water

Article
The Species Diversity of the Genus Echinogorgia in Xiamen Bay
and Its New Record in China
Yun-Pei Wang 1,2 , Jing Yang 1,2 , Ta-Jen Chu 1,2 and Jia-Ying Liu 1,2, *

1 Fisheries College, Jimei University, Xiamen 361021, China; [email protected] (Y.-P.W.);

[email protected] (J.Y.); [email protected] (T.-J.C.)
2 Fujian Provincial Key Laboratory of Marine Fishery Resources and Eco-Environment, Jimei University,
Xiamen 361021, China
* Correspondence: [email protected]

Abstract: The rapid reduction in coral reefs worldwide has led to increasing attention toward
protecting and restoring coral reef ecosystems. Coral reefs not only have a rich diversity of coral
species, but they can also provide important products and services for human beings. One type of
coral, Echinogorgia, has important scientific research value and application prospects. To understand
the diversity of coral species, diving surveys were conducted in Xiamen Bay in 2017 and 2021, and
a total of 928 samples were collected. Taxonomic research was conducted using methods such as
morphological identification through electron microscopy. Specific phylogenetic trees of the COI
gene, mtMuts gene, and ITS1 gene were analyzed. There were 47 specimens of Echinogorgia coral
included among 928 samples. Fifteen species of Echinogorgia were identified, including Echinogorgia
ramosa, Echinogorgia flexilis, Echinogorgia russelli, Echinogorgia ramulosa, and Echinogorgia gracilima
(which represent the newly recorded species in the waters of China). This study increases the
species diversity records in China and contributes to new geographical distribution information of
Echinogorgia worldwide. The primary data also serve as the baseline data for long-term biomonitoring
programs to estimate the status of octocorals in Xiamen Bay.

Keywords: Echinogorgia; new record species; taxonomy; biodiversity; Xiamen Bay

Citation: Wang, Y.-P.; Yang, J.; Chu,

T.-J.; Liu, J.-Y. The Species Diversity
of the Genus Echinogorgia in Xiamen 1. Introduction
Bay and Its New Record in China. Coral reefs, often referred to as an “oasis in tropical ocean deserts” or “rainwater in the
Water 2023, 15, 3547. https:// ocean”, are known for their ability to provide excellent habitats for numerous organisms;
doi.org/10.3390/w15203547 in addition, they form unique and highly productive ecosystems [1]. According to the
Academic Editor: José statistics, coral reefs are distributed in more than 100 countries and territories. Even though
Luis Sánchez-Lizaso they cover less than 0.2% of the seafloor, they support multiple functions, including marine
species diversity, coastal protection, food, and economic value [2]. Coral reef ecosystems
Received: 7 September 2023 are estimated to provide 2.85% of the value and services of marine ecosystems [3]. Coral
Revised: 25 September 2023
reef ecosystems are estimated to provide 2.85% of the value and services of marine ecosys-
Accepted: 28 September 2023
tems [3] and they are considered to have made an inestimable contribution to the world.
Published: 11 October 2023
Since the discovery of recorded corals, the investigation and classification of coral resources
have been one of the research focuses of scholars.
Corals are a global biological resource. In terms of distribution, the Indo–Pacific
Copyright: © 2023 by the authors. region, including the Pacific Ocean, Southeast Asia Sea, Indian Sea, and Red Sea, accounts
Licensee MDPI, Basel, Switzerland. for 92% of the world’s coral reef area [4]. According to a certain report [5], the second
This article is an open access article most populous place for coral reefs in Southeast Asia is the South China Sea, with an
distributed under the terms and estimated area of 37,935 square kilometers, which accounts for about 5%. In China, coral
conditions of the Creative Commons reefs also appear in certain sea areas, such as the Fujian, Guangdong, Guangxi, and Hainan
Attribution (CC BY) license (https:// coasts [4]. Zou [4] believes that the hermatypic corals community in Dongshan, Fujian is
creativecommons.org/licenses/by/ the northernmost sea area where hermatypic corals appear in China.
4.0/).

Water 2023, 15, 3547. https://doi.org/10.3390/w15203547 https://www.mdpi.com/journal/water

Water 2023, 15, 3547 2 of 21

In China, a number of coral species have been recorded, including 80 genera, or sub-
genera, and more than 700 species. A total of 1422 species of cnidarians are included in
the “List of Marine Biota of the China Sea” [6]. Among them, there are 763 species of
coral, including 41 species of Cerriantipatharia of Anthozoa, 328 species of Octocorollia, and
394 species of Seleactinia of Hexacorollia. As of 2020, China’s corals have been recorded in two
categories, as well as in sixteen families, seventy-seven genera, and four hundred forty-five
species [7]. In the waters of Fujian, there are fifty-four species of gorgonians in twenty-two
genera and nine families [8]. The places where Scleractinian corals are distributed in Fujian
include Xiamen, Dongshan, and Niushan Island, as well as in the Taishan Islands and other
such islands [8,9]. However, there are currently few studies on the coral classification in
Xiamen Bay. In 2006, a total of 38 species of coral were recorded in Xiamen Bay. Among them,
there were twenty-eight species in seven families of Alcyonacea, and ten species in six families
of Scleractinia [10]. In 2007, Huang et al. [11] reported on the species of Octocorallia corals
in the waters near Wuyu Island, and these belonged to four families and seven genera. In
2017, Ni et al. [12] found six species of scleractinian corals in Baiha Reef, Xiamen Bay. In 2022,
Liu et al. [13] reported three species of Astrogorgia coral inhabiting Xiamen Bay. In 2023, Yang
et al. [14] found a newly recorded species in Xiamen Bay.
The functions of coral reefs support marine biodiversity and provide important prod-
ucts and services to humans [15,16]. Octocorallia includes blue corals, soft corals, sea pens,
and gorgonians (sea fans and sea whips) within three orders: Alcyonacea, Helioporacea,
and Pennatulacea [17]. There are two orders and seventy-nine families in Octocorallia [18].
Octocorallia coral plays an important role in maintaining the structural integrity and biodi-
versity of marine ecosystems [19]. The genus Echinogorgia belongs to the Malacalcyonacea
of Octocorallia, which is similar to the Paramuriceidae. Echinogorgia was established in
1865, and the type species are E. sasappo (Esper, 1794), E. reticulata (Esper, 1791), and E.
umbratica (Esper, 1791) [20]. This genus has the following characteristics: the colonies
surface is flat, it is in a network-shaped fan shape, and it has short lateral branches on
the main branch [20]. Moreover, the sclerites are spindle-shaped and it has leaf-shaped
sclerites in the coenenchymata. These corals are red, brown, yellow, or white. As of
June 2023, WORMS (https://www.marinespecies.org, accessed on 2 March 2023) records
42 valid species of this genus. The species of this genus occur in many sea areas, including
the offshore waters of mainland China, Hong Kong, Germany, and the Indian Ocean [21].
Among them, eight species of this genus have been observed in the waters of China, namely
E. pseudosassapo, E. ridley [22], E. sassapo, E. flora, E. furfuracea, E. complexa, E. aurantiaca, and
E. lami [8,11,23]. Among them, E. ridley is recorded in the offshore waters of Taiwan, E.
pseudosassapo is recorded in the offshore waters of Taiwan and Fujian, while the other six
species are mainly distributed in the offshore waters of Fujian.
At present, the following two issues are of concern to the genus Echinogorgia: one is
taxonomic identification and the other is natural active substances. The issue of natural
active substances includes the extraction of substances [24,25], as well as the structure
and biological activity of substances [26–28]. Most of the above studies show the status of
unspecified species [29,30], and this uncertainty is not conducive to future research and
production applications. Uncertainty in species classification is mainly due to the fact
that previous authors did not assign the holotype and that the specimens and sclerites are
mostly insufficient in correctly identifying the species. Furthermore, certain species have
been identified based on only a few specimens or fragments [31]. Therefore, an in-depth
taxonomic study of the species in this genus is crucial.
With the rapid development of molecular technology, these tools are also widely used
in coral classification and identification. Certain studies have shown that 18S rDNA [32,33],
ITS [34,35], COI, ND2, and mtMuts gene fragments [36–38] are suitable for the phylogenetic
study of corals. On the basis of morphological identification, Xu et al. [39] established a phy-
logenetic tree of the mtMuts gene to study the taxonomy and phylogeny of Octocorallia in
western Pacific seamounts. Li et al. [33] clearly demonstrated the phylogenetic relationship
of Gorgonian coral by establishing a 18S rDNA phylogenetic tree. McFadden et al. [18] used
Water 2023, 15, 3547 3 of 21

the mtMuts gene to establish a phylogenetic tree and conducted a phylogenetic analysis on
185 taxa of Octocorallia coral. Hume et al. [40] studied coral species diversity using ITS2
markers.
In this study, the morphological classification method was used to identify the samples
of Echinogorgia collected from Xiamen Bay. Also, via molecular techniques, phylogenetic
analysis was conducted using the COI gene sequences, mtMuts gene sequences, and ITS
gene sequences. The determination of the specific types of corals in Xiamen Bay will help
with providing data support for biodiversity conservation in Xiamen Bay.

2. Materials and Methods

2.1. Station and Sample Collection
Nine hundred and twenty-eight coral samples were collected via diving sampling in
2017 and 2021. Among them, 823 samples were collected in 10 stations in 2017. In 2021,
105 samples were collected from 4 stations. The information collected from the sampling
Water 2023, 15, x FOR PEER REVIEW stations is shown in Table 1, and the schematic diagram of the3 ofsampling
21 stations is shown
in Figure 1.
of Octocorallia in western Pacific seamounts. Li et al. [33] clearly demonstrated the phylo-
Table 1. The sampling station information from 2017 and 2021.
genetic relationship of Gorgonian coral by establishing a 18S rDNA phylogenetic tree.
McFadden et al. [18] used the mtMuts gene to establish a phylogenetic tree and conducted
Year Station
a phylogenetic analysis Longitude
on 185 taxa of Octocorallia coral. Hume et al. [40] studied coral Latitude
species diversity
Shangyuusing ITS2 markers.
Island (SY) 118◦ 110 1900 –118◦ 110 2500 24◦ 270 1200 –24◦ 270 1300
In this study, the morphological
Huangcuo (HC) classification method
118◦was used
070 50 00 to identify the sam- 24◦ 250 2500
ples of Echinogorgia
Kulangsucollected from Xiamen Bay. Also,
Island (KLS) 118◦via molecular
030 14 00 –118◦ 03 techniques,
0 4100 phyloge- 24◦ 260 2300 –24◦ 260 3500
netic analysis was
Fireconducted
Island (FI)using the COI gene sequences,118◦mtMuts
030 5400 gene sequences, and 24◦ 290 3500
ITS gene sequences. The determination
Qingyu Island (QY) of the specific types
118◦ 05 0 3500 of corals
–118 ◦ 070in 28Xiamen
00 Bay will 24◦ 210 4500 –24◦ 210 5500
2017 help with providing data support
Wuyu Island (WY) for biodiversity118 conservation
◦ 030 5400 –118 in ◦Xiamen
080 3500 Bay. 24◦ 200 2300 –24◦ 290 3500
Dabai Island (DB) 118◦ 260 5800 –118◦ 270 4000 24◦ 330 4600 –24◦ 340 900
2. MaterialsXiaobai
and Methods
Island (XB) 118◦ 270 4700 24◦ 330 2100
Jiaoyu
2.1. Station and Island
Sample (JY)
Collection 118◦ 240 1400 24◦ 320 4100
Baihaand
Reeftwenty-eight
(BH) 118 ◦ 220 0700 –118◦ 220 1700 ◦ 0 00 ◦ 0 00
Nine hundred coral samples were collected via diving sampling in 24 31 38 –24 31 55
2017 and 2021. Among
Qingyu them,
Island (QY)823 samples were collected
118◦ 070 21 in00 –118
10 stations in 2017. In 2021,
◦ 070 5000 24◦ 210 4500 –24◦ 220 1100
105 samplesWuyu
were collected from
Island (WY) 4 stations. The information collected
118 08 28 –118◦ 080 57
◦ 0 00 from
00 the sampling 24◦ 200 3100 –24◦ 200 5100
2021 stations is shown
DabaiinIsland
Table 1, and the schematic diagram
(DB) 118◦ 45of0 02
the sampling
00 –118 ◦ 460 06stations
00 is shown 24◦ 560 3100 –24◦ 570 5100
in Figure 1. Xiaobai Island (XB) 118◦ 420 5800 –118◦ 430 3800 24◦ 580 2600 –24◦ 580 9600

Figure 1. The
Figure 1.locations of coral sampling
The locations in Xiamen
of coral Bay (KLS,
sampling FI, SY, HC,Bay
in Xiamen WY,(KLS,
QY, JY, FI,
BH, SY,
XB, and
HC, WY, QY, JY, BH, XB, and
DB). Schematic diagram of sampling stations.
DB). Schematic diagram of sampling stations.
Water 2023, 15, 3547 4 of 21

2.2. Material and Sample Processing

The samples were collected and brought back to the laboratory in order to take photos
of the living corals, and these were numbered for preservation. Suitable lengths of coral
samples were cut and placed in centrifuge tubes filled with 95% ethanol for traditional
morphological and molecular biology experiments. The remaining samples were stored in
an ultralow temperature refrigerator at −70 ◦ C.

2.3. Experimental Instruments

In this study, certain experimental instruments were used, including a Nikon SMZ1270
dissecting microscope, a NiKon ECLIPSE 80i microscope, a DHG-9050A air-drying oven, a
G5 PhenomProX2017 electron scanning electron microscope, an A200 PCR amplification
apparatus, a Z216MK centrifuge, an MK200-2 dry thermostat, a DYY-8C electrophoresis
apparatus, and a JS-20.2 gel imaging system.

2.4. Identification Method

Generally, octocorals are identified, classified, and described primarily on the basis of
external and internal morphology. These morphological characteristics include the colonies’
size, shape, color, and calyx structures, as well as their sclerite content, dominance, shape,
size, and arrangement [31,32,37,41].
(1) Exterior feature observation
First, certain characteristics were observed, including the coral appearances, colors,
polyps, surfaces, spindles, branches, bases, top colonies, etc. In addition, actions were
carried out, including measuring, photographing, describing, and recording the relevant
parts of the coral.
(2) Observation of local appearance and morphology
A dissecting microscope (Nikon SMZ1270) was used to observe (as well as photograph)
the color and shape of the polyps, as well as the calyx structure.
(3) Observation of sclerites
After the tissue samples were dissolved in sodium hypochlorite, different parts of the
sclerite samples (polyps, coenenchymata, and tentacles) were observed and examined. The
sclerites were washed with distilled water and subsequently dried using a blast dryer. The
samples were sent to the scanning electron microscope (SEM) (G5 PhenomProX2017) set
up in the National Key Laboratory of Xiamen University for observation. Then, detailed
images of the sclerites through SEM were obtained. The images for each sclerite type were
then optimized using Adobe Photoshop 2020. When the coral branches were placed in the
Petri dish, a solution of ultra-pure water and sodium hypochlorite (with a ratio of 3:1–5:1)
was injected into it for dissolution. Next, the arrangement of the spicules under a dissecting
microscope were observed and pictures were taken.

2.5. Classification Basis

2.5.1. Identification Documents
Certain important documents were used for species classification and identification
such as “Soft Corals and Sea Fans” [42], the World Register of Marine Species (WROMS) [21],
and taxonomic terminology references [43].

2.5.2. DNA Extraction and PCR Amplification

With the use of the marine animal tissue genomic DNA extraction kit of Shanghai
Biotechnology Co., Ltd., three coral individuals were prepared for total genome DNA
extraction. The steps of extraction were followed as per the manufacturer’s instructions.
The primers used in this study are shown in Table 2.
Water 2023, 15, 3547 5 of 21

Table 2. The primers used for genetic analyses.

Primers Gene Region Sequence (50 -30 ) References

F-GGA ATG GCG GGG ACA GCT
COI-LA-8398
COI gene TCG AGT ATG TTA ATA CGG [44]
R-ATC ATA GCA TAG ACC
COIoct
ATACC
F-AGG AGA ATT ATT CTA AGT
AnthoCorMSH
MSH gene ATGG [44]
Mut3458R R-TSG AGC AAA AGC CAC TCC
ITS1 F-TCCGTAGGTGAACCTGCGG
ITS gene [45]
ITS2 R-GCTGCGTTCTTCATCGATGC

2.5.3. Phylogenetic Analysis of Coral Samples Based on COI, mtMuts, and ITS
Gene Fragments
Based on the morphological results, using molecular technology to extract the DNA
from certain coral samples for amplification analysis, the COI gene sequence, mtMuts
gene sequence, and ITS1 gene sequence results of the samples were compared with the
GenBank database. The gene sequence fragments of the species with a similarity of over
95% were compared with the corresponding screened gene fragment information in the
NCBI database using MEGA7.0 software. The neighbor joining method, based on the
Kimura 2 parameter (K2P) model with 1000 bootstrap replicates, was used to construct
phylogenetic trees and to conduct a phylogenetic analysis.

3. Results
3.1. Systematic Approaches
The morphological classification method was used to identify 47 samples of the genus
Echinogorgia, and the results showed that these samples were classified into 15 species. A
total of 15 species named Echinogorgia ramosa, E. flexilis, E. russelli, E. ramulosa, E. gracillima,
E. sp1, E. sp2, E. sp3, E. sp4, E. sp5, E. sp6, E. sp7, E. sp8, E. sp9, and E. sp10 were identified.
We found five new recorded species in China, including E. ramose, E. flexilis, E. russelli, E.
ramulosa, and E. gracillima.
The morphological descriptions of the five newly recorded species were as follows.

3.1.1. Echinogorgia ramosa (Thomson and Henderson, 1905)

Sample collection location: Qingyu (118◦ 070 3400 , 24◦ 210 4600 ), water depth: 7.5 m;
Study sample number: 20210423-QY-33;
Coral group (Figure 2a): The living colonies were 9 cm high, and most of their branches
were on the same plane. The lateral branches bent outward and upward. The irregular
branches were mainly distributed on one side of the main trunk. The diameter of the central
shaft was greater than 0.5 mm. The central axis was divided into two layers: inner and outer
(with an uneven yellow color on the inner layer and a uniform dark brown color on the outer
layer). The ratio of the inner and outer layers of the axis radius was approximately 2:3;
Polyps (Figure 2a(B,C)): The polyps could freely contract and were mainly distributed
on the surface of the trunk and branches. The polyps contracted into the coral calyx, which
was circular in shape and had a diameter of about 0.5 mm;
Sclerites (Figure 2b): The polyps contained straight or curved spindle-shaped sclerites
with a length of about 0.2–0.4 mm. The surface of the sclerites contained small and conical
columnar protrusions. The coenenchymata contained leaf-shaped sclerites and a few pan-
shaped sclerites with a length of about 0.1–0.25 mm. The leaf-shaped sclerites contained
serrated edges, and the surface of the sclerites presented protrusions of varying sizes.
Sclerites are colorless;
Color (Figure 2a(A)): reddish brown, and dark brown in alcohol;
Sample collection location: the waters near Qingyu Island in Xiamen Bay.
 rites with a length of about 0.2–0.4 mm. The surface of the sclerites contained small and
conical columnar protrusions. The coenenchymata contained leaf-shaped sclerites and a
few pan-shaped sclerites with a length of about 0.1–0.25 mm. The leaf-shaped sclerites
contained serrated edges, and the surface of the sclerites presented protrusions of varying
sizes. Sclerites are colorless;
Water 2023, 15, 3547 6 of 21
Color (Figure 2a(A)): reddish brown, and dark brown in alcohol;
Sample collection location: the waters near Qingyu Island in Xiamen Bay.

(a) (b)
Figure 2.
Figure 2. E. ramosa: (a)
E. ramosa: (a) Corals’
Corals’ external
external morphologies
morphologies ((A).
((A). Coral
Coral colonies;
colonies; (B,C).
(B,C). Polyps;
Polyps; (D).
(D). Axis);
Axis);
(b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the coenenchymata;
(b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the coenenchymata;
Scales: A = B = 0.2 mm).
Scales: A = B = 0.2 mm).
3.1.2. Echinogorgia flexilis (Thomson and Simpson, 1909)
3.1.2. Echinogorgia flexilis (Thomson and Simpson, 1909)
Coral group (Figure 3a): The living colonies were in a fan-shaped shape and were up
Coral group
to 10 cm high. The(Figure 3a): were
branches The living colonies
irregular and were
on theinsame
a fan-shaped shape
plane. The and axis
central werehad
up
to 10 cm high. The branches were irregular and on the same plane. The central axis
two layers. The inner layer was an uneven yellow, and the outer layer was a uniform dark had
two layers.
brown. TheThe
axisinner layer
radius waswas
3:2; an uneven yellow, and the outer layer was a uniform dark
brown. The axis radius was 3:2;
Polyps (Figure 3a(B,C)): The polyps’ monotypes were distributed on the surface of the
stems and branches. The gaps between the polyps were approximately 0.5 mm in diameter.
The coral calyx protruded and appeared as a dome, and the polyps contracted into the
calyx. The polyps turned purple after alcohol immersion;
Sclerites (Figure 3b): Straight or slightly curved fusiform-shaped sclerites were dis-
tributed in the polyps and were about 0.18–0.3 mm long, and some of the fusiform-shaped
sclerites were bifurcated at one end with columnar and prickly protrusions on the sclerites.
The surface layers of the coenenchymata had leaf-shaped, flat-shaped, and irregular-shaped
sclerites with a length of about 0.1–0.35 mm. The leaf-shaped sclerites had serrated edges,
and the surface of the sclerites all contained warty protrusions. The inner layers of the
coenenchymata contained multiple spicules (approximately 0.05–0.15 mm long), and the
sclerites were colorless;
Color (Figure 3a(A)): brownish red, and dark brown in alcohol;
Sample collection location: the waters near Qingyu Island in Xiamen Bay.
 rites. The surface layers of the coenenchymata had leaf-shaped, flat-shaped, and irregular-
shaped sclerites with a length of about 0.1–0.35 mm. The leaf-shaped sclerites had serrated
edges, and the surface of the sclerites all contained warty protrusions. The inner layers of
the coenenchymata contained multiple spicules (approximately 0.05–0.15 mm long), and
Water 2023, 15, 3547 the sclerites were colorless; 7 of 21
Color (Figure 3a(A)): brownish red, and dark brown in alcohol;
Sample collection location: the waters near Qingyu Island in Xiamen Bay.

(a) (b)
Figure 3. E. flexilis: (a) The corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D).
Figure 3. E. flexilis: (a) The corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D). Axis);
Axis); (b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the surface
(b)layers
SEMofimages of the coral(C).
coenenchymata; sclerites ((A).
Sclerites Sclerites
of the inner of the polyps;
layers (B). Sclerites
of coenenchymata; of theAsurface
Scales: = B = 0.2layers
mm; of
coenenchymata;
C = 0.1 mm). (C). Sclerites of the inner layers of coenenchymata; Scales: A = B = 0.2 mm; C = 0.1 mm).

3.1.3.Echinogorgia
3.1.3. Echinogorgiarusselli
russelli (Bayer,
(Bayer, 1949)
collection location: (118◦ 80 5700 ,24◦ 20 51005),m;
Sample collection location: Wuyu (118°8′57″,24°2′51″),
Sample 5 m;
Study sample number: 20210423-WY-15;
Study sample number: 20210423-WY-15;
Coralgroup
Coral group(Figure
(Figure4a):
4a): The
The living
living colonies
colonieswere
were2020cm cmtalltallwith
withdense
denseand irregular
and irregular
branches that bent upward and downward. Most of the branches were at right with
branches that bent upward and downward. Most of the branches were at right angles angles
with a small number of the coenenchymata shedding from the base of the main stem. The
diameter of the central axis was about 1 mm and was an uneven yellow color;
Polyps (Figure 4a(A,B)): The polyps could contract completely and freely, and they
were mainly distributed on the surface of the main stems and branches. The calyx slightly
protruded, and it resembled a low dome-shaped wart. The polyps completely contracted
into the calyx with a diameter of less than 1 mm. After alcohol immersion, the polyps
turned purple;
Sclerites (Figure 4b): The polyps contained columnar- and spindle-shaped sclerites, about
0.18–0.3 mm long, with columnar and spiny processes on the sclerites. The outer layers of
the coenenchymata contained leaf-shaped sclerites, approximately 0.18–0.25 mm long, with
serrated edges on the sclerites. The inner layers of the coenenchymata contained quadrangular
sclerites with a length of approximately 0.05–0.08 mm. The sclerites were colorless;
Color (Figure 4a(A)): light brownish red, and dark brown in alcohol;
Sample collection location: the waters near Wuyu Island in Xiamen Bay.
 about 0.18–0.3 mm long, with columnar and spiny processes on the sclerites. The outer
layers of the coenenchymata contained leaf-shaped sclerites, approximately 0.18–0.25 mm
long, with serrated edges on the sclerites. The inner layers of the coenenchymata con-
tained quadrangular sclerites with a length of approximately 0.05–0.08 mm. The sclerites
Water 2023, 15, 3547 were colorless; 8 of 21
Color (Figure 4a(A)): light brownish red, and dark brown in alcohol;
Sample collection location: the waters near Wuyu Island in Xiamen Bay.

(a) (b)
Figure 4. E. russelli: (a) The corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D).
Figure 4. E. russelli: (a) The corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D). Axis);
Axis); (b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the outer
(b)layers
SEMofimages of the coral
coenenchymata; sclerites
(C). ((A).
Sclerites Sclerites
of the of theofpolyps;
inner layers (B). Sclerites
coenenchymata; of the
Scales: A = outer
B = 0.2layers
mm; of
coenenchymata;
C = 0.1 mm). (C). Sclerites of the inner layers of coenenchymata; Scales: A = B = 0.2 mm; C = 0.1 mm).

3.1.4.Echinogorgia
3.1.4. Echinogorgiaramulosa
ramulosa (Gray, 1870)
Samplecollection
Sample collection location:
location: Wuyu (118◦ 80 570024°2′51″),
Wuyu (118°8′57″, , 24◦ 20 51005),m;
5 m;
Study sample number: 20210423-WY-15;
Study sample number: 20210423-WY-15;
Coralgroup
Coral group(Figure
(Figure 5a):
5a): The
The living
livingcolonies
colonieswerewerebranching
branching and
andwere
wereupup
to to
14 14
cmcm
high with abundant short branches. The small branches appeared at right
high with abundant short branches. The small branches appeared at right angles to the angles to the
mainbranch,
main branch,and
andthe
theshort
short branches
branches were
wereslightly
slightlyswollen
swollenatatthe theend. The
end. coenenchymata
The coenenchymata
were thicker, and the diameter of the central axis was less than 0.5 mm. The central axis
was uniformly yellow;
Polyps (Figure 5a(B,C)): The polyps appeared uniformly on the surface of the trunks and
branches, with a diameter of about 0.5 mm. The calyx protruded, resembling a circle, and some
of the polyps contracted into the calyx. After soaking in alcohol, the polyp turned purple;
Sclerites (Figure 5b): The polyps contained columnar- and spindle-shaped sclerites
about 0.1–0.4 mm long. The spindle-shaped sclerites were relatively flat, and the sur-
face of the spicules contained more verrucous protrusions. The surface layers of the
coenenchymata contained leaf-shaped sclerites and irregular sclerites with a length of
about 0.1–0.2 mm, and the edges of the sclerites contained serrated protrusions. The inner
layers of the coenenchymata contained multiple spicules with a length of approximately
0.1–0.15 mm. The sclerites were colorless;
Color (Figure 5a(A)): brick red, and dark brown in alcohol;
Sample collection location: the waters near Wuyu Island in Xiamen Bay.
 of the spicules contained more verrucous protrusions. The surface layers of the coenen-
chymata contained leaf-shaped sclerites and irregular sclerites with a length of about 0.1–
0.2 mm, and the edges of the sclerites contained serrated protrusions. The inner layers of
the coenenchymata contained multiple spicules with a length of approximately 0.1–0.15
Water 2023, 15, 3547 mm. The sclerites were colorless; 9 of 21
Color (Figure 5a(A)): brick red, and dark brown in alcohol;
Sample collection location: the waters near Wuyu Island in Xiamen Bay.

(a) (b)
Figure 5. E. ramulosa: (a) Corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D). Axis);
Figure 5. E. ramulosa: (a) Corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D). Axis);
(b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the outer layers of coe-
(b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the outer layers of
nenchymata; (C). Sclerites of the inner layers of coenenchymata; Scales: A = B = 0.2 mm; C = 0.1 mm).
coenenchymata; (C). Sclerites of the inner layers of coenenchymata; Scales: A = B = 0.2 mm; C = 0.1 mm).
3.1.5. Echinogorgia gracillima (Kükenthal, 1917)
Echinogorgia
3.1.5. Sample gracillima
collection (Kükenthal,
location: 1917) 24°2′51″), 5 m;
Wuyu (118°8′57″,
Sample collection
Study sample location:
number: Wuyu (118◦ 80 5700 , 24◦ 20 5100 ), 5 m;
20210423-WY-11;
Study
Coral sample number:
group (Figure 6a):20210423-WY-11;
The living colonies were fan-shaped and were up to 10 cm
withCoral
abundant
group and overlapping
(Figure branches.
6a): The There were
living colonies werea large numberand
fan-shaped of lateral
were branches
up to 10 cm
on one
with plane with
abundant andslightly enlarged
overlapping ends. The
branches. inner
There layer
were of thenumber
a large central axis was uneven
of lateral branches
on one plane with slightly enlarged ends. The inner layer of the central axis was uneven
and orange–yellow, and the outer layer was an uneven dark brown. The radius of the axis
was about 2:1 for the inner and outer layers;
Polyps (Figure 6a(B,C)): The polyps appeared on the surface of the trunks and branches
with protruding calyxes. The polyps could fully contract into the calyx with a diameter of
about 0.5 mm. After alcohol immersion, the polyps turned yellow;
Sclerites (Figure 6b): The polyps contained columnar- and spindle-shaped sclerites, which
were about 0.1–0.25 mm long. The sclerites contained verrucous protrusions, and some of the
spindle-shaped sclerites were bifurcated at one end. The outer layers of the coenenchymata
contained leaf-shaped sclerites, approximately 0.15–0.2 mm long, with serrated protrusions at
the edges of the sclerites. The inner layers of the coenenchymata contained radiating sclerites,
approximately 0.03–0.04 mm in length. The sclerites were colorless.
Color (Figure 6a(A)): yellow, and gray-brown in alcohol.
Sample collection location: the waters near Wuyu Island in Xiamen Bay.
 some of the spindle-shaped sclerites were bifurcated at one end. The outer layers of the
coenenchymata contained leaf-shaped sclerites, approximately 0.15–0.2 mm long, with
serrated protrusions at the edges of the sclerites. The inner layers of the coenenchymata
contained radiating sclerites, approximately 0.03–0.04 mm in length. The sclerites were
Water 2023, 15, 3547 colorless. 10 of 21
Color (Figure 6a(A)): yellow, and gray-brown in alcohol.
Sample collection location: the waters near Wuyu Island in Xiamen Bay.

(a) (b)
Figure 6. E. gracillima: (a) Corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D).
Figure 6. E. gracillima: (a) Corals’ external morphologies ((A). Coral colonies; (B,C). Polyps; (D). Axis);
Axis); (b) SEM images of the coral sclerites ((A). Sclerites of the polyps; (B). Sclerites of the outer
(b)layers
SEMofimages of the coral
coenenchymata; sclerites
(C). ((A).
Sclerites Sclerites
of the of theofpolyps;
inner layers (B). Sclerites
coenenchymata; of the
Scales: A = outer
B = 0.2layers
mm; of
coenenchymata;
C = 0.1 mm). (C). Sclerites of the inner layers of coenenchymata; Scales: A = B = 0.2 mm; C = 0.1 mm).

3.2.DNA
3.2. DNAAnalysis
Analysis
Thegene
The genesequence
sequenceofofthethesuccessfully
successfullyamplified
amplified Echinogorgia
Echinogorgia coral
coral sample
sample was
was up-
uploaded
loaded to thetoNCBI
the NCBI database
database to obtain
to obtain the genethesequence
gene sequence
number,number,
as shownasinshown in A.
Appendix
Appendix
The A. The gene
gene sequences of thesequences of thecompared
samples were samples were
with compared withusing
and screened and NCBI’s
screenedNu-
using BLAST
cleotide NCBI’s software
Nucleotide BLAST software (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PR
(https://blast.ncbi.nlm.nih.gov/Blast.cgi?PROGRAM=blastn&
OGRAM=blastn&PAGE_TYPE=BlastSearch&LINK_LOC=blasthome,
PAGE_TYPE=BlastSearch&LINK_LOC=blasthome, accessed on 12 March accessed on 12
2023), andMthe
arch 2023), and the corresponding gene fragment information screened in
corresponding gene fragment information screened in the NCBI database was used in the the NCBI
database was used in the MEGA7.0 software. The K2P model and NJ method wer
MEGA7.0 software. The K2P model and NJ method were used to model the phylogenetic
e used to model the phylogenetic trees of the COI gene, mtMuts gene, and ITS1 ge
trees of the COI gene, mtMuts gene, and ITS1 gene, respectively. The confidence level
was derived from 1000 non-parametric bootstrap analyses. The specific phylogenetic trees
of the COI gene, mtMuts gene, and ITS1 gene depicted the evolutionary lineages of the
different species. The results of the phylogenetic trees are shown in Figure 7 (the login
numbers in parentheses in the figure represent the samples of this study).
 e phylogenetic trees are shown in Figure 7 (the login numbers in parentheses in th
e figure represent the samples of this study).
Figure 7a depicts a phylogenetic tree that was established using COI gene sequences.
From the figure, it can be concluded that the COI gene sequence can be used to distinguish
the class of the genus Echinogorgia from the other genus. Our molecular phylogenetic anal-
Water 2023, 15, 3547 11 ofE.
ysis showed that E. sp1, E. sp2, E. sp4, E. sp5, E. ramosa, E. flexilis, E. sp6, E. sp7, E. sp8, 21

sp9, E. sp10, E. ramulosa, and E. gracillima are genetically closer.

(a) (b)

(c)
Figure 7. NJ phylogenetic tree: (a) Based on fragments of the COI gene sequences; (b) Based on
Figure 7. NJ phylogenetic tree: (a) Based on fragments of the COI gene sequences; (b) Based on
fragments of the mtMuts gene sequence; (c) Based on fragments of the ITS1 gene sequences.
fragments of the mtMuts gene sequence; (c) Based on fragments of the ITS1 gene sequences.

Figure 7b depicts
Figure 7a depictsaaphylogenetic
phylogenetictree
tree established
that using using
was established mtMutsCOIgene
genesequences.
sequences.
From
From the figure, it can be concluded that the COI gene sequence can be usedused
the figure, it can be concluded that the mtMuts gene sequence can be to distin-
to distinguish
the class of the genus Echinogorgia from the other genus. Our molecular phylogenetic
analysis showed that E. sp1, E. sp2, E. sp4, E. sp5, E. ramosa, E. flexilis, E. sp6, E. sp7, E. sp8,
E. sp9, E. sp10, E. ramulosa, and E. gracillima are genetically closer.
Figure 7b depicts a phylogenetic tree established using mtMuts gene sequences. From
the figure, it can be concluded that the mtMuts gene sequence can be used to distinguish the
class of the genus Echinogorgia from the other genus. Our molecular phylogenetic analysis
showed that E. ramulosa, E. gracilima, E. russelli, E. sp10, E. sp9, E. sp8, E. sp7, E. sp6, E.
flexilis, E. ramosa, E. sp5, E. sp4, E. sp1, and E. sp3 are genetically closer.
Figure 7c is a phylogenetic tree established based on the ITS1 gene sequence. From
the figure, it can be concluded that the ITS gene sequence can be used to distinguish the
Water 2023, 15, 3547 12 of 21

species of the genus Echinogorgia. Our molecular phylogenetic analysis showed that E. sp4,
E. russelli, E. ramulosa, E. sp2, and E. sp3 are genetically closer.

4. Discussion
4.1. Key Points for the Morphological Identification of the Genus Echinogorgia
The external characteristics are the main basis for the classification and identification
of Octocorallia corals. The characteristics—such as coral specimens (color, branching, size,
and the distribution of the coral), polyps (shape during relaxation and contraction), and
sclerites (shape, size, and color)—were observed [22,31,32,41,46]. The living coral sample
with the sample number of 20210423-QY-33 was found to be reddish-brown. Most of the
branches were on the same plane. There were a few anastomoses between the branches.
The branches were irregular and mainly distributed on one side of the main trunk. The
polyps contained straight or curved spindle-shaped sclerites, and the coenenchymata
contained leaf-shaped sclerites and a small number of pan-shaped sclerites. In the original
literature of the species of Econogorgia ramosa (Thomson and Henderson, 1905), it was
described that the coral body contains a large number of branches, some of which are
anastomosed. In addition, the polyps contain spindle-shaped sclerites, the coenenchymata
contain leaf-shaped sclerites and pan-shaped sclerites, and the color of the coral body is
brick-red [47]. After comparing the morphological characteristics of the coral sample with
the original literature description and image of E. ramosa (Thomson and Henderson, 1905),
it was identified as E. ramosa (Thomson and Henderson, 1905).
The coral sample with the sample number 20210423-QY-27 had a fan-shaped coral
body, branching coral bodies, and small gaps between the polyps. The calyx protruded and
appeared in a dome-like shape. The polyps were distributed with straight or slightly spindle-
shaped sclerites. The surface of the coenenchymata contained leaf-shaped, pan-shaped, and
irregular-shaped sclerites. The leaf-shaped sclerites contained serrated edges, and the surface
of the sclerites contained warty projections. The inner layer of the coenenchymata contained
multiple sclerites. The original literature on the species described that the coral body is
fan-shaped, the coral body is branched, the calyx is prominent, the polyps are distributed
with spindle-shaped sclerites, and the symphysis contains multiple sclerites in Econogorgia
flexilis (Thomson and Simpson, 1909) [48]. The morphological characteristics of the coral body
with the sample number 20210423-QY-27 corresponded to the original literature, and it was
identified as the species of E. flexilis (Thomson and Simpson, 1909).
The sample number was found to be 20210423-WY-15. The living colonies exhibited
dense branching with anastomoses between the branches. The branches were irregular
and grew upward and downward. Most of the branches were at right angles. The polyps
contained columnar- and spindle-shaped sclerites, and the outer layer of the common flesh
contained leaf-shaped bone needles. The coenenchymata in the inner layers contained
quadrangular sclerites. The morphological description of its coral body, branches, and the
sclerites of polyps corresponded to that described in the original literature of Econogorgia
ruselli (Bayer, 1949). Its coral body was found to be upright, and the coral body had many
branches with many anastomoses between the branches and curved branches; in addition,
many of the branches were at right angles. The polyps contained spindle-shaped sclerites,
and the coenenchymata contained multi-shoot-shaped sclerites [47]. Therefore, the sample
with sample number 20210423-WY-15 was identified as E. russelli (Bayer, 1949).
The sample with the sample number 20210423-WY-6 was found to have a branching
coral body with abundant short branches. The small branches were at right angles to
the main branch, and the end of the short branch was slightly enlarged. The calyx pro-
truded, resembling a circle, and the polyps contracted into the calyx. The polyps contained
columnar- and spindle-shaped sclerites that were about 0.1–0.4 mm long. They also had flat
spindle-shaped sclerites, and the surface of the sclerites contained more verrucous protru-
sions. The surface layers of the coenenchymata contained leaf-shaped and irregular-shaped
sclerites with a length of approximately 0.1–0.2 mm. The inner layers of the coenenchymata
contained multiple spicules with a length of approximately 0.1–0.15 mm. In the original
Water 2023, 15, 3547 13 of 21

literature of Echinogorgia ramulosa (Gray, 1870), the coral was described as having a branch-
ing shape, rich branches, as well as especially short and small branches with right angles
between the branches and ends. The polyps are distributed on the surface of twigs. The
calyx protrudes. The polyps contain spindle-shaped sclerites with a length of 0.08–0.3 mm.
The surface of the sclerites contains many warty projections [49]. By comparing the morpho-
logical description of sample number 20210423-WY-6 with the description of the original
literature on E. ramulosa (Gray, 1870) [50], it was identified as E. ramulosa (Gray, 1870) [50].
Sample number 20210423-WY-11 showed a fan-shaped coral body with a height of
10 cm and had abundant and overlapping branches. There were a large number of lateral
branches on one plane, and the ends of the branches were slightly enlarged. The polyps had
a diameter of about 0.5 mm and protruding coral calyxes. The polyps contained columnar-
and spindle-shaped sclerites, which were about 0.1–0.25 mm long. The sclerites contained
verrucous protrusions, and some spindle-shaped sclerites were bifurcated at one end. The
leaf-shaped sclerites were shown on the outer layers of the coenenchymata, while the inner
layers of the coenenchymata contained radiating sclerites, which were colorless. The coral
living organisms were yellow. In the original literature description of Echinogorgia gracilima
(Kükenthal, 1917), the coral bodies had numerous lateral branches on a plane. The branch
parts overlapped. The polyps were small. The distance between the polyps was about 1 mm,
and the diameter was about 0.5 mm. The sclerites of the coral polyps were spindle-shaped
with a length of 0.18 mm. The sclerites contained warty protrusions, and the coenenchymata
contained leaf-shaped sclerites [51]. The morphological description of the sample with
sample number 20210423-WY-11 corresponded to the original literature description of E.
gracilima (Kükenthal, 1917); as such, it is identified as E. gracilima (Kükenthal, 1917).
As of 2 May 2023, WORMS (https://www.marinespecies.org, accessed on 2 March
2023) has recorded 42 valid species of this genus. After collecting and organizing the
relevant original literature on forty-two species, it was found that the original literature
on seven of the species could not be collected, and the original literature on nineteen of
the species did not attach a species comparison map. In addition, the original literature
describing the species of the genus Echinogorgia also had certain limitations such as sim-
plistic morphological descriptions, a lack of corresponding example maps, and incomplete
literature [20,52,53]. This made it difficult for certain samples to be identified as certain
species through their morphology alone. Therefore, there are still 10 undetermined species
in this study.
In addition to the corals of this genus, the identification of other genera was also
the same, let alone for those at the family level. Koido et al. [54] mentioned that species
identification is difficult due to the high morphological variability and plasticity of the
Xeniidae family. Regarding the classification of Chrysogorgia, Untiedt et al. [55] believed that
morphological information is still needed for taxonomic revisions. In particular, species
identification relies on the observation of subtle features that are not easily accessible to
non-experts. Furthermore, phenomena such as homogeneous traits, subtle differences, and
environmental changing forces may blur the boundaries of coral species [56–58].
The descriptions of many octocorals still rely on morphological evidence, and an inte-
grated approach is clearly needed but not yet prevalent [59]. Untiedt et al. [55] mentioned
that an integrated approach assessing morphological and molecular variation is needed to
address classification issues. Information integration is often considered the key to alleviat-
ing octocoral taxonomic problems [60–62]. The integration of genetic and morphological
data is often considered key to mitigating taxonomic issues in octocorals [60–62]. As early
as 2001, the scholar Bayer mentioned that new technologies in molecular analysis will allow
for the possibility of solving the concept of species and genus, especially in problems that
change with long-distance changes in geographical and ecological conditions [63].

4.2. Phylogenetic Analysis of the Genus Echinogorgia

Various molecular markers, such as mtMuts, ND2, and 28S rDNA have been used to
differentiate octocoral species [64–67]. Few molecular phylogenetic analyses of xeniids have
Water 2023, 15, 3547 14 of 21

been performed at the species level. Therefore, COI, mtMuts, ND2, and 28S rDNA were
used to compare some of the genera of xeniids. However, there are still some problems and
limitations [64]. Furthermore, molecular techniques require large amounts of high-quality
DNA, and the need to extract it from recently collected material is critical [68,69].
Given the challenges faced in the morphological identification of certain genera of
coral species in Octocorallia, many scholars have conducted phylogenetic analysis on
coral species to further clarify their species relationships and to help confirm their species
status. Quattrini et al. [70] established a phylogenetic tree based on mtMuts and 28S
rRNA gene sequence fragments for the purposes of phylogenetic analysis, but the results
were inconsistent with the morphological results. Arrigoni et al. [71] used COI gene
fragments for molecular markers to study the molecular biology of coral species in the
Indian Ocean; however, these also differed from the morphological results. Through the
specific amplification and sequencing of COI genes, Li et al. [34] compared and analyzed
the sequence of COI gene fragments of eight species of corals in Xuwen Island. They
clearly pointed out that the traditional morphological classification results differed slightly
from the results of their molecular phylogenetic analysis [34]. Therefore, the classification
and identification of the corals required a combination of morphology descriptions and
molecular biology [18,72].
(1) In this study, the phylogenetic analysis of the genus Echinogorgia, the COI gene
sequence fragments, and the mtMuts gene sequence fragments could only be identified
as a genus class, while the ITS gene sequence fragments could be identified as a species
class. The phylogenetic analysis of corals in the study Nehoray et al. [73] in the Eilat Sea
area of the Red Sea used the COI gene. That analysis identified 14 families, 39 genera, and
94 species. In the paper of Li et al. [74], the phylogenetic relationships of eight species of
scleractinian corals were analyzed using mitochondrial COI genes. The results showed that
the COI gene sequence fragments could identify the species class of the scleractinian corals,
but there were certain differences in terms of morphological identifications. Zhou et al. [75]
selected the mitochondrial msh1 gene and COI gene sequences for species identification
when identifying the Alcyonacea of Sarcophyton in the sea area near Hainan Island. The
results showed that, of the twenty-six samples collected, five species were identified.
Xiao et al. [76] used ITS gene fragments to study the evolutionary relationship of the
scleractinian coral systems in the outer Lingding Island, and the results showed that the
ITS gene fragment could help with identifying the species class. Xie et al. [35] used the ITS
gene to analyze the phylogenetic relationship of scleractinian corals in the waters of the
Dapeng Peninsula. The results showed that ITS could help with identifying the species
class, but there was a significant difference found in comparison with the morphological
characteristics. According to current research, ITS gene fragments are mainly used for the
phylogenetic analysis of coral. In this study, ITS gene fragments were used for a systematic
analysis of the coral collected from Xiamen Bay, and the results showed that the ITS gene
fragment could help with identifying the species class. Further research and analysis are
required to test the application of ITS gene fragments in the coral species.
(2) For a phylogenetic analysis of corals of different genera, it is necessary to identify
the characteristic gene fragments of that genus. With the rapid development of molecular
biology, the use of DNA barcoding technology has become an important method of genetic
differentiation among closely related species [77,78]. However, at present, DNA barcoding
is not applicable to the identification of all coral species. In this study, only ITS gene
fragments were applicable to the differentiation of the species of the genus Echinogorgia,
while COI gene sequence fragments and mtMuts gene sequence fragments are applicable to
the differentiation of Echinogorgia. The selection of DNA barcoding is particularly important
for coral species identification.
Water 2023, 15, 3547 15 of 21

(3) Global coral researchers are needed to jointly improve coral molecular information
in the NCBI database. As of February 2023, in the NCBI database, there are thirty instances
of molecular sequence data regarding the genus Echinogorgia, including five COI and
eight mtMuts gene sequences. Most of them are the undetermined species of the genus
Echinogorgia’s gene. In this paper, the species information of the genus Echinogorgia are
compared and screened in the NCBI database, based on the COI gene sequence fragments.
The mtMuts gene sequence fragment was used to establish a phylogenetic tree for the
phylogenetic analysis of the species of the genus Echinogorgia, which was then validated
through morphological results. Further research is needed to enrich the molecular data
information of the species in the genus Echinogorgia.
Recently, new techniques such as the target capture enrichment of ultra-conserved
elements are often considered and used [79–84]. This technology has advantages over
traditional sequencing methods such as RAD-seq [55]. Erickson et al. [83] believed that new
approaches to coral species delineation are needed to overcome certain challenges. Bound-
aries and group structure within species of two octocoral genera (Alcyium and Sinularia)
were tested by using the method described above. Quattrini et al. [84] advised that target
enrichment methods have shown effectiveness in resolving relatively old phylogenetic
relationships. In the future, the use of target enrichment methods in terms of phylogenetic
relationships may be considered and applied.

4.3. Distribution of Species in the Genus Echinogorgia

The species of the Echinogorgia genus are mainly distributed in Hong Kong, Germany,
the Indian Ocean, and other such places [21]. According to certain reports, seven species of
this genus have been found, including E. pseudosassapo, E. ridley [22], E. sassapo, E. furfuracea,
E. complexa, E. aurantiaca, and E. lami in the offshore waters of China [8,11,23]. Among them,
E. pseudosasapo and E. ridley inhabit the offshore waters of Taiwan, while the rest inhabit the
shallow waters along the coast of Fujian. Moreover, E. complexa, E. pseudosasapo, and E. lami are
also distributed in the waters of Hong Kong [85]. E. pseudosasapo is distributed in the offshore
waters of Hong Kong, Taiwan and in the shallow waters of Fujian. The results show that
most of the discovered species of Echinogorgia in China’s offshore waters are distributed in
the shallow waters off the coast of Fujian. However, the answer as to whether other coastal
waters in China are inhabited by Echinogorgia species remains to be determined.

4.4. Management Recommendations

The global decline in coral cover has resulted in serious consequences, thereby re-
quiring a reflection and evaluation of current management measures [86]. The health and
abundance of coral cover are declining for many reasons, including overfishing, climate
change, runoff pollution, plastic pollution, coastal construction, and dynamite fishing [87].
Jones et al. [88] showed that fish biodiversity is also threatened whenever permanent reef
degradation occurs. From single corals (e.g., genetics, reproduction, and physiology) to
coral populations, reef communities, and ecosystems, a variety of coral reef restoration
approaches are currently being pursued [89]. Species identification and verification are,
therefore, necessary for coral ecosystem management. This fundamental task in species
identification in corals has not yet been fully scientifically described. In this study, the
newly recorded species of Echinogorgia were revealed to have contributed to enriching
the diversity of coral species in China. However, this type of meaningful information
still requires attention to successfully complete complicated tasks in the future. Clearly,
the work on coral population management techniques—which include the parameters of
population status, as well as population dynamics and assessment—is rather limited.
Water 2023, 15, 3547 16 of 21

Hein et al. [89] referred to the National Academies of Sciences, Engineering, and
Medicine (NASEM), as well as the Reef Restoration and Adaptation Program (RRAP),
as examples of some of the interventions that could improve the physiological resilience
of coral to climate change [90,91]. Eleven conservation zones, with corals as the main
protection targets, have been established and implemented in nature reserves in China [92].
In China, 11 nature reserves with coral as the main protection target have been established
and implemented [92]. One of them is located in the Dongshan Coral Nature Reserve in
Fujian [93]. Effective conservation measures have been demonstrated in the establishment
of these protected areas. Therefore, it appears advisable to establish similar coral protection
areas in coral distribution and concentration areas in Xiamen Bay. According to the World
Resources Institute [94] report, an estimated 2679 coral reef areas worldwide have marine
protected areas (MPAs), which account for about 27% of all reef areas. Fernandez et al. [95]
identified certain key success factors in protected area measures, including communication
on the issues to be solved, organizing independent experts, extensive and participatory
consultations, obtaining high-level support, and solving fishermen problems. To address
the need for coral conservation, MPA managers need to understand why MPAs were
created, the state and status of their resources, the forces that are impacting their future
the most, as well as the essential management actions, equipment, people, and facilities
required. Once MPAs have been established, it is important to determine how to promote
and adapt the relevant management efforts [96]. Therefore, after the establishment of
coral protection areas, the protection of coral species diversity in Xiamen Bay will need be
implemented, including the establishment of a network of protection areas, strengthening
the fishing management of fishermen, reducing land-based pollutants, and eliminating
illegal coral fishing.

5. Conclusions
Xiamen Bay is a sea area with typical ecological characteristics and extremely high
biodiversity. Understanding the diversity of coral species is crucial. This study has added
the identification of 15 new species of the genus Echinogorgia, including E. ramosa, E. flexilis,
E. russelli, E. ramulosa, and E. gracilima, which are new recorded species in Xiamen Bay and
also in China. The morphological description and molecular analysis of these five species
can also provide reference for other scholars to study the species of this genus. The results
have also enriched the coral record. We believe that, based on the existing research results,
government authorities should direct their attention and should design specific measures
for coral protection as soon as possible in order to protect precious coral ecologies.

Author Contributions: Conceptualization, Y.-P.W. and J.-Y.L.; methodology, Y.-P.W. and J.-Y.L.;
software, Y.-P.W., J.-Y.L., J.Y. and T.-J.C.; validation, Y.-P.W. and J.-Y.L.; investigation, J.-Y.L., Y.-P.W.
and J.Y.; resources, J.-Y.L.; data curation, Y.-P.W. and J.-Y.L.; writing—original draft preparation,
J.-Y.L. and Y.-P.W.; writing—review and editing, T.-J.C. and J.-Y.L.; visualization, Y.-P.W. and J.-Y.L.;
supervision, J.-Y.L.; project administration, J.-Y.L.; funding acquisition, J.-Y.L. All authors have read
and agreed to the published version of the manuscript.
Funding: This research was funded by the Natural Science Foundation of Fujian Province (No.
2019J01690), Xiamen Ocean and Fishery Bureau (Southern Center Project) (No. 13GQT001NF14), and
National Foundation Incubation Program of Jimei University (No. ZP2020021).
Data Availability Statement: Not applicable.
Acknowledgments: We thank Shi Yi-Jia for her suggestions and contributions to the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
Water 2023, 15, 3547 17 of 21

Appendix A

Table A1. The GenBank accession numbers and reference species involved in this study.

Number Species GenBank Accession Number Gene Segment

1 Echinogorgia sp1 OQ001251
2 Echinogorgia sp2 OQ001252
3 Echinogorgia sp4 OQ001253
4 Echinogorgia sp5 OQ001254
5 Echinogorgia ramosa OQ001255
6 Echinogorgia flexilis OQ001256
7 Echinogorgia sp6 OQ001257
8 Echinogorgia sp7 OQ001258 COI
9 Echinogorgia sp8 OQ001259
10 Echinogorgia sp9 OQ001260
11 Echinogorgia sp10 OQ001261
12 Echinogorgia ramulosa OQ001262
13 Echinogorgia gracillima OQ001263
14 Echinogorgia sp. MW401652.1
15 Echinomuricea sp. KC984637.1
16 Echinogorgia sp1 OQ061094
17 Echinogorgia sp3 OQ061095
18 Echinogorgia sp4 OQ061096
19 Echinogorgia sp5 OQ061097
20 Echinogorgia ramosa OQ061098
21 Echinogorgia flexilis OQ061099
22 Echinogorgia sp6 OQ061100
23 Echinogorgia sp7 OQ061101 mtMuts
24 Echinogorgia sp8 OQ061102
25 Echinogorgia sp9 OQ061103
26 Echinogorgia sp10 OQ061104
27 Echinogorgia russelli OQ061105
28 Echinogorgia ramulosa OQ061106
29 Echinogorgia complexa HQ694670.1
30 Echinogorgia complexa HQ694668.1
31 Echinogorgia sp1 OQ002388
32 Echinogorgia sp2 OQ002387
33 Echinogorgia sp3 OQ002389
34 Echinogorgia sp8 OQ002390
ITS1
35 Echinogorgia russelli OQ002405
36 Echinogorgia ramulosa OQ002404
37 Menella indica OP984327
38 Euplexaura sp2 OQ002379

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