensuke Yanagi (Coastal Branch of Natural History Museum and Institute) for permission to subsample specimens, and assistance in visiting the CMNH. Prof. Akihiro Takemura (University of the Ryukyus) is thanked for giving us technical support. The first author was supported by JSPS KAKENHI grant number 19J12174. We thank two reviewers and the editor, who all provided helpful comments on earlier versions of this manuscript.
Table S1
Data type: GenBank accession numbers
Explanation note: GenBank accession numbers used for phylogenetic analyses in this study. Newly obtained sequences indicated in bold.