Research Article |
Corresponding author: Hironobu Fukami ( hirofukami@cc.miyazaki-u.ac.jp ) Academic editor: James Reimer
© 2019 Tatsuki Koido, Yukimitsu Imahara, Hironobu Fukami.
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:
Koido T, Imahara Y, Fukami H (2019) High species diversity of the soft coral family Xeniidae (Octocorallia, Alcyonacea) in the temperate region of Japan revealed by morphological and molecular analyses. ZooKeys 862: 1-22. https://doi.org/10.3897/zookeys.862.31979
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The soft coral family Xeniidae, commonly found in tropical and subtropical regions, consists of 20 genera and 162 species. To date, few studies on this family have been conducted in Japan, especially at higher latitudes. Although molecular phylogenetic analyses have recently been used to distinguish soft coral species, it is difficult to identify species and genera in this family due to the limited taxonomic indices and high morphological variation. In this study, we found a large Xeniidae community off the coast of Oshima Island (31°31.35'N, 131°24.27'E) at Miyazaki, Kyushu Island, located in the temperate region of Japan. The species composition and molecular phylogenetic relationships were investigated to uncover the species diversity of Xeniidae in this community. A total of 182 xeniid specimens were collected and identified to the species level, after which the samples were molecularly analyzed using a mitochondrial marker (ND2) and a nuclear marker (ITS) to infer the phylogenetic relationships. A total of 14 xeniid species were identified, including five undescribed species from five genera (Anthelia, Heteroxenia, Sympodium, Xenia, and Yamazatum). Miyazaki was identified as having the highest xeniid species diversity in Japan. The molecular phylogenetic trees inferred from each marker recovered very similar topologies: four genera (Anthelia, Heteroxenia, Sympodium, and Yamazatum) were monophyletic, whereas one (Xenia) was polyphyletic. Thus, except for Xenia, the morphological characteristics used for traditional taxonomy well reflected the phylogeny of the Xeniidae at the genus level. On the other hand, our results show that further taxonomic revisions of Xenia are needed.
high latitude, Miyazaki, phylogeny, taxonomy, Xeniidae
Tropical marine animals, including zooxanthellate alcyonacean corals (i.e., soft corals) abound in the southern part of the temperate region of Japan, due to the Kuroshio – a strong warm current running along the coast from the Ryukyu Archipelago to the mainland of Japan. However, studies looking into the zooxanthellate alcyonacean corals in Japan are limited, especially regarding the family Xeniidae Ehrenberg, 1828. Xeniidae comprises 20 genera and 162 species (
The present study describes a large community of xeniids found around Oshima Island (31°31.35'N, 131°24.27'E) at Miyazaki, Kyushu Island. As xeniids are uncommon in Japan, this is an unusual community. Due to this area’s higher latitude, coral reef structures are usually not formed, but there are over 100 zooxanthellate scleractinian coral species (
Species identification difficulties are common among the anthozoans due to their limited key taxonomic characteristics and high morphological variation and plasticity. Recently, molecular phylogenetic analyses have been used to overcome such limitations. In particular, molecular phylogenetic data have been used frequently in scleractinian corals to revise taxonomy, identify cryptic species and describe new species (e.g.,
To date, the molecular data of xeniids indicate that mitochondrial ND2 marker is one of the best markers to infer the phylogenetic relationships among genera within many octocoral families (e.g.,
Specimens of xeniids were collected around Oshima Island, Miyazaki, Japan (31°31.35'N, 131°24.27'E; Fig.
For species identification, we first summarized the morphological characteristics for all species in the five genera we found in this study (Xenia, Heteroxenia, Sympodium, Yamazatum Benayahu, 2010, and Anthelia) from original descriptions and related references to define the criteria for each species (Suppl. materials
Octocoral specimens for which partial ND2 and ITS sequences were obtained. MUFS-C: Miyazaki University, Fisheries Science for coral collections. NA: Not Analyzed.
Family | Species | Specimen Catalog # | Date | Depth (m) | GenBank # | |
---|---|---|---|---|---|---|
ND2 | ITS | |||||
Xeniidae | Anthelia cf. glauca | MUFS-COMO18 | 2012.7.2 | 4.3 | LC467016 | NA |
MUFS-COMO67 | 2012.12.25 | <10 | LC467017 | LC467102 | ||
MUFS-COMO70 | 2012.12.25 | <10 | LC467018 | NA | ||
Anthelia rosea | MUFS-COTUN6 | 2014.12.3 | <15 | LC467019 | LC467103 | |
Anthelia cf. tosana | MUFS-COMO13 | 2012.7.2 | <5 | LC467020 | NA | |
Heteroxenia cf. elisabethae | MUFS-COSU2 | 2012.5.5 | <1 | LC467021 | LC467104 | |
MUFS-COSU3 | 2012.5.5 | <1 | LC467022 | LC467105 | ||
Heteroxenia medioensis | MUFS-COOTUC4 | 2014.12.3 | <15 | LC467023 | LC467106 | |
MUFS-COOTUE3 | 2014.12.3 | <15 | LC467024 | LC467107 | ||
Heteroxenia minuta | MUFS-COMO10 | 2012.7.2 | 3.7 | LC467025 | LC467108 | |
MUFS-COMO12 | 2012.7.2 | 5.0 | LC467026 | LC467109 | ||
MUFS-COMO28 | 2012.8.31 | <10 | LC467027 | LC467110 | ||
Sympodium sp. 1 | MUFS-COMO63 | 2012.12.25 | <10 | LC467028 | LC467111 | |
MUFS-COOTUG2 | 2014.12.3 | <15 | LC467029 | LC467112 | ||
MUFS-COOTUK16 | 2014.12.3 | <15 | LC467030 | LC467113 | ||
Sympodium sp. 2 | MUFS-COMO149 | 2013.7.30 | <10 | LC467031 | LC467114 | |
Xenia sp. 1 | MUFS-COMO100 | 2012.12.25 | <10 | LC467032 | LC467115 | |
MUFS-COMO154 | 2013.7.30 | <10 | LC467033 | LC467116 | ||
MUFS-COMO166 | 2013.7.30 | <10 | LC467034 | LC467117 | ||
MUFS-COMO4 | 2012.7.2 | <5 | LC467035 | LC467118 | ||
MUFS-COMO53 | 2012.12.25 | <10 | LC467036 | LC467119 | ||
MUFS-COMO54 | 2012.12.25 | <10 | LC467037 | LC467120 | ||
MUFS-COMO64 | 2012.12.25 | <10 | LC467038 | LC467121 | ||
MUFS-COMO68 | 2012.12.25 | <10 | LC467039 | LC467122 | ||
MUFS-COMO76 | 2012.12.25 | <10 | LC467040 | LC467123 | ||
MUFS-COMO77 | 2012.12.25 | <10 | LC467041 | LC467124 | ||
MUFS-COMO82 | 2012.12.25 | <10 | LC467042 | LC467125 | ||
MUFS-COMO83 | 2012.12.25 | <10 | LC467043 | LC467126 | ||
MUFS-COMO85 | 2012.12.25 | <10 | LC467044 | NA | ||
Xenia kuekenthali | MUFS-COMO11 | 2012.7.2 | 2.9 | LC467045 | NA | |
MUFS-COMO3 | 2012.7.2 | 3.9 | LC467046 | LC467127 | ||
MUFS-COMO87 | 2012.12.25 | <10 | LC467047 | NA | ||
MUFS-COMO152 | 2013.7.30 | <10 | LC467048 | NA | ||
Xenia novaecaledoniae | MUFS-COMO155 | 2013.7.30 | <10 | LC467049 | NA | |
MUFS-COMO5 | 2012.7.2 | 3.2 | LC467050 | LC467128 | ||
MUFS-COMO65 | 2012.12.25 | <10 | LC467051 | LC467129 | ||
Xenia plicata | MUFS-COKMG3 | 2014.12.3 | <3 | LC467052 | NA | |
MUFS-COMO148 | 2013.7.30 | <10 | LC467053 | LC467130 | ||
MUFS-COMO15 | 2012.7.2 | 4.6 | LC467054 | LC467131 | ||
MUFS-COMO2 | 2012.7.2 | 4.8 | LC467055 | LC467132 | ||
MUFS-COMO26 | 2012.8.31 | <10 | LC467056 | NA | ||
MUFS-COMO40 | 2012.12.25 | <10 | LC467057 | LC467133 | ||
MUFS-COMO50 | 2012.12.25 | <10 | LC467058 | LC467134 | ||
MUFS-COMO69 | 2012.12.25 | <10 | LC467059 | LC467135 | ||
MUFS-COMO7 | 2012.7.2 | 4.0 | LC467060 | LC467136 | ||
MUFS-COMO80 | 2012.12.25 | <10 | LC467061 | LC467137 | ||
Xeniidae | Xenia sp. 2 | MUFS-COMO161 | 2013.7.30 | <10 | LC467062 | NA |
MUFS-COMO165 | 2013.7.30 | <10 | LC467063 | LC467138 | ||
MUFS-COMO6 | 2012.7.2 | 4.2 | LC467064 | NA | ||
MUFS-COMO8 | 2012.7.2 | 3.2 | LC467065 | LC467139 | ||
MUFS-COMO9 | 2012.7.2 | 3.9 | LC467066 | LC467140 | ||
MUFS-COSU1 | 2012.5.5 | <1 | LC467067 | NA | ||
MUFS-COSU4 | 2012.5.5 | <1 | LC467068 | LC467141 | ||
MUFS-COSU5 | 2012.5.5 | <1 | LC467069 | NA | ||
MUFS-COSU6 | 2012.5.5 | <1 | LC467070 | NA | ||
Yamazatum sp. 1 | MUFS-COMO1 | 2012.7.2 | 4.7 | LC467071 | LC467142 | |
MUFS-COMO14 | 2012.7.2 | 3.7 | LC467072 | LC467143 | ||
MUFS-COMO147 | 2013.7.30 | <10 | LC467073 | NA | ||
MUFS-COMO162 | 2013.7.30 | <10 | LC467074 | NA | ||
MUFS-COMO42 | 2012.12.25 | <10 | LC467075 | NA | ||
MUFS-COMO45 | 2012.12.25 | <10 | LC467076 | NA | ||
MUFS-COMO48 | 2012.12.25 | <10 | LC467077 | NA | ||
MUFS-COMO73 | 2012.12.25 | <10 | LC467078 | NA | ||
MUFS-COMO89 | 2012.12.25 | <10 | LC467079 | NA | ||
Briareidae | Briareum sp. | MUFS-COMO17 | 2012.7.2 | 3.7 | LC467080 | NA |
Clavulariidae | Clavularia sp. | MUFS-COAK6 | 2012.6.5 | <3 | LC467081 | NA |
Alcyoniidae | Cladiella pachyclados | MUFS-COSU13 | 2012.5.5 | <1 | LC467082 | LC467144 |
Cladiella digitulatum | MUFS-COSU14 | 2012.5.5 | <1 | LC467083 | LC467145 | |
Cladiella sphaerophora | MUFS-COAK1 | 2012.6.5 | <3 | LC467084 | LC467146 | |
Klyxum okinawanum | MUFS-COAK5 | 2012.6.5 | <3 | LC467085 | LC467147 | |
Klyxum sp. | MUFS-COMO150 | 2013.7.30 | <10 | LC467086 | NA | |
MUFS-COMO164 | 2013.7.30 | <10 | LC467087 | NA | ||
MUFS-COOTUD8 | 2014.12.3 | <15 | LC467088 | NA | ||
Sarcophyton sp. | MUFS-COAK7 | 2012.6.5 | <3 | LC467089 | NA | |
MUFS-COSU16 | 2012.5.5 | <1 | LC467090 | NA | ||
Sinularia sp. | MUFS-COAK2 | 2012.6.5 | <3 | LC467091 | NA | |
MUFS-COAK3 | 2012.6.5 | <3 | LC467092 | NA | ||
MUFS-COAK4 | 2012.6.5 | <3 | LC467093 | NA | ||
MUFS-COAK8 | 2012.6.5 | <3 | LC467094 | NA | ||
MUFS-COAK9 | 2012.6.5 | <3 | LC467095 | NA | ||
Nephtheidae | Dendronephthya rigida | MUFS-COSS4 | 2012.5.29 | <5 | LC467096 | NA |
Dendronephthya gigantea | MUFS-COSS1 | 2012.5.29 | <5 | LC467097 | NA | |
MUFS-COSS2 | 2012.5.29 | <5 | LC467098 | NA | ||
MUFS-COSS3 | 2012.5.29 | <5 | LC467099 | NA | ||
Stereonephthya rubriflora | MUFS-COSU15 | 2012.5.5 | <1 | LC467100 | NA | |
Stereonephthya japonica | MUFS-COAK10 | 2012.6.6 | <10 | LC467101 | NA |
Tissue samples were kept in CHAOS solution for at least a week to dissolve proteins at room temperature. Total DNA was extracted from the CHAOS solution with tissue samples by conventional phenol/chloroform extraction method. We used the primers reported by
MEGA5 (
A total of 14 species from five genera in the family Xeniidae were identified: three species from Anthelia, three from Heteroxenia, two from Sympodium, five from Xenia, and one species from Yamazatum (Table
In the present study, Xenia sp. 1, X. sp. 2, Yamazatum sp. 1, Sympodium sp. 1 and S. sp. 2 were identified as undescribed species for the following reasons: Xenia sp. 1 shared common morphological characteristics with the genus Xenia, such as the colony shape and the presence of oval sclerities, but presented also with unique needlelike sclerites with many small spines (Fig.
From the collected 14 species (78 samples), we obtained 673–707 bases of ND2 and 910–1039 bases of ITS. Molecular phylogenetic trees using the NJ and ML methods showed very similar topologies. Therefore, in this study, only ML trees for each marker are shown (Figs
In the present study, except Xenia, all genera were monophyletic (clades III, IV, VI, VII). Therefore, the synapomorphy reflecting each of the four clades is consistent with the key morphological characteristics for each genus. On the other hand, only Xenia was polyphyletic (clades I, II, and V). Therefore, to determine the synapomorphy for each clade, the morphological characteristics of the species in these three clades were compared. In clade I, including X. plicata and X. sp. 1, the synapomorphy is a colony form 25–40 mm in height and without secondary branches. Clade II, including X. novaecaledoniae and X. kuekenthali, presented a colony form similar to clade I (typical and no secondary branches), but shorter (10–20 mm in height). It is noteworthy that, although the family Xeniidae is taxonomically defined as presenting oval sclerites, both species in clade II lacked sclerites. Clade V, with just X. sp. 2, was characterized by a unique colony form, comprising a stalk measureing about 10 mm high and 20 mm in diameter, and many short branches extending from the top, becoming hump-shaped. This type of colony form has not been reported previously in the genus Xenia.
The present study identified 14 species from five genera in the family Xeniidae around Oshima Island, Miyazaki, in Japan. Among these species, 12 (Anthelia cf. glauca, A. rosea, A. cf. tosana, H. cf. elisabethae, H. minuta. H. medioensis, Sympodium sp. 1, S. sp. 2, Xenia novaecaledoniae, X. sp. 1, X. sp. 2 and Yamazatum sp. 1) were recorded in Japan for the fitst time, including five undescribed species (Sympodium sp. 1 and S. sp. 2, Xenia sp. 1, Xenia sp. 2 and Yamazatum sp. 1). On the other hand, two genera, Fungulus Tixier-Durivault, 1970 and Cespitularia, recorded previously in Japan (
Miyazaki has the highest Xeniidae species diversity in Japan (Table
Distribution of Xeniidae by country. List of number of species and genera of the family Xeniidae, previously reported in the world. See Suppl. material
Location | Number of species | Number of genera | References |
---|---|---|---|
Philippines | 42 | 5 | 15, 16, 26, 27, 29, 32 |
Indonesia | 38 | 7 | 2, 12, 13, 16, 18, 21, 26, 28, 30, 32, 36 |
Red Sea | 35 | 6 | 3, 10, 11, 12, 13, 16, 21, 24, 25, 26, 28, 30, 39, 40, 41, 44, 45, 46 |
Japan | 32 | 8 | 4, 5, 14, 15, 16, 23, 32, 34, 35, 37, This study |
Miyazaki Prefecture | 14 | 5 | This study |
Nansei Islands | 13 | 7 | 4, 5, 14, 15, 16, 37 |
Mainland of Japan (Honshu, Shikoku and Kyushu) | 8 | 3 | 16, 23, 32, 34, 35 |
Australia | 27 | 8 | 1, 13, 15, 16, 21, 30, 43 |
Tanzania | 17 | 6 | 13, 16, 21, 30, 31 |
Taiwan | 13 | 6 | 7, 8, 16, 32, 33 |
Seychelles | 11 | 5 | 12, 17, 18 |
New Caledonia | 7 | 3 | 15, 16, 18, 21, 42 |
Mozambique | 6 | 4 | 13, 18, 21, 31, 32 |
Papua New Guinea | 6 | 2 | 13, 21, 30, 31, 47 |
Fiji | 6 | 2 | 1, 13, 21, 28 |
Palau | 4 | 3 | 16, 18, 32 |
Malay | 4 | 3 | 1, 16 |
Chagos Archipelago | 4 | 3 | 1, 12, 21, 26, 31 |
Cargados Carajos | 3 | 3 | 31 |
Norwegian Sea | 3 | 2 | 9, 19, 20 |
Madagascar | 2 | 2 | 12, 16 |
Kenya | 2 | 2 | 30 |
Tonga | 2 | 2 | 13, 21, 28 |
Republic of South Africa | 2 | 2 | 21, 22 |
Sri Lanka | 2 | 1 | 13 |
Singapore | 1 | 1 | 6 |
Samoa | 1 | 1 | 28 |
New Zealand | 1 | 1 | 11 |
Hong Kong | 1 | 1 | 38 |
Korea | 1 | 1 | 16, 21, 31 |
Antarctic Ocean | 1 | 1 | 13, 21, 22 |
Guam | 1 | 1 | 18 |
Alcyonacean corals (soft corals) have been known as pioneers in coral reefs (
Heteroxenia and Yamazatum were monophyletic, although Xenia were closely related to both genera (Figs
In the present study, the phylogenetic position of Yamazatum sp. 1 was ambiguous as this species formed a sister group with clade I in the ND2 tree (Fig.
Xenia was polyphyletic, particularly due to X. sp. 2 (Figs
Two undescribed species, S. sp. 1 and S. sp. 2, were found in Sympodinium, and presented different sclerites and microstructure types (Fig.
Studies on the species composition and biodiversity of alcyonacean corals have drawn considerably less attention than those on scleractinian corals, since alcyonacean corals do not form the same three-dimensional structures with their hard skeletons as scleractinian corals, and, therefore, provide less habitat for other animals. However, coral communities have been reported to shift from scleractinian corals to alcyonacean corals in the future, if ocean acidification persists (
We are grateful to two anonymous reviewers for their helpful and constructive comments. We thank S. Nakachi and T. Mezaki of the Biological Institute on Kuroshio for their assistance with the microstructure analysis and sampling. We also thank Y. Oku and S. Ishizu of University of Miyazaki for their assistance with sampling. This study was founded by the Grant of Kuroshio Biological Research Foundation to T. Koido, and by JSPS KAKENHI (No.18K06423) to H. Fukami.
Table S1. Morphological features and key characters for species identification of Xenia
Data type: morphological data
Table S2. Morphological features and key characters for species identification of Yamazatum
Data type: morphological data
Table S3. Morphological features and key characters for species identification of Heteroxenia
Data type: morphological data
Table S4. Morphological features and key characters for species identification of Sympodium
Data type: morphological data
Table S5. Morphological features and key characters for species identification of Anthelia
Data type: morphological data
Table S6. List of references used in Table
Data type: reference data