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Article

Epizoans on Floating Golden Tide Macroalgae in the Southern Yellow Sea

by
Jing Xia
1,2,†,
Chongxiang Li
2,†,
Yiyuan Tang
2,
Ji Li
1,3,*,
Tingjian Wu
2,
Jinlin Liu
2,* and
Jianheng Zhang
2,4,*
1
School of Oceanography, Shanghai Jiao Tong University, Shanghai 200030, China
2
College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China
3
Shanghai Frontiers Science Center of Polar Science (SCOPS), Shanghai 200030, China
4
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2023, 11(3), 479; https://doi.org/10.3390/jmse11030479
Submission received: 24 January 2023 / Revised: 13 February 2023 / Accepted: 18 February 2023 / Published: 23 February 2023
(This article belongs to the Special Issue New Insights in the Study of Harmful Algal Bloom)
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Versions Notes

Abstract

:
Golden tide macroalgae have been accumulating in the Southern Yellow Sea (SYS) for several years, causing serious damage to local coastal economy and ecosystems. However, little is known about the environmental and ecological significance of the epizoans drifting on the floating macroalgae. In this study, floating macroalgae collected from four stations were identified as Sargassum horneri. Furthermore, morphological and molecular (based on the Cytochrome C Oxidase Subunit I, COI) identification revealed that the 28 epizoans on the macroalgae consisted of four crustacean (Ampithoe lacertosa, Idotea metallica, Apohyale sp., and Peramphithoe tea). Apohyale sp. and P. tea were found at all stations, while A. lacertosa is found at only one station. The weight range of Apohyale sp., P. tea, I. metallica, and A. lacertosa is 0.0037~0.0420 g, 0.0057~0.0304 g, 0.0222~0.6592 g, and 0.0047 g, respectively. The specific roles of these epizoans in the golden tide in SYS deserve further study. Our results provide a reference for future studies of invasive macroalgae and epizoans.

1. Introduction

In recent years, fast-growing macroalgal blooms have occurred frequently all over the world, particularly in developed countries and developing countries undergoing rapid industrialization [1,2,3,4,5]. Frequent macroalgal blooms may cause the degradation of the coastal ecosystems and are detrimental to local aquaculture development, tourism, and other economic activities [6,7,8,9,10]. In China, some largest macroalgal blooms have been reported [11,12], mainly due to the proliferation of macroalgae or irregular offshore macroalgal aquaculture activities [13,14,15]. The causes of macroalgal blooms are likely related to global warming and eutrophication [16,17,18,19].
Blooms of macroalgae Ulva and Sargassum, often called the green and golden tides, have been the most reported in the world [20,21,22]. In China, green tides have been occurring for many years [23,24,25,26,27] while golden tides have bloomed more frequently in the Southern Yellow Sea (SYS) in recent years [18,28,29,30]. Massive golden tides have accumulated in offshore aquaculture areas (e.g., Neopyropia and Saccharina raft aquaculture areas and fish farms), causing substantial economic losses [18,31,32]. Additionally, the decay of massive macroalgae biomass accumulated in the intertidal zones of the Shandong and Jiangsu provinces resulted in the emission of toxic gases such as H2S. Consequently, pollution negatively impacts the coastal environment and human health [33].
To date, few studies on the golden tide have mainly focused on the benthic and floating macroalgae [9,31,32,34,35] or the diversity of their symbiotic microorganisms [36]. Epizoans (specifically epizoan communities constituted of small invertebrates), such as amphipods, isopods, polychaetes, and echinoderms, transfer the primary production to higher-level consumers and are critical links in the marine food chain, and play a vital role in ecosystems’ material cycling and energy flow [37,38,39]. Macroalgae serve as epizoans’ feeding grounds, habitats, and sanctuaries [40,41]. The epizoans feed on the surface debris and microorganisms from the thalli [38,42,43], promoting the growth of macroalgae. Therefore, the epizoan community is an essential part of macroalgae-based ecosystems. However, in general terms, there are few information on the composition of the epizoan community inhabiting the golden tides.
The combination of morphological and molecular biological species identification technology has been a powerful methodology for species identification [39]. Among the molecular techniques available, DNA barcoding identification technology is a commonly-used reliable method [44,45,46]. For the Phaeophyta, the Cytochrome C Oxidase Subunit I (COI), COIII, Internally Transcribed Spacer gene (ITS), 23S rDNA (23S), and Large Subunit of Ribulose 1,5 Bisphosphate Carboxylase (rbcL) genes are typically used for DNA barcoding [32,47,48,49]. For epizoans, researchers use the COI, 16S rDNA (16S), 18S rDNA (18S), and 28S rDNA (28S) genes for species identification [39,50,51].
In this study, we used morphological and molecular (COI gene) identification techniques to identify floating macroalgae [47,52] and epizoans [50] collected from the SYS. The frequency of occurrences of epizoans from each station was counted, and the fresh weight of the collected sample was also measured. We also assessed the diversity of epizoans living on the floating golden tide macroalgae and evaluated their roles in the floating macroalgal ecosystem.

2. Materials and Methods

2.1. Sample Collection of Macroalgae and Epizoans

Samples were collected on a research cruise from 22–25 March 2021, offshore in Jiangsu Province. Macroalgae and epizoan samples were taken at four stations (2021SYSA; 2021SYSB; 2021SYSC; 2021SYSD) in the SYS on March 25 (Figure 1); the macroalgae were identified as Sargassum on-site based on morphological observation [53] (Figure 1).
Thalli of macroalgae were collected onto the deck with grappling hooks and cleaned with filtered seawater by using the Vacuum Pump filter (GM-0.33A, Jinteng, Tianjin, China) and filter membrane (0.45 µm, Xinya, Shanghai, China). Meanwhile, 0.5 kg of macroalgae material was stored at 4 °C (BD-138W, Haier Group, Qingdao, China). All epizoans were separated from the macroalgae by sterilized tweezers and numbered, and the fresh weight was weighed using an electronic balance (AL-104, Mettler Toledo, Switzerland), and preserved in a prepared 75% alcohol solution (A500737-0005, Sangon Biotechnology Co., Ltd., Shanghai, China). For subsequent morphological and molecular biology identification, samples were transported back to the laboratory at 4 °C (HYUNDAI-6L, Hyundai Group, Seoul, South Korea).

2.2. Morphological and Molecular Identification of Macroalgae

The macroalgae sample were further identified, and pictures of morphological characteristics were recorded using a Nikon camera (D5600, Nikon Corporation, Tokyo, Japan). Per sample, 0.3 g of fresh algae biomass was separated from three single thalli from each station. A total of 12 samples were processed for molecular identification by DNA barcoding. After grinding the samples in liquid nitrogen (Sangon Biotechnology) using a mortar and pestle, the DNA from the samples were extracted using the Ezup Spin Column Super Plant Genomic DNA Extraction Kit (Sangon Biotechnology) following manufacturer’s instructions. The COI sequences were amplified through polymerase chain reaction (PCR) with forwarding primer GazF1 (5′-TCAACAAATCATAAAGATATTGG-3′) [54] and reverse primer R686 (5′-CCACCWGMAGGATCAA-3′) [55]. The 50 µL PCR reaction volume contained 25 µL of 2 × PCR-mix, 19 µL of dd-H2O, 2 µL of each primer (10 mM), and 2 µL of DNA. The PCR amplification protocol featured an initial denaturation at 94 °C for 1.5 min, followed by 40 cycles at 94 °C for 30 s, 47 °C for 40 s, and 72 °C for 40 s, and a final extension at 72 °C for 5 min [56] using an Applied Biosystems device (Thermo Fisher Scientific, Singapore). Amplicon size was confirmed by 1% agarose gel electrophoresis (PowerPac Basic & Gel DocTM XR+ with Image LabTM Software, Bio-Rad Laboratories, Hercules, CA, USA); all qualified PCR products were sent to Sangon Biotechnology for sequencing.
The obtained sequences were checked using BioEdit sequence software [57]. The sequences were compared by the Basic Local Alignment Search Tool (BLAST) of the National Center for Biotechnology Information (NCBI, https://www.ncbi.nlm.nih.gov/, accessed on 4 February 2022) database to identify the species composition of the golden tide macroalgae. To further identify species based on DNA barcoding, the COI sequences of Sargassum species (S. horneri, Sargassum fusiforme, Sargassum confusum, Sargassum fallax, Sargassum muticum, and Sargassum thunbergii) were downloaded from the NCBI database for comparisons of COI sequences present identity similarity based on BLAST results (Table 1). Neopyropia yezoensis, also known as Pyropia yezoensis [58], was chosen as the outgroup for subsequent analysis (Table 1). All sequences were aligned using the MEGA 11 program [59] based on the Maximum Composite Likelihood (MCL) method with the Tamura–Nei model [60], and the phylogenetic tree was optimized using the iTOL database (https://itol.embl.de/, accessed on 4 February 2022) [61]. After establishing the phylogenetic tree, the COI sequences of the 12 samples were uploaded to NCBI, and GenBank accession numbers were obtained subsequently (Table 1).

2.3. Morphological and Molecular Identification of Epizoans

The preliminary on-site morphological identifications based on historical literature indicated that the collected epizoans were mainly species of Ampithoidae, Hyalidae, and Idoteidae [65,66,67,68]. In the lab, the 28 epizoans collected from the four stations (8 at station 2021SYSA; 3 at station 2021SYSB; 7 at station 2021SYSC, and 10 at station 2021SYSD) were identified based on morphology. Subsequently, all epizoans were identified by DNA barcoding. The DNA from the samples were extracted by the Ezup Column Animal Genomic DNA Purification Kit (Sangon Biotechnology) and PCR amplified. The COI sequences of Amphipoda were amplified with forward primer COI-F (5′-GGTCAACAAATCATAAAGATATTGG-3′) and reverse primer COI-R (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′) [39]. The PCR cycle was: predenaturation at 94 °C for 4 min, followed by 30 cycles at 94 °C for 30 s, 45 °C for 30 s, and 72 °C for 30 s, and a final extension at 72 °C for 5 min [39]. Meanwhile, the COI sequences of Isopoda were amplified with forward primer LCO1718 (5′-TWGGDGCNCCDGAYATGGCHTTYCCDCG-3′) and reverse primer HCO2386 (5′-AAAATTTTAATTCCAGTAGGAACTGCAATAATTAT-3′) [69]. The PCR cycle was: predenaturation process at 95 °C for 2 min, following by 41 cycles at 95 °C for 50 s, 45 °C for 1 min 30, 72 °C for 1 min 30 s, and a final extension at 72 °C for 10 min [69]. The PCR reaction volume was 40 µL and contained 20 µL of 2× PCR-mix, 15.5 µL of dd-H2O, 1.5 µL of each primer (10 mM), and 1.5 µL of DNA. Then all PCR amplification products were produced using the Applied Biosystems device. The agarose gel electrophoresis, sequencing, sequence checking, and BLAST processes were the same as those described above in Section 2.2.
To further identify species based on DNA barcoding, the most similar COI sequences of epizoan species (Ampithoe lacertosa, Ampithoe helleri, Apohyale sp., Apohyale cf. pugettensis, Idotea metallica, Idotea emarginata, and Peramphithoe tea) were downloaded from the NCBI database based on BLAST results. Table 2 provides detailed information about these samples. Oratosquilla oratoria [70] was chosen as the outgroup for subsequent analysis (Table 2). The alignment of sequences and construction of the phylogenetic tree were conducted following the processes described in Section 2.2. After establishing the phylogenetic tree, COI sequences of the 28 samples were uploaded to NCBI, and GenBank accession numbers were subsequently obtained (Table 2).

3. Results

3.1. Identification of Macroalgae

The floating macroalgae collected from the four stations were morphologically identified as Sargassum sp., which had the main branch and branched structure (Figure 2a,b), and secondary branches that grew out of the extended leaf axils of the main branch. The top of the thalli had split leaves, and the thalli had a distinct gas bladder structure (Figure 2b,c). The gas bladders grew from the leaf axils and were cylindrical, with spikes at both ends (Figure 2c), and they were often arranged in racemose form. Very few thalli had receptacles, but when present, they were cylindrical and long; both ends were thin (Figure 2d) and grew from the terminal or inner area of the leaf axils [53]. Based on these morphological observations, the samples were preliminarily identified as S. horneri (Section Spongocarpus) [53].
The length of the COI gene sequence obtained from Sangon Biotechnology was about 630 base pairs (bp). After checking and proofreading these sequences, the COI gene sequences of the 12 samples were obtained (each sequence length was 596 bp), available at GenBank, accession numbers are OM444204–OM444215 (Table 1). A comparison of the sequences with those in the NCBI database using BLAST showed that these samples had 100% similarity with S. horneri. The MCL phylogenetic tree further supported the molecular biology identification results. All 12 sequences clustered with S. horneri (KC782896 and KY047195) as the main clade (marked with orange), which was different from the clade of S. fusiforme, S. confusum, S. fallax, S. muticum, and S. thunbergii, with high genetic distance (Figure 3).
Based on the abovementioned detailed morphological and molecular biology identification, the golden tide macroalgae that accumulated in the SYS in the offshore sea area of Jiangsu Province in March 2021 was S. horneri. The taxonomy of this species is Chromista, Ochrophyta, Phaeophyceae, Fucales, Sargassaceae, Sargassum [53].

3.2. Species Composition and Biological Parameters of Epizoans

Morphological and molecular identification results showed that the collected epizoans consisted of four species with the following taxonomy (Table 3, Figure 4). Taxonomic status and distribution are referred to at the Global Biodiversity Information Facility (https://www.gbif.org/, accessed on 10 February 2023). There are fewer reports about these species on floating S. horneri in SYS.
The length of COI standard gene sequences obtained from Sangon Biotechnology were 647, 606, 626, and 653 bp, respectively. The BLAST results of the 28 samples showed the similarity of the obtained sequences with the sequences of A. lacertosa, Apohyale sp., I. metallica, and P. tea from NCBI were 100%, 99.17–99.5%, 97.7%, and 99.39–99.84%. Thus, the epizoans collected from the four stations were 1 A. lacertosa (accounting for 3.6%), 13 Apohyale sp. (46.4%), 6 I. metallica (21.4%), and 8 P. tea (28.6%).
Table 2 provides details about the GenBank accession numbers for the epizoans. The MCL phylogenetic tree supported the molecular biology identification results. The sequence of A. lacertosa clustered with OK480914 (A. lacertosa) as the main clade (marked with gray), which was not the same clade as that of A. helleri (KX223985). The 13 sequences of Apohyale sp. clustered with OK180438 (Apohyale sp.) as the main clade (marked with orange) and were not in the same clade as A. Pugettensis (MG315613). The six sequences of I. metallica clustered with KU530515 (I. metallica) as the main clade (marked with green), which was not the same clade as that of I. emarginata (KU530492). The eight sequences of P. tea clustered with JN575608 (P. tea) as the main clade (marked with blue), and the genetic distance between different species was large (Figure 5). In summary, the richness of epizoans from the floating golden tide macroalgae in the SYS in March 2021 included A. lacertosa, Apohyale sp., I. metallica, and P. tea.
The frequency of occurrence and fresh weight of epizoans from each station were counted and measured (Figure 6 and Figure 7). The fresh weight of amphipods ranged from 0.0037 g to 0.0420 g each, and the weight of isopods ranged from 0.0222 g to 0.6592 g (Figure 7). The eight samples collected from the 2021SYSA station consisted of four Apohyale sp. (accounting for 50%, 0.0044 ~ 0.0204 g) and four P. tea (50%, 0.0112 ~ 0.0304 g) (Figure 6 and Figure 7). One A. lacertosa (accounting for 33.3%, 0.0047 g), one Apohyale sp. (33.3%, 0.0420 g) and one P. tea (33.4 %, 0.0078 g) were collected from the 2021SYSB station (Figure 6 and Figure 7). The seven samples collected from the 2021SYSC station included three Apohyale sp. (42.9%, 0.0112 ~ 0.0248 g), three I. metallica (42.9%, 0.1015 ~ 0.6592 g), and one P. tea (14.2%, 0.0143 g) (Figure 6 and Figure 7). The samples collected from the 2021SYSD station consisted of five Apohyale sp. (50%, 0.0037 ~ 0.0186 g), three I. metallica (30%, 0.0222 ~ 0.1685 g), and two P. tea (20%, 0.0056 ~ 0.0278 g) (Figure 6 and Figure 7). Apohyale sp. and P. tea were found at all stations and the frequency of occurrence is higher, while A. lacertosa is only found at 2021SYSB (Figure 6).

4. Discussion

4.1. Golden Tides in the SYS and the Origin of Blooms

Golden tides are caused by Sargassum spp. in USA, Mexico, Japan, China, South Korea, and Australia [18]. The distribution and coverage areas of golden tides in the SYS of China have been increasing in the recent decade. In 2013, 2015, 2016, 2017, and 2020, large-scale S. horneri blooms were observed in the Yellow Sea [17,18,30,75,76]. These results were consistent with the golden tide macroalgae reported in the SYS in previous years [39], with no changes within the dominant bloom-forming species.
The source of large-scale S. horneri blooms in the Yellow Sea remains unknown, although some evidence points toward two main sources originating in Zhejiang and Shandong Provinces [77,78,79]. During the investigation, local fishermen indicated that the spring-floating S. horneri may come from the coastal areas of Shandong Province and the eastern sea area. Meanwhile, some researchers speculate that benthic populations of S. horneri in the coastal waters of South Korea [78] could be the source of the S. horneri blooms observed in the Yellow Sea. Generally, suitable climatic conditions can promote large-scale proliferation and bloom of benthic S. horneri in seaweed beds and intertidal zones. Human activities, such as removing macroalgae from aquaculture rafts may promote the process of S. horneri floating into the open sea area. Over several decades, seaweed farmers in Shandong and Zhejiang Province periodically removed S. horneri from the aquaculture infrastructure (kelp and mussel rafts) during aquaculture activities. In addition, S. horneri as the dominant species were also used in marine ranching in Shandong, Zhejiang, Fujian Province, etc., which may provide the initial biomass for the golden tide. It is worth noting that more evidence is required for these perceptions, which deserve subsequent attention and in-depth study. The special gas bladder structure of macroalgae is conducive to floating to other sea areas with ocean currents to settle and gradually form local intertidal zone populations [80], which in turn causes new blooms locally. Therefore, the large scale of S. horneri entering the SYS and its origin deserve attention.

4.2. Potential Effects of Epizoans Entering the SYS

Rafting on artificial and natural objects is an important dispersal mechanism for coastal invertebrates [81]. Rafting on macroalgae with gas bladders, which can provide a food source and long survival time [81], is an effective marine dispersal mechanism for epizoans that may have a profound impact on coastal biodiversity [82]. I. metallica is an obligate rafter (as opposed to a facultative rafter) that occurs in the Atlantic, Pacific, Mediterranean, and Black Sea [83]. For this species, rafting is a specific and evolutionarily developed life strategy [84]. The low feeding rates, high assimilation efficiency, and total lipid contents of I. metallica allow it to adapt to long-distance rafting [84]. I. metallica may be used as a sensitive indicator for climate change due to its high natural capacity for dispersal and response to changing environmental conditions [85]. Isopods and amphipods, as important community members in drifting macroalgae [39,83,85], may have potential ecological value. On the one hand, epizoans can indicate environmental changes (e.g., warming) in SYS. On the other hand, epizoans can drift long distances on the macroalgae, which can be used to trace the origin of S. horneri in SYS by comparing the genetic relationships of different epizoan populations. However, there are few studies on the epizoans from floating S. horneri in the Yellow Sea, and population genetic analysis could be carried out with more epizoan sequences in the future.

4.3. Relevance of Epizoans in Marine Ecosystems

Small herbivorous marine invertebrates, also known as mesograzers, are primary consumers that are distributed in almost all marine vegetation habitats, and the top-down control by mesograzers has an important impact on the seaweed communities [37,86] and periphyton biomass [86,87]. Due to their special status in the marine food web, mesograzers have important impacts on both primary producers and higher consumers, and trophically link primary production with fish [88,89].
In this study, we reported four crustacean species belonging to the genera Peramphithoe, Apohyale, Ampithoe, and Idotea on the floating S. horneri in China for the first time. Sano et al. (2003) [90] also found epizoans such as Perampithoe, Amphithoe, and Idotea on floating Sargassum spp. Epizoans fed on floating macroalgae and plankton, and omnivorous epizoans (e.g., Idotea) also fed on crustaceans. In turn, these epizoans are preyed on by other carnivores and large predators [82,83] (Figure 8). In summary, these epizoans and floating macroalgae found in this study constitute a floating community, and herbivorous and omnivorous epizoans promote energy flows that connect primary production by macroalgae and epiphytes with carnivores [90] (Figure 8). Certainly, there may be more epizoans on the floating S. horneri in SYS. The above four species were found in this study, and the ecological flowchart will be improved if more species are found in the future. However, we could not quantify the biomass and density of epizoans because the density of S. horneri was sparse and its surface was difficult to salvage when using common nets for collection. Moreover, grappling hooks may have caused epizoans to flee the algal mat. These issues precluded quantitative analysis in our study. In this study, the sample was pulled out of the water by nets and hooks. The epizoan on the macroalgae could be startled, causing an underestimation of the epizoan biomass. To better quantify the epizoan biomass, the sample methods need be improved in future study.
Grazing pressure by mesograzers can influence the abundance of macroalgae in eutrophic waters [91,92]. Apohyale sp. found in this study is considered to be able to reduce the biomass and growth of floating macroalgae [68]. Idotea spp. are observed as active grazers of macroalgae [91]. This study obtained the body weights of each epizoan on floating S. horneri at four stations in the SYS, however, the productivity of these epizoans requires further assessment. Meanwhile, whether the grazing effect of epizoans can decrease the growth of S. horneri during the bloom stage when they are increasing requires further study. Yu et al. (2021) [93] cut ~3 cm long segments from the top of the main branch or lateral branch of S. horneri for culture and found that the carbon and nitrogen contents of the thalli were higher during the growth phase, which might help to resist the stress of unfavorable environments. Wang et al. (2020) [94] reported that low culture density was beneficial to the growth of S. horneri, indicating that S. horneri could grow rapidly when floating on the sea surface. Epizoans may graze macroalgae into small thalli, which would quickly grow under suitable temperature and light conditions.
Furthermore, these epizoans may promote pollination in seaweed. Lavaut et al. (2022) [95] found that Idotea balthica can significantly increase pollination in Gracilaria gracilis by directly transporting spermatia of the thalli. Spermatia can adhere to the cuticles of Idotea that can be transmitted to female thalli by Idotea [95]. A similar process may also occur in the interaction between S. horneri and epizoans (i.e., I. metallica in this study). Idotea may also be able to transport male gametes to promote the reproduction of S. horneri, and contribute to the bloom development.
The SYS is rich in nutrients from different sources [96,97], and suitable hydrological conditions may promote the large-scale proliferation of S. horneri. The interaction between epizoans may also be an important variable. These processes may partially explain the golden tides’ large coverage and distribution areas. However, these hypotheses need to be further studied and confirmed. The initial biomass of floating S. horneri entering the sea and environmental parameters are the primary factors determining the scale of the golden tide, but epizoans drifting into sea areas with S. horneri blooms likely will have a certain impact on the local ecosystem, and the related research still has a long way to go.

5. Conclusions

Combined with morphological and molecular identification, S. horneri was found to be the dominant species of the 2021 golden tide in the SYS. Meanwhile, molecular identification based on COI indicated that 28 epizoans on S. horneri were composed of four crustaceans: A. lacertosa, I. metallica, Apohyale sp., and P. tea. Among them, Apohyale sp. and P. tea were found at all stations, while A. lacertosa with a low frequency of occurrence. Epizoans are an important component of drifting macroalgal ecosystems, which are predicted to have a certain impact on local coastal ecosystems and have potential application value. This study provides a reference for future studies on the ecological significance of golden tide macroalgae in the SYS.

Author Contributions

Conceptualization, investigation and methodology, J.X., C.L., Y.T. and J.L. (Jinlin Liu); resource, T.W.; writing—original draft, J.X. and J.L. (Jinlin Liu); writing—review and editing, funding acquisition, J.L. (Jinlin Liu), J.Z. and J.L. (Ji Li). All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by Shanghai Frontiers Science Center of Polar Science (SCOPS), Technology Innovation Center for Land Spatial Eco-restoration in Metropolitan Area, M.N.R. (CXZX202006), Natural Science Foundation of Shanghai (21ZR1427400), Project of Key Laboratory of Marine Ecological Monitoring and Restoration Technologies, M.N.R. (202003), and National Natural Science Foundation of China (41576163).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Fernandez, C. Boom-bust of Sargassum muticum in northern Spain: 30 years of invasion. Eur. J. Phycol. 2020, 55, 285–295. [Google Scholar] [CrossRef]
  2. Wang, H.; Wang, G.C.; Gu, W.H. Macroalgal blooms caused by marine nutrient changes resulting from human activities. J. Appl. Ecol. 2020, 57, 766–776. [Google Scholar] [CrossRef]
  3. Joniver, C.F.H.; Photiades, A.; Moore, P.J.; Winters, A.L.; Woolmer, A.; Adams, J.M.M. The global problem of nuisance macroalgal blooms and pathways to its use in the circular economy. Algal. Res. 2021, 58, 102407. [Google Scholar] [CrossRef]
  4. Kang, E.J.; Han, A.R.; Kim, J.H.; Kim, I.N.; Lee, S.; Min, J.O.; Nam, B.R.; Choi, Y.J.; Edwards, M.S.; Diaz-Pulido, G.; et al. Evaluating bloom potential of the green-tide forming alga Ulva ohnoi under ocean acidification and warming. Sci. Total Environ. 2021, 769, 144443. [Google Scholar] [CrossRef] [PubMed]
  5. Bermejo, R.; Golden, N.; Schrofner, E.; Knöller, K.; Fenton, O.; Serrão, E.; Morrison, L. Biomass and nutrient dynamics of major green tides in Ireland: Implications for biomonitoring. Mar. Pollut. Bull. 2022, 175, 113318. [Google Scholar] [CrossRef]
  6. Guo, X.N.; Zhu, A.; Chen, R.S. China’s algal bloom suffocates marine life. Science 2021, 373, 751. [Google Scholar] [CrossRef]
  7. Liu, J.L.; Li, C.X.; Xia, J.; Sun, Y.Q.; Tong, Y.C.; Zhang, J.H.; Zhao, S.; Zhuang, M.M.; He, P.M. Epizoic Ulva attached to intertidal animals in the Subei intertidal zone are not the additional source of the famed Yellow Sea green tides. J. Sea. Res. 2021, 174, 102065. [Google Scholar] [CrossRef]
  8. Liu, J.L.; Xia, J.; Zhuang, M.M.; Zhang, J.H.; Yu, K.F.; Zhao, S.; Sun, Y.Q.; Tong, Y.C.; Xia, L.H.; Qin, Y.T.; et al. Controlling the source of green tides in the Yellow Sea: NaClO treatment of Ulva attached on Pyropia aquaculture rafts. Aquaculture 2021, 535, 736378. [Google Scholar] [CrossRef]
  9. Vazquez-Delfin, E.; Freile-Pelegrin, Y.; Salazar-Garibay, A.; Serviere-Zaragoza, E.; Mendez-Rodriguez, L.C.; Robledo, D. Species composition and chemical characterization of Sargassum influx at six different locations along the Mexican Caribbean coast. Sci. Total Environ. 2021, 795, 148852. [Google Scholar] [CrossRef]
  10. Liu, J.L.; Tong, Y.C.; Xia, J.; Sun, Y.Q.; Zhao, X.H.; Sun, J.Y.; Zhao, S.; Zhuang, M.M.; Zhang, J.H.; He, P.M. Ulva macroalgae within local aquaculture ponds along the estuary of Dagu River, Jiaozhou Bay, Qingdao. Mar. Pollut. Bull. 2022, 174, 113243. [Google Scholar] [CrossRef]
  11. Wang, S.Y.; Huo, Y.Z.; Zhang, J.H.; Cui, J.J.; Wang, Y.; Yang, L.L.; Zhou, Q.Y.; Lu, Y.W.; Yu, K.F.; He, P.M. Variations of dominant free-floating Ulva species in the source area for the world’s largest macroalgal blooms, China: Differences of ecological tolerance. Harmful Algae 2018, 74, 58–66. [Google Scholar] [CrossRef]
  12. Hiraoka, M. Massive Ulva Green Tides Caused by Inhibition of Biomass Allocation to Sporulation. Plants 2021, 10, 2482. [Google Scholar] [CrossRef]
  13. Liu, D.Y.; Keesing, J.K.; Xing, Q.U.; Shi, P. World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar. Pollut. Bull. 2009, 58, 888–895. [Google Scholar] [CrossRef]
  14. Han, H.B.; Li, Y.; Ma, X.J.; Song, W.; Wang, Z.L.; Zhang, X.L. Factors influencing the spatial and temporal distributions of green algae micro-propagules in the coastal waters of Jinmenghaiwan, Qinhuangdao, China. Mar. Pollut. Bull. 2022, 175, 113328. [Google Scholar] [CrossRef]
  15. Sun, Y.Q.; Liu, J.L.; Xia, J.; Tong, Y.C.; Li, C.X.; Zhao, S.; Zhuang, M.M.; Zhao, X.H.; Zhang, J.H.; He, P.M. Research development on resource utilization of green tide algae from the Southern Yellow Sea. Energy Rep. 2022, 8, 295–303. [Google Scholar] [CrossRef]
  16. Wu, H.L.; Feng, J.C.; Li, X.S.; Zhao, C.Y.; Liu, Y.H.; Yu, J.T.; Xu, J.T. Effects of increased CO2 and temperature on the physiological characteristics of the golden tide blooming macroalgae Sargassum horneri in the Yellow Sea, China. Mar. Pollut. Bull. 2019, 146, 639–644. [Google Scholar] [CrossRef]
  17. Zhang, J.H.; Shi, J.T.; Gao, S.; Huo, Y.Z.; Cui, J.J.; Shen, H.; Liu, G.Y.; He, P.M. Annual patterns of macroalgal blooms in the Yellow Sea during 2007–2017. PLoS ONE 2019, 14, e0210460. [Google Scholar] [CrossRef]
  18. Liu, J.L.; Xia, J.; Zhuang, M.M.; He, P.M.; Sun, Y.Q.; Tong, Y.C.; Zhao, S.; Zhang, J.H. Golden seaweed tides accumulated in Pyropia aquaculture areas are becoming a normal phenomenon in the Yellow Sea of China. Sci. Total Environ. 2021, 774, 145726. [Google Scholar] [CrossRef]
  19. Xiao, J.; Wang, Z.L.; Liu, D.Y.; Fu, M.Z.; Yuan, C.; Yan, T. Harmful macroalgal blooms (HMBs) in China’s coastal water: Green and golden tides. Harmful Algae 2021, 107, 102061. [Google Scholar] [CrossRef]
  20. Gower, J.F.R.; King, S.A. Distribution of floating Sargassum in the Gulf of Mexico and the Atlantic Ocean mapped using MERIS. Int. J. Remote Sens. 2011, 32, 1917–1929. [Google Scholar] [CrossRef]
  21. Smetacek, V.; Zingone, A. Green and golden seaweed tides on the rise. Nature 2013, 504, 84–88. [Google Scholar] [CrossRef] [PubMed]
  22. Byeon, S.Y.; Oh, H.J.; Kim, S.; Yun, S.H.; Kang, J.H.; Park, S.R.; Lee, H.J. The origin and population genetic structure of the ‘golden tide’ seaweeds, Sargassum horneri, in Korean waters. Sci. Rep. 2019, 9, 7757. [Google Scholar] [CrossRef]
  23. Gao, G.; Zhong, Z.; Zhou, X.; Xu, J. Changes in morphological plasticity of Ulva prolifera under different environmental conditions: A laboratory experiment. Harmful Algae 2016, 59, 51–58. [Google Scholar] [CrossRef] [PubMed]
  24. Feng, Z.; Zhang, T.; Shi, H.; Gao, K.; Xu, J.; Wang, J.; Wang, R.; Li, X.; Gao, G. Microplastics in bloom-forming macroalgae: Distribution, characteristics and impacts. J. Hazard. Mater. 2020, 397, 122752. [Google Scholar] [CrossRef] [PubMed]
  25. Feng, Z.; Zhang, T.; Wang, J.; Huang, W.; Wang, R.; Xu, J.; Fu, G.; Gao, G. Spatio-temporal features of microplastics pollution in macroalgae growing in an important mariculture area, China. Sci. Total Environ. 2020, 719, 137490. [Google Scholar] [CrossRef]
  26. An, D.Y.; Yu, D.F.; Zheng, X.Y.; Zhou, Y.; Meng, L.; Xing, Q.G. Monitoring the Dissipation of the Floating Green Macroalgae Blooms in the Yellow Sea (2007–2020) on the Basis of Satellite Remote Sensing. Remote Sens. 2021, 13, 3811. [Google Scholar] [CrossRef]
  27. Zhang, T.; Wang, J.X.; Liu, D.X.; Sun, Z.W.; Tang, R.K.; Ma, X.; Feng, Z.H. Loading of microplastics by two related macroalgae in a sea area where gold and green tides occur simultaneously. Sci. Total Environ. 2022, 814, 152809. [Google Scholar] [CrossRef]
  28. Liu, F.; Pan, J.; Zhang, Z.S.; Moejes, F.W. Organelle genomes of Sargassum confusum (Fucales, Phaeophyceae): mtDNA vs cpDNA. J. Appl. Phycol. 2018, 30, 2715–2722. [Google Scholar] [CrossRef]
  29. Chen, Y.L.; Wan, J.H.; Zhang, J.; Ma, Y.J.; Wang, L.; Zhao, J.H.; Wang, Z.Z. Spatial-Temporal Distribution of Golden Tide Based on High–Resolution Satellite Remote Sensing in the South Yellow Sea. J. Coastal Res. 2019, 90, 221–227. [Google Scholar] [CrossRef]
  30. Zhang, J.H.; Ding, X.W.; Zhuang, M.M.; Wang, S.Y.; Chen, L.; Shen, H.; He, P.M. An increase in new Sargassum (Phaeophyceae) blooms along the coast of the East China Sea and Yellow Sea. Phycologia 2019, 58, 374–381. [Google Scholar] [CrossRef]
  31. Zhuang, M.M.; Liu, J.L.; Ding, X.W.; He, J.Z.; Zhao, S.; Wu, L.J.; Gao, S.; Zhao, C.Y.; Liu, D.Y.; Zhang, J.H.; et al. Sargassum blooms in the East China Sea and Yellow Sea: Formation and management. Mar. Pollut. Bull. 2021, 162, 111845. [Google Scholar] [CrossRef]
  32. Resiere, D.; Valentino, R.; Neviere, R.; Banydeen, R.; Gueye, P.; Florentin, J.; Cabie, A.; Lebrun, T.; Megarbane, B.; Guerrier, G.; et al. Sargassum seaweed on Caribbean islands: An international public health concern. Lancet 2018, 392, 2691. [Google Scholar] [CrossRef]
  33. Liu, F.; Pang, S.J.; Li, X.; Li, J. Complete mitochondrial genome of the brown alga Sargassum horneri (Sargassaceae, Phaeophyceae): Genome organization and phylogenetic analyses. J. Appl. Phycol. 2015, 27, 469–478. [Google Scholar] [CrossRef]
  34. Liu, F.; Liu, X.F.; Wang, Y.; Lin, Z.; Moejes, F.W.; Sun, S. Insights on the Sargassum horneri golden tides in the Yellow Sea inferred from morphological and molecular data. Limnol. Oceanogr. 2018, 63, 1762–1773. [Google Scholar] [CrossRef]
  35. Li, J.J.; Liu, Z.Y.; Zhong, Z.H.; Zhuang, L.C.; Bi, Y.X.; Qin, S. Limited Genetic Connectivity Among Sargassum horneri (Phaeophyceae) Populations in the Chinese Marginal Seas Despite Their high Dispersal Capacity. J. Phycol. 2020, 56, 994–1005. [Google Scholar] [CrossRef]
  36. Mei, X.Y.; Wu, C.H.; Zhao, J.; Yan, T.; Jiang, P. Community Structure of Bacteria Associated with Drifting Sargassum horneri, the Causative Species of Golden Tide in the Yellow Sea. Front. Microbiol. 2019, 10, 1192. [Google Scholar] [CrossRef]
  37. Duffy, J.E.; Hay, M.E. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr. 2000, 70, 237–263. [Google Scholar] [CrossRef]
  38. Jiang, R.J.; Zhang, S.Y.; Bi, Y.X.; Wang, Z.H. Food sources of small invertebrates in the macroalgal bed of Gouqi Island. J. Fish. China 2015, 39, 1487–1498. [Google Scholar] [CrossRef]
  39. Liu, J.L.; Zhuang, M.M.; Zhao, L.J.; Liu, Y.K.; Wen, Q.L.; Fu, M.L.; Yu, K.F.; Zhang, J.H.; He, P.M. Taxonomy and Genetic Diversity of Amphipods Living on Ulva lactuca L. from Gouqi Coast, China. Pac. Sci. 2020, 74, 137–146. [Google Scholar] [CrossRef]
  40. McDonald, P.S.; Bingham, B.L. Comparing macroalgal food and habitat choice in sympatric, tube-building amphipods, Ampithoe lacertosa and Peramphithoe humeralis. Mar. Biol. 2010, 157, 1513–1524. [Google Scholar] [CrossRef]
  41. Quillien, N.; Nordstrom, M.C.; Le Bris, H.; Bonsdorff, E.; Grall, J. Green tides on inter- and subtidal sandy shores: Differential impacts on infauna and flatfish. J. Mar. Biol. Assoc. UK 2018, 98, 699–712. [Google Scholar] [CrossRef]
  42. Catenazzi, A.; Donnelly, M.A. Role of supratidal invertebrates in the decomposition of beach-cast green algae Ulva sp. Mar. Ecol. Prog. Ser. 2007, 349, 33–42. [Google Scholar] [CrossRef]
  43. Schaal, G.; Leclerc, J.C.; Droual, G.; Leroux, C.; Riera, P. Biodiversity and trophic structure of invertebrate assemblages associated with understorey red algae in a Laminaria digitata bed. Mar. Biol. Res. 2016, 12, 513–523. [Google Scholar] [CrossRef]
  44. Hebert, P.D.N.; Cywinska, A.; Ball, S.L.; DeWaard, J.R. Biological identifications through DNA barcodes. Proc. R. Soc. B Biol. Sci. 2003, 270, 313–321. [Google Scholar] [CrossRef] [PubMed]
  45. Ward, R.D.; Zemlak, T.S.; Innes, B.H.; Last, P.R.; Hebert, P.D.N. DNA barcoding Australia’s fish species. Proc. R. Soc. B Biol. Sci. 2005, 360, 1847–1857. [Google Scholar] [CrossRef]
  46. Chen, L.P.; Chang, Y.G.; Li, J.; Wang, J.M.; Liu, J.L.; Zhi, Y.C.; Li, X.J. Application of DNA Barcoding in the Classification of Grasshoppers (Orthoptera: Acridoidea)—A Case Study of grasshoppers from Hebei Province, China. Zootaxa 2018, 4497, 99–110. [Google Scholar] [CrossRef]
  47. Mattio, L.; Payri, C. Assessment of five markers as potential barcodes for identifying Sargassum subgenus Sargassum species (Phaeophyceae, Fucales). Cryptogam Algol. 2011, 31, 467–485. [Google Scholar]
  48. Yip, Z.T.; Quek, R.Z.B.; Huang, D.W. Historical biogeography of the widespread macroalga Sargassum (Fucales, Phaeophyceae). J. Phycol. 2019, 56, 300–309. [Google Scholar] [CrossRef]
  49. Yip, Z.T.; Quek, R.Z.B.; Low, J.K.Y.; Wilson, B.; Bauman, A.G.; Chou, L.M.; Todd, P.A.; Huang, D.W. Diversity and phylogeny of Sargassum (Fucales, Phaeophyceae) in Singapore. Phytotaxa 2018, 369, 200–210. [Google Scholar] [CrossRef]
  50. Donald, K.M.; Preston, J.; Williams, S.T.; Reid, D.G.; Winter, D.; Alvarez, R.; Buge, B.; Hawkins, S.J.; Templado, J.; Spencer, H.G. Phylogenetic relationships elucidate colonization patterns in the intertidal grazers Osilinus Philippi, 1847 and Phorcus Risso, 1826 (Gastropoda: Trochidae) in the northeastern Atlantic Ocean and Mediterranean Sea. Molec. Phylogenet. Evol. 2012, 62, 35–45. [Google Scholar] [CrossRef]
  51. Linse, K.; Jackson, J.A.; Malyutina, M.V.; Brandt, A. Shallow-Water Northern Hemisphere Jaera (Crustacea, Isopoda, Janiridae) Found on Whale Bones in the Southern Ocean Deep Sea: Ecology and Description of Jaera tyleri sp. nov. PLoS ONE 2014, 9, e93018. [Google Scholar] [CrossRef]
  52. Ng, P.K.; Chiou, Y.S.; Liu, L.C.; Sun, Z.M.; Shimabukuro, H.; Lin, S.M. Phylogeography and genetic connectivity of the marine macro-alga Sargassum ilicifolium (Phaeophyceae, Ochrophyta) in the northwestern Pacific. J. Phycol. 2019, 55, 7–24. [Google Scholar] [CrossRef]
  53. Tseng, C.K.; Lu, B.R. Marine Algal Flora of China Tomus III Phaeophyta Fucales; Science Press: Beijing, China, 2000; pp. 43–44. [Google Scholar]
  54. Saunders, G.W. Applying DNA barcoding to red macroalgae: A preliminary appraisal holds promise for future applications. Phil. Trans. R. Soc. B 2005, 360, 1879–1888. [Google Scholar] [CrossRef]
  55. Sherwood, A.R.; Kurihara, A.; Conklin, K.Y.; Sauvage, T.; Presting, G.G. The Hawaiian Rhodophyta Biodiversity Survey (2006–2010): A summary of principal findings. BMC Plant Biol. 2010, 10, 258. [Google Scholar] [CrossRef]
  56. Du, G.Y.; Wu, F.F.; Guo, H.; Xue, H.F.; Mao, Y.X. DNA barcode assessment of Ceramiales (Rhodophyta) in the intertidal zone of the northwestern Yellow Sea. Chin. J. Oceanol. Limnol. 2015, 33, 685–695. [Google Scholar] [CrossRef]
  57. Hall, T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41, 95–98. [Google Scholar] [CrossRef]
  58. Niwa, K.; Sano, F.; Sakamoto, T. Molecular evidence of allodiploidy in F1 gametophytic blades from a cross between Neopyropia yezoensis and a cryptic species of the Neopyropia yezoensis complex (Bangiales, Rhodophyta) by the use of microsatellite markers. Aquac. Rep. 2020, 18, 100489. [Google Scholar] [CrossRef]
  59. Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
  60. Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512–526. [Google Scholar] [CrossRef]
  61. Ivica, L.; Peer, B. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021, 49, W293–W296. [Google Scholar] [CrossRef]
  62. Zhao, X.B.; Pang, S.J.; Shan, T.F.; Liu, F. Applications of three DNA barcodes in assorting intertidal red macroalgal flora in Qingdao, China. J. Ocean Univ. China 2013, 12, 139–145. [Google Scholar] [CrossRef]
  63. Silberfeld, T.; Leigh, J.W.; Verbruggen, H.; Cruaud, C.; De Reviers, B.; Rousseau, F. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the “brown algal crown radiation”. Mol. Phylogenet. Evol. 2010, 56, 659–674. [Google Scholar] [CrossRef] [PubMed]
  64. Rizzo, C.; Genovese, G.; Morabito, M.; Faggio, C.; Pagano, M.; Spanò, A.; Zammuto, V.; Minicante, S.A.; Manghisi, A.; Cigala, R.M.; et al. Potential Antibacterial Activity of Marine Macroalgae against Pathogens Relevant for Aquaculture and Human Health. J. Pure Appl. Microbiol. 2017, 11, 1695–1706. [Google Scholar] [CrossRef]
  65. Wei, C.D.; Chen, Y.S. Fauna of Zhejiang Crustacea; Zhejiang Science & Technology Press: Hangzhou, China, 1991; 481p. [Google Scholar]
  66. Jiang, N.C.; Lu, J.P. Field Internship Guidance of Zhejiang Coastal Zoology; Zhejiang Universuty Press: Zhejiang, China, 2005; 184p. [Google Scholar]
  67. Ren, X.Q. Crustacea Amphipoda Gammaridea I, Fauna Sinica Invertebrata; Science Press: Beijing, China, 2006; 588p. [Google Scholar]
  68. Miao, X.X.; Xiao, J.; Fan, S.L.; Zang, Y.; Zhang, X.L.; Wang, Z.L. Assessing Herbivorous Impacts of Apohyale sp. on the Ulva prolifera Green Tide in China. Front. Plant Sci. 2021, 12, 795560. [Google Scholar] [CrossRef]
  69. Yoshino, H.; Yamaji, F.; Ohsawa, T.A. Genetic structure and dispersal patterns in Limnoria nagatai (Limnoriidae, Isopoda) dwelling in non-buoyant kelps, Eisenia bicyclis and E. arborea, in Japan. PLoS ONE 2018, 3, e0198451. [Google Scholar] [CrossRef]
  70. Zhang, D.Z.; Ding, G.; Zhou, T.T.; Yang, W.J.; Li, J.; Peng, X.; Tang, B.P. Genetic Diversity of Oratosquilla oratoria Populations in Yellow Sea. Chin. J. Zool. 2013, 48, 232–240. [Google Scholar] [CrossRef]
  71. Lobo, J.; Ferreira, M.S.; Antunes, I.C.; Teixeira, M.A.L.; Borges, L.M.S.; Sousa, R.; Gomes, P.A.; Costa, M.H.; Cunha, M.R.; Costa, F.O. Contrasting morphological and DNA barcode-suggested species boundaries among shallow-water amphipod fauna from the southern European Atlantic coast. Genome 2017, 60, 147–157. [Google Scholar] [CrossRef]
  72. Dewaard, J.R.; Hebert, P.D.N.; Humble, L.M. A Comprehensive DNA Barcode Library for the Looper Moths (Lepidoptera: Geometridae) of British Columbia, Canada. PLoS ONE 2011, 6, e18290. [Google Scholar] [CrossRef]
  73. Panova, M.; Nygren, A.; Jonsson, P.R.; Leidenberger, S. A molecular phylogeny of the north-east Atlantic species of the genus Idotea (Isopoda) with focus on the Baltic Sea. Zool. Scr. 2017, 46, 188–199. [Google Scholar] [CrossRef]
  74. Kim, Y.H.; Hong, S.S.; Conlan, K.E.; Lee, K.S. The genus Peramphithoe Conlan & Bousfield, 1982 from Korean waters (Crustacea: Amphipoda: Ampithoidae). Zootaxa 2012, 3400, 1–19. [Google Scholar] [CrossRef]
  75. Kim, K.; Shin, J.; Kim, K.Y.; Ryu, J.H. Long-Term Trend of Green and Golden Tides in the Eastern Yellow Sea. J. Coastal Res. 2019, 90, 317–323. [Google Scholar] [CrossRef]
  76. Xiao, J.; Wang, Z.L.; Song, H.J.; Fan, S.L.; Yuan, C.; Fu, M.Z.; Miao, X.X.; Zhang, X.L.; Su, R.G.; Hu, C.M. An anomalous bi-macroalgal bloom caused by Ulva and Sargassum seaweeds during spring to summer of 2017 in the western Yellow Sea, China. Harmful Algae 2020, 93, 101760. [Google Scholar] [CrossRef]
  77. Qi, L.; Hu, C.M.; Wang, M.Q.; Shang, S.L.; Wilson, C. Floating algae blooms in the East China Sea. Geophys. Res. Lett. 2017, 44, 11501–11509. [Google Scholar] [CrossRef]
  78. Huang, B.X.; Ding, L.P.; Qin, S.; Fu, W.T.; Lu, Q.Q.; Liu, Z.Y.; Pang, Y.L.; Li, X.L.; Sun, Z.M. The taxonomical status and biogeographical distribution of Sargassum horneri with the origin analysis of its drifting population in the end of 2016 at the Western Yellow Sea. Oceanol. Et Limnol. Sin. 2018, 49, 214–223. [Google Scholar] [CrossRef]
  79. Ding, X.W.; Zhang, J.H.; Zhuang, M.M.; Kang, X.Y.; Zhao, X.H.; He, P.M.; Liu, S.R.; Liu, J.F.; Wen, Y.; Shen, H.; et al. Growth of Sargassum horneri distribution properties of golden tides in the Yangtze Estuary and adjacent waters. Mar. Fish. 2019, 41, 188–196. [Google Scholar] [CrossRef]
  80. Zhao, J.; Jiang, P.; Qiu, R.; Ma, Y.Y.; Wu, C.H.; Fu, H.H.; Chen, H.X.; Li, F.C. The Yellow Sea green tide: A risk of macroalgae invasion. Harmful Algae 2018, 77, 11–17. [Google Scholar] [CrossRef]
  81. Thiel, M. Rafting of benthic macrofauna: Important factors determining the temporal succession of the assemblage on detached macroalgae. Hydrobiologia 2003, 503, 49–57. [Google Scholar] [CrossRef]
  82. Thiel, M.; Gutow, L. The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr. Mar. Biol. 2005, 43, 279–418. [Google Scholar] [CrossRef]
  83. Riera, R. Are marine drifting species cosmopolitan? the example of the isopod Idotea metallica. Thalassas 2014, 30, 75–78. [Google Scholar]
  84. Gutow, L.; Strahl, J.; Wiencke, C.; Franke, H.-D.; Saborowski, R. Behavioural and metabolic adaptations of marine isopods to the rafting life style. Mar. Biol. 2006, 149, 821–828. [Google Scholar] [CrossRef]
  85. Franke, H.D.; Gutow, L.; Janke, M. The recent arrival of the oceanic isopod Idotea metallica Bosc off Helgoland (German Eight, North Sea): An indication of a warming trend in the North Sea? Helgol. Mar. Res. 1998, 52, 347–357. [Google Scholar] [CrossRef]
  86. Duffy, J.E. Amphipods on seaweeds: Partners or pests? Oecologia 1990, 83, 267–276. [Google Scholar] [CrossRef] [PubMed]
  87. Liess, A.; Kahlert, M. Gastropod grazers affect periphyton nutrient stoichiometry by changing benthic algal taxonomy and through differential nutrient uptake. J. N. Am. Benthol. Soc. 2009, 28, 283–293. [Google Scholar] [CrossRef]
  88. Edgar, G.J.; Shaw, C. The production and trophic ecology of shallow-water fish assemblages in southern Australia III. General relationships between sediments, seagrasses, invertebrates and fishes. J. Exp. Mar. Biol. Ecol. 1995, 194, 107–131. [Google Scholar] [CrossRef]
  89. Zheng, X.Q. A Preliminary Study on the Impacts of Amphipods’ Grazing on the Macroalgal Community in Yundang Lagoon; Xiamen University: Xiamen, China, 2008; 106p. [Google Scholar]
  90. Sano, M.; Omori, M.; Taniguchi, K. Predator-prey systems of drifting seaweed communities off the Tohoku coast, northern Japan, as determined by feeding habit analysis of phytal animals. Fish. Sci. 2003, 69, 260–268. [Google Scholar] [CrossRef]
  91. Geertz-Hansen, O.; Sand-Jensen, K.; Hansen, D.F.; Christiansen, A. Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary. Aquat. Bot. 1993, 46, 101–109. [Google Scholar] [CrossRef]
  92. Hauxwell, J.; McClelland, J.; Behr, P.J.; Valiela, I. Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries. Estuaries 1998, 21, 347–360. [Google Scholar] [CrossRef]
  93. Yu, J.; Kuang, L.L.; Wang, Q.H.; Liu, Y.; Gong, Q.L.; Li, J.Y. Differences in photosynthesis, growth and resource accumulation bet ween drif-ting alga Sargassum horneri and cultured alga Undaria pinnatifida and their roles in interspecies competition. Period. Ocean Univ. China 2021, 51, 1–10. [Google Scholar] [CrossRef]
  94. Wang, L.M.; Wang, S.Y.; Xu, W.D.; Li, H.L.; He, P. Effects of temperature, light intensity and ratio of nitrogen to phosphorus on growth of seedlings in sea weed Sargassum horneri. J. Dalian Ocean Univ. 2020, 35, 376–381. [Google Scholar] [CrossRef]
  95. Lavaut, E.; Guillemin, M.L.; Colin, S.; Faure, A.; Coudret, J.; Destombe, C.; Valero, M. Pollinators of the sea: A discovery of animal-mediated fertilization in seaweed. Science 2022, 377, 528–530. [Google Scholar] [CrossRef]
  96. Li, H.M.; Zhang, C.S.; Han, X.R.; Shi, X.Y. Changes in concentrations of oxygen, dissolved nitrogen, phosphate, and silicate in the southern Yellow Sea, 1980–2012: Sources and seaward gradients. Estuar. Coast. Shelf Sci. 2015, 164, 44–45. [Google Scholar] [CrossRef]
  97. Zhao, S.B.; Xu, B.C.; Yao, Q.Z.; Burnette, W.C.; Charettef, M.A.; Su, R.G.; Lian, E.; Yu, Z. Nutrient-rich submarine groundwater discharge fuels the largest green tide in the world. Sci. Total Environ. 2021, 770, 144845. [Google Scholar] [CrossRef]
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Figure 1. (a) Sampling sites of golden tide macroalgae in the Southern Yellow Sea; (b–e) Marine habitats of stations 2021SYSA, 2021SYSB, 2021SYSC, and 2021SYSD, respectively.
Figure 1. (a) Sampling sites of golden tide macroalgae in the Southern Yellow Sea; (b–e) Marine habitats of stations 2021SYSA, 2021SYSB, 2021SYSC, and 2021SYSD, respectively.
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Figure 2. (a) Morphology of Sargassum thalli collected in the Southern Yellow Sea; (b) Blades; (c) Gas bladders; (d) Receptacles.
Figure 2. (a) Morphology of Sargassum thalli collected in the Southern Yellow Sea; (b) Blades; (c) Gas bladders; (d) Receptacles.
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Figure 3. MCL phylogenetic tree of the golden tide macroalgae analyzed in this study; 1000 bootstrap replicates were used to verify the support rate of each node in this tree.
Figure 3. MCL phylogenetic tree of the golden tide macroalgae analyzed in this study; 1000 bootstrap replicates were used to verify the support rate of each node in this tree.
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Figure 4. Morphology of the collected epizoans: (a) Apohyale sp.; (b) Idotea metallica; (c) Peramphithoe tea.
Figure 4. Morphology of the collected epizoans: (a) Apohyale sp.; (b) Idotea metallica; (c) Peramphithoe tea.
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Figure 5. MCL phylogenetic tree of the epizoans analyzed in this study; 1000 bootstrap replicates were used to verify the support rate of each node in this tree.
Figure 5. MCL phylogenetic tree of the epizoans analyzed in this study; 1000 bootstrap replicates were used to verify the support rate of each node in this tree.
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Figure 6. The occurrence frequency of epizoans from each site.
Figure 6. The occurrence frequency of epizoans from each site.
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Figure 7. Scatter graph of fresh weight of epizoans from each site.
Figure 7. Scatter graph of fresh weight of epizoans from each site.
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Figure 8. Flowchart of the floating Sargassum ecosystem.
Figure 8. Flowchart of the floating Sargassum ecosystem.
Jmse 11 00479 g008
Table
Table 1. Detailed information about the macroalgae used to build the phylogenetic tree.
Table 1. Detailed information about the macroalgae used to build the phylogenetic tree.
Species NumberAuthorityCollection LocalityLatitude, LongitudeGenBank InformationSourceSpecimen LocationReference
2021SYSA1, 2021SYSA2, 2021SYSA3This studySouthern Yellow Sea, China33.4283° N, 121.4723° EOM444204, OM444205, OM444206This studyShanghai Ocean UniversityThis study
2021SYSB1, 2021SYSB2, 2021SYSB3This studySouthern Yellow Sea, China33.0997° N, 121.6630° EOM444207, OM444208, OM444209This studyShanghai Ocean UniversityThis study
2021SYSC1, 2021SYSC2, 2021SYSC3This studySouthern Yellow Sea, China32.7661° N, 121.7887° EOM444210, OM444211, OM444212This studyShanghai Ocean UniversityThis study
2021SYSD1, 2021SYSD2, 2021SYSD3This studySouthern Yellow Sea, China32.8477° N, 121.8477° EOM444213, OM444214, OM444215This studyShanghai Ocean UniversityThis study
dl-3Sargassum horneriQingdao, ChinaN.A.KC782896NCBIChinese Academy of Sciences [62]
HY20130629.201Sargassum horneriYantai, China36.7900° N, 120.9700° EKY047195NCBIOcean University of China [56]
FJ20130427.193Sargassum fusiformeFujian, China25.1800° N, 119.2700° EKY047223NCBIOcean University of China [56]
RZ20121016.86Sargassum confusumRizhao, China35.3900° N, 119.5700° EKY047204NCBIOcean University of China [56]
TJS0168Sargassum fallaxTasmania, AustraliaN.A.GQ368266NCBIMuséum National d’Histoire Naturelle of Paris [63]
SAM539Sargassum muticumCelestia, Italy45.4386° N, 12.3496° EKY682972NCBIUniversity of Messina [64]
QD20120918.77Sargassum thunbergiiQingdao, China36.09° N, 120.49° EKY047198NCBIOcean University of China [56]
mbccc20Pyropia yezoensisQingdao, ChinaN.A.JQ619144NCBIChinese Academy of Sciences [62]
Note: N.A. means no information.
Table
Table 2. Detailed information about the epizoans used to build the phylogenetic tree.
Table 2. Detailed information about the epizoans used to build the phylogenetic tree.
Species NumberAuthorityCollection LocalityLatitude, LongitudeGenBank
Information		SourceSpecimen
Location		Reference
2021SYSAe1, 2021SYSAe2, 2021SYSAe3, 2021SYSAe4, 2021SYSAe5, 2021SYSAe6, 2021SYSAe7, 2021SYSAe8This studySouthern Yellow Sea, China33.4283° N, 121.4723° EOM714522,
OM714523,
OM723195,
OM714524,
OM714525,
OM723196,
OM723197,
OM723198		This studyShanghai Ocean UniversityThis study
2021SYSBe1, 2021SYSBe2, 2021SYSBe3This studySouthern Yellow Sea, China33.0997° N, 121.6630° EOM665403,
OM723205,
OM714526		This studyShanghai Ocean UniversityThis study
2021SYSCe1, 2021SYSCe2, 2021SYSCe3, 2021SYSCe4, 2021SYSCe5, 2021SYSCe6, 2021SYSCe7This studySouthern Yellow Sea, China32.7661° N, 121.7887° EOM723199,
OM723200,
OM723201, OM714527, OM701800,
OM701801,
OM701802		This studyShanghai Ocean UniversityThis study
2021SYSDe1, 2021SYSDe2, 2021SYSDe3, 2021SYSDe4, 2021SYSDe5, 2021SYSDe6, 2021SYSDe7, 2021SYSDe8, 2021SYSDe9, 2021SYSDe10This studySouthern Yellow Sea, China32.8477° N, 121.8477° EOM723206,
OM723207,
OM714528,
OM723202,
OM723203,
OM714529,
OM723204,
OM701797,
OM701798,
OM701799		This studyShanghai Ocean UniversityThis study
17Ampithoe lacertosaZhoushan, China30.7400° N, 122.8300° EOK480914NCBIShanghai Ocean University [39]
SFAM13-003Ampithoe helleriMinho, Portugal41.6940° N, 8.8510° WKX223985NCBIUniversity of Minho [71]
YSGT2021Apohyale sp.Southern Yellow Sea, China36.1369° N,
121.4222° E		OK180438NCBIMinistry of Natural Resources [68]
BCAMP0132Apohyale cf. pugettensisBritish Columbia, Canada48.8580° N, 125.1600° WMG315613NCBIUniversity of Guelph [72]
NRM-CGI-000108Idotea metallicaHelgoland Island, Germany54.1726° N, 7.8791° EKU530515NCBISwedish Museum of Natural History [73]
NRM-CGI-000072Idotea emarginataHelgoland Island, Germany54.1726° N, 7.8791° EKU530492NCBISwedish Museum of Natural History [73]
AP312Peramphithoe teaPado-ri, South Korea36.705° N,
126.13° E		JN575608NCBIInha University [74]
H38Oratosquilla oratoriaLianyungang, ChinaN.A.JX522527NCBIYancheng Teachers University [70]
Note: N.A. means no information.
Table
Table 3. Taxonomy, major morphological features, and distribution of epizoans.
Table 3. Taxonomy, major morphological features, and distribution of epizoans.
SpeciesTaxonomic StatusMajor Morphological FeaturesDistribution
Ampithoe lacertosa Spence Bate, 1858Animalia; Arthropoda; Malacostraca; Amphipoda; Ampithoidae; Ampithoe Leach, 1814The first and second antennae are almost equal in length. The gnathopods are sub-chelate, the second is larger than the first. The third pereiopod is shorter. The exopodite of the third uropod has hooked terminal spines and the tip of the endopodite has setae [66].USA, Canada, Japan, South Korea, and China
Apohyale sp.Animalia; Arthropoda; Malacostraca; Amphipoda; Hyalidae; Apohyale Bousfield & Hendrycks, 2002The second antennae is slightly longer than the first, and accessory flagellum is absent. The first gnathopod is smaller than the second. The third uropod is not segmented, and the telson is cleft [68].China [68]
Idotea metallica Bosc, 1802Animalia; Arthropoda; Malacostraca; Isopoda; Idoteidae; Idotea Fabricius, 1798The body is wide and flat. The thoracic segments are almost the same length. The number of segments of the second antennae is more. The abdomen is generally composed of 3 sections, of which each side of the base of the last section has a side suture [65].USA, Japan, Mexico, Canada, Australia, Germany, France, U.K., Brazil, New Zealand, Spain, and Sweden
Peramphithoe tea J.L.Barnard, 1965Animalia; Arthropoda; Malacostraca; Amphipoda; Ampithoidae; Sunamphitoe Spence Bate, 1857The second gnathopod is larger than the first. Pereiopods 5~7 are similar to each other. The tip of the exopodite of the third uropod has 2 hooked spines, the endopodite has small spines and terminal setae, and the telson is complete [67].South Korea, Canada, and the USA
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Xia, J.; Li, C.; Tang, Y.; Li, J.; Wu, T.; Liu, J.; Zhang, J. Epizoans on Floating Golden Tide Macroalgae in the Southern Yellow Sea. J. Mar. Sci. Eng. 2023, 11, 479. https://doi.org/10.3390/jmse11030479

AMA Style

Xia J, Li C, Tang Y, Li J, Wu T, Liu J, Zhang J. Epizoans on Floating Golden Tide Macroalgae in the Southern Yellow Sea. Journal of Marine Science and Engineering. 2023; 11(3):479. https://doi.org/10.3390/jmse11030479

Chicago/Turabian Style

Xia, Jing, Chongxiang Li, Yiyuan Tang, Ji Li, Tingjian Wu, Jinlin Liu, and Jianheng Zhang. 2023. "Epizoans on Floating Golden Tide Macroalgae in the Southern Yellow Sea" Journal of Marine Science and Engineering 11, no. 3: 479. https://doi.org/10.3390/jmse11030479

APA Style

Xia, J., Li, C., Tang, Y., Li, J., Wu, T., Liu, J., & Zhang, J. (2023). Epizoans on Floating Golden Tide Macroalgae in the Southern Yellow Sea. Journal of Marine Science and Engineering, 11(3), 479. https://doi.org/10.3390/jmse11030479

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