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Algae > Volume 38(1); 2023 > Article
Kim, Boo, Yoon, and Kim: Insight into the species identification and distribution of Grateloupiaceae (Halymeniales, Rhodophyta) having Grateloupia filicina-like morphology in the Northwest Pacific


Accurately identifying species is the basis of all biological studies. There has been much confusion in the identification of Grateloupiacean species, which have finely pinnate gross morphology similar to Grateloupia filicina (the type species of the family). The objective of this study was to comprehensively investigate species identification and distribution of G. filicina-like species in the Northwest Pacific, based on the rbcL sequences. A total of 118 specimens from 78 sites in Korea and Japan were collected from 2001 to 2021 and analyzed for their rbcL sequences. Additional 341 sequences downloaded from the GenBank were included in our comprehensive dataset. Based on these sequences, we documented the nomenclatural history and geographical distribution of the species, and commented on the application of species name. G. asiatica was the most abundant G. filicina-like species in the Northwest Pacific, and its high degree of morphological variation caused many misidentifications. In particular, G. dalianensis, G. serra, and G. variata require reconsideration of their conspecificity with G. asiatica using more specimens from China. By contrast, G. oligoclora was presumed to be a heterotypic synonym of G. subpectinata. The occurrence of G. acuminata, G. ramosissima, and G. livida in Korea resulted from misidentifications with other species.


The red algal family Grateloupiaceae includes nine genera: Grateloupia, Dermocorynus, Mariaramirezia, Neorubra, Pachymeniopsis, Kintokiocolax, Phyllymenia, Prionitis, and Yonagunia (Kim et al. 2021). Species belonging to this family are a notorious red algal group that are difficult to identify based only on the gross morphology due to significant intraspecific and interspecific variations (e.g., Verlaque et al. 2005, Kim et al. 2013). In general, any Grateloupia species with a finely pinnate thallus have been considered as Grateloupia filicina (J. V. Lamouroux) C. Agardh, the type species of the family (De Clerck et al. 2005). Identifying species in Grateloupiaceae is difficult for even algal taxonomist. Thus, many misidentifications of these species have been detected. For example, recent biochemical studies about the effect of extracts from Grateloupia species collected from Korea and China used the name G. filicina (e.g., Jung et al. 2016, Sun et al. 2017, Liu et al. 2019). Using G. filicina in a patent can be problematic because the distribution of G. filicina is limited to the Mediterranean basin (De Clerck et al. 2005). G. filicina-like species from the Northwest Pacific are different entities that share superficially similar gross morphology with G. filicina (Kawaguchi et al. 2001).
Three species in the Northwest Pacific have been considered as G. filicina because of their similar gross morphology, such as G. asiatica S. Kawaguchi & H. W. Wang, G. catenata Yendo, and G. subpectinata Holmes. Kawaguchi et al. (2001) concluded that G. filicina-like specimens from Japan and China were Grateloupia asiatica sp. nov., showing that they were distantly related to genuine G. filicina from the Mediterranean, the type locality of the species. Subsequently, the occurrence of G. aisatica has been confirmed in Korea using rbcL sequences (Lee et al. 2009, Kim et al. 2013, Yang and Kim 2015). Recently, Yang et al. (2021) showed that G. asiatica is common along the coasts of the Korean peninsula and Jeju Island.
Grateloupia catenata is known as G. filicina var. lomentaria Howe, G. filicina var. porracea (Mertens ex Kützing) Okamura, and G. filicina var. porracea f. lomentaria (Howe) Okamura (Okamura 1936). It was reinstated as G. catenata based on rbcL sequences from Japanese specimens reported by Wang et al. (2000). The occurrence of G. catenata in Taean (west coast), Uljin (east coast), and Jeju Island, Korea was confirmed by rbcL sequences (Lee et al. 2009, Kim et al. 2013, Yang and Kim 2015). Sheng et al. (2012) demonstrated the presence of G. catenata in China, revising Sinotubimorpha catenata (Yendo) W.-X. Li & Z. -F. Ding, S. claviformis W.-X. Li & Z. -F., S. guangdongensis W.-X. Li & Z. -F., S. qingdaoensis W.-X. Li & Z. -F., and S. ramosissima W.-X. Li & Z. -F. as heterotypic synonyms with G. catenata.
Grateloupia subpecinata, which was originally described by Holmes in 1912, was long placed into synonymy under G. filicina by Okamura (1936) based on morphology. However, G. subpectinata has been resurrected by Faye et al. (2004) based on the rbcL phylogeny and the detailed morphology of six specimens from Japan. Identifying G. subpectinata in the field is difficult because its gross morphology is similar to that of G. asiatica. In addition, the distribution range of G. subpectinata is unclear compared to that of G. asiatica. Several reports of G. subpectinata have been made in Korea based on rbcL sequences, but most are limited to the northeast coast and Jeju Island (Lee et al. 2009, Kim et al. 2013, Yang and Kim 2015).
The plastid rbcL gene is a suitable marker for the identifying halymenialean species (De Clerck et al. 2005, Lee et al. 2009, Yang and Kim 2015). In addition, the female reproductive structures (i.e., type of ampullae and post-fertilization events) reflecting genus delimitations are consistent with the rbcL phylogeny (Gargiulo et al. 2013, Calderon et al. 2014, Lee and Kim 2019). During the past two decades, many taxonomic studies have been conducted on Grateloupiacean species in the Northwest Pacific based on the rbcL sequences. (e.g., Kawaguchi et al. 2001, Faye et al. 2004, Kim et al. 2013, 2021). Accordingly, numerous rbcL sequences have been deposited in NCBI GenBank. However, there is much taxonomic confusion. For example, when blasting using the G. asiatica sequence in NCBI homepage, almost 100% sequence identity can be obtained under the names G. asiatica and also G. subpectinata and G. fastigiata W. -X. Li & Z. -F. Ding, making it difficult for non-taxonomic researchers to correctly identify their specimens. The objective of this study was to comprehensively investigate the identification and distribution of Grateloupiacean species with G. filicina-like morphology in the Northwest Pacific based on rbcL sequences.
We selected 29 species within Grateloupiaceae based on morphology, nomenclatural history, and distribution (Table 1). Among the 29 species, 8 Chinese species names (Grateloupia didymecladia W. -X. Li & Z. -F. Ding, G. fastigiata, G. qingdaoensis W. -X. Li & Z. -F. Ding, Sinotubimorpha catenata, S. guangdongensis, S. qingdaoensis, S. claviformis, and S. ramosissima) were included for a comprehensive understanding of G. filicina-like species, but they were not discussed in detail. These species have been described as new species based on the morphology described by Xia (2004). Subsequently, they were synonymized based on rbcL sequences. G. didymecladia was synonymized to G. subpectinata, and G. fastigiata and G. qingdaoensis were synonymized to G. asiatica, and the other five Sinotubimorpha species (S. catenata, S. claviformis, S. guangdongensis, S. ramosissima, and S. qingdaoensis) were synonymized to G. catenata (Sheng et al. 2012, Li et al. 2016, Liu et al. 2017, 2020).


In total, 21 G. filicina-like species from the Northwest Pacific are discussed in detail in the Results and discussion section (Table 1). The G. filicina-like habit of four representative species (Grateloupia asiatica, G. catenata, G. divaricata Okamura, and G. subpectinata) is shown in Fig. 1.
A total of 118 specimens of G. filicina-like species were collected from Korea and Japan (78 localities) between 2001 and 2021 (Supplementary Table S1). Specimens were pressed on herbarium sheets for habit observation, and most specimens were dehydrated in each plastic bag with silica gel for molecular study. Total genomic DNA was extracted from the silica gel-dried specimens or herbarium materials using the LaboPass Tissue Mini kit (Cosmo Genetech, Seoul, Korea) following the manufacturer’s instructions. The rbcL gene was amplified using the F7-R898 and F7-R1442 primer pairs (Freshwater and Rueness 1994, Kim et al. 2010). Polymerase chain reaction (PCR) amplification was performed using AccuPower PCR PreMix (Bioneer, Daejeon, Korea) or TaKaRa Ex Taq DNA polymerase (Takara Shuzo, Kyoto, Japan). The reaction was run with an initial denaturation at 94°C for 4 min, followed by 35 cycles of amplification (denaturation at 94°C for 30 s, annealing at 50°C for 30 s, and extension at 72°C for 1 min), and a final extension at 72°C for 6 min. The PCR products were purified using the LaboPass PCR purification kit (Cosmo Genetech) and then sequenced commercially by Macrogen Co. (Daejeon, Korea). The sequence reads were edited and assembled into a consensus using Chromas v. 1.45 (http://www.technelysium.com.au/chromas.html) or Geneious v. 11.1.5 (http://www.geneious.com) (Kearse et al. 2012), and aligned by manually.
In total, 459 rbcL sequences were used to infer the phylogeny and confirm the distribution of each species in the Northwest Pacific. The rbcL sequences of the G. filicina-like species were searched by name and downloaded from GenBank. We used a nucleotide BLAST search to include available GenBank sequences whether they were correctly identified or not. (https://blast.ncbi.nlm.nih.gov/Blast.cgi). Based on ≥99% identity with target species, all sequences were downloaded and aligned with our sequence data. The collection information found in each study for the downloaded sequences is listed in Supplementary Table S2.
Phylogenetic analyses were performed using the maximum likelihood (ML) method and the RAxML program (Stamatakis 2006) with the GTR + G evolutionary model. We performed 200 independent tree inferences using the -# option with default -I (automatically optimized SPR rearrangement) and -c (25 distinct rate categories) option in the program to identify the best tree. We used 1,000 replications under the same model settings to generate the bootstrap values. Bayesian inference was performed with MrBayes (v3.2.2) software (Ronquist et al. 2012). Two independent searches were done under the default settings, such as four chains of the Metropolis-coupled Markov Chain Monte Carlo, every 100th trees sampling, for 20 million generations, and the same evolution model (GTR + G) used in the ML search. Twenty-five percent of saved trees were discarded (as a burn-in point) for the Bayesian posterior probability calculations.


Phylogeny of the Grateloupia filicina-like species within the family Grateloupiaceae

Despite their highly similar gross morphology, the specimens were grouped into three different clades within the Grateloupiaceae, including the G. subpectinata clade, the Prionitis clade, and the Grateloupia sensu stricto clade (Fig. 2). These three clades have been suggested to be separate genera by Gargiulo et al. (2013). Although Rodríguez-Prieto et al. (2022) combined the G. subpectinata clade with the genus Phyllymenia, we do not agree because Neorubra species were not included in the combined tree. Neorubra species should be included to discuss relationships among Phyllymenia, the G. subpectinata clade, and Neorubra. As shown in Fig. 2, the monophyly of those three genera has been moderately supported (88% Bootstrap support [BTS]) (Fig. 2), while the monophyly of Phyllymenia and G. subpectinata clade is not supported (53% BTS not shown). We considered that the G. subpectinata clade could be a distinct new genus separate from Grateloupia sensu stricto. In addition, Pachymeniopsis, Prionitis, and Neorubra were suggested as the Phyllymenia/Prionitis complex by Rodríguez-Prieto et al. (2022), are also considered to be three distinct genera within Grateloupiaceae. A more comprehensive study on this issue will be our next publication. In this study, we suggest a detailed discussion of the 21 G. filicina-like species for each of the three separate clades, following the view of Gargiulo et al. 2013, including the G. subpectinata clade (= G. subpectinata group in Gargiulo et al. 2013), the Prionitis clade (= G. americana group in Gargiulo et al. 2013), and the Grateloupia sensu stricto clade (= G. filicina group in Gargiulo et al. 2013).

Grateloupia subpectinata clade

The G. subpectinata clade was fully supported, including G. subpectinata and other western Pacific species such as G. huangiae Show M. Lin & H. -Y. Ling, G. phuquocensis Tanaka & Pham-Hoàng Hô, G. sparsa (Okamura) Chiang, G. taiwanensis Show M. Lin & H. -Y. Ling, and G. turuturu Y. Yamada (100% BTS) (Figs 2 & 3). Although Grateloupia luxurians (A. Gepp & E. S. Gepp) R. J. Wilkes, L. M. McIvor & Guiry has been placed in synonymy with G. subpectinata (Verlaque et al. 2005), two rbcL sequences were designated G. luxurians from Australia (AY435175) and the United Kingdom (AY435176), which are distinct from G. subpectinata (Fig. 2). These specimens need to be confirmed as reported by Nelson et al. (2013). With the exception of these two specimens, and 12 specimens reported as introduced cases (marked with * in Fig. 3), G. subpectinata has been confirmed from Korea, Japan, and China. Liu et al. (2017) collected and analyzed 11 specimens known in China as G. didymecladia from Dalian, Wenzhou, and Shantou (KY047357-67) and synonymized them with G. subpectinata. Of the 11 specimens, the two from Shantou (Guangdong province) represented the southernmost point of the species distribution to date. The latitudinal distribution of G. subpectinata ranges from Shantou in the southern part of China (not shown in the map of Fig. 3), to Hakodate in the northern part of Japan (marked as “9” in Fig. 3). Collectively, this species is not abundant compared to other Grateloupiaceaen species, but appears to be widely distributed in the Northwest Pacific, including the southern part of China.
Among the published G. subpectinata sequences, it is noteworthy to mention about two recently published plastid genomes (i.e., MG598531 and AP018129). The former (MG598531) was published as G. filicina by Zhang et al. (2018), who collected specimens from Xiangshan Habor, Zhejiang Province, China, which is outside the distribution range of genuine G. filicina. The latter (AP018129) was published as G. asiatica from Hokkaido, Japan by Sumikawa et al. (2020). However, their genuine identity was G. subpectinata based on the rbcL sequence (marked with # in Fig. 3). This is one of the examples of the prevailing misidentification of G. filicina-like species in the Northwest Pacific region. This finding is significant because it could affect comparative plastid genomic studies of Halymeniales. The genomic differences between MG598531 and AP018129 should be treated as intraspecific differences rather than interspecific differences between distantly related species (i.e., G. filicina and G. asiatica).
Duan et al. (2022) reported that five specimens collected from Wenzhou, Zhejiang, China were G. oligoclora H. W. Wang & Y. Bian sp. nov. They suggested that this new species was the closest sister species to G. subpectinata with 1% sequence divergence. However, they compared the new sequences (five specimens were 100% identical to each other) with only one G. subpectinata sequence from Japan (AB114213) and did not consider genetic variation within G. subpectinata. Intraspecies variation of G. subpectinata ranged from 0 to 12 bp (0–1%) in our analyses. The G. oligoclora sequences were different from MG598531 at only 3 bp (0.27%) after including 81 G. subpectinata sequences from various regions. In our phylogenetic analysis, G. oligoclora was consistently monophyletic with other G. subpectinata sequences with high support (96% BTS in Fig. 2 & 93% BTS in Fig. 3). Duan et al. (2022) suggested that lateral branches and the branching patterns were the most obvious differences between G. oligoclora and G. subpectinata (G. oligoclora: unbranched, dichotomously branched or irregularly split; G. subpectinata: pinnately branched). However, we observed several specimens that dichotomously branched similar to G. oligoclora, as shown in Fig. 1D. Therefore, dichotomous branching cannot be used as a key to distinguish G. subpectinata from G. oligoclora. We consider that G. oligoclora should be synonymous with G. subpectinata based on available data (monophyletic in ML phylogeny, very row genetic divergence, and no distinct in gross morphology).
Among the sequences downloaded from GenBank, the sequences under the name G. corymbcladia W. -X. Li & Z. -F. Ding (MT656298-303) had the same rbcL sequences as G. subpectinata, in spite of no accessible references or specimens could be obtained. Considering the previous publications (e.g., Sheng et al. 2012, Li et al. 2016, Liu et al. 2017, 2020), this species may be synonymous with G. subpectinata.

Prionitis clade

The Prionitis clade was fully supported (100% BTS in Figs 2 & 4) and it includes following 7 selected G. filicina-like species; Grateloupia acuminata Holmes, G. asiatica, G. dalianensis H. W. Wang & D. Zhao, G. divaricata, G. livida (Harvey) Yamada, G. serra H. W. Wang & Y. Lou, and G. variata Cao, C. C., Li, Y. Z. & H. W. Wang. The monophyly of Grateloupia asiatica, G. variata, G. serra, and G. livida was fully supported within the Prionitis clade (Fig. 4). Although G. dalianensis also appears to be included in this clade (92% BTS) (Fig. 2), the discussion of this species is in the last section of the Results and discussion. Based on our sequences from collected specimens and the downloaded sequences, G. asiatica was considered the most abundant species not only within the Prionitis clade but also among G. filicina-like species in the Northwest Pacific. However, their latitudinal distribution range (from Hirado, Nagasaki, Japan to Oshoro, Hokkaido, Japan; the southernmost and northernmost points were marked with red stars in Fig. 4 because there were too many collection sites in Korea) was narrower than that of G. subpectinata. It may be different when more specimens are added from southern China, but so far, the southern distribution limit of this species is north of that of G. subpectinata.
Kawaguchi et al. (2001) suggested that G. livida is one of the few western Pacific Grateloupia species with a similar habit as G. asiatica. In this study, we collected four G. livida specimens from three different collection sites in Japan (Shimoda, Oshoro, and Nagasaki) (Supplementary Table S1), but G. livida has never been found in Korea. These four specimens from Japan formed a monophyletic group together with the previously published G. livida sequences from Weihai, China (marked with “8” in Fig. 4) and several regions on the Pacific side of Japan (marked with “1”, “6”, “7” in Fig. 4). Although G. livida has been reported by ecological studies in Korea (i.e., Lee and Kang 1986, Kim and Kim 2000), the correct species identification should be re-examined according to our collections.
G. serra and G. variata were monophyletic with all G. asiatica specimens (marked as “G. asiatica complex”) (Figs 2 & 4). G. variata was described based on the specimens collected from one site (four specimens; Luxun Park, Qingdao, China) on May 3, 2011 and G. serra has been described based on four specimens collected from the same site as G. variata on May 25, 2013 (Cao et al. 2016, Lou et al. 2019). We assigned these three species (G. asiatica, G. serra, and G. variata) to the “G. asiatica complex” because further analysis with more individuals is necessary.
Lou et al. (2019) suggested that the minimum interspecific divergence between G. asiatica and G. serra (3.72%) was evidence of a new species. However, they reported that the genetic difference between G. asiatica and G. serra was 15 bp, and the alignment comparison was 1,186 bp. The genetic divergence between G. asiatica and G. serra was 1.2–1.9% in our analyses (Supplementary Table S3). The highest p-distance value within the G. asiatica specimens (1.34% between MZ753751 and MZ 753752) was higher than the p-distance value between G. asiatica and G. serra (1.25% between AB055489 and KP195735). In other words, the lowest p-distance value between G. asiatica and G. serra was included in the intraspecific variation range of G. asiatica. The numerous proliferous branchlets on the surface of the main axes have been suggested as a key distinguishing character between G. serra and G. asiatica by Liu et al. (2019). Although Kawaguchi et al. (2001) reported “a few” proliferations on the surface of G. asiatica, several individuals (not common) had numerous proliferations on the surface of axes (Supplementary Fig. S1A–C).
The p-distance value between G. asiatica and G. variata was 2.3–3.2%, which is acceptable compared to other species of Halymeniales (Kim et al. 2014, Yang and Kim 2015). However, the rbcL sequence of this species was also monophyletic with all G. asiatica and G. serra sequences (Figs 2 & 4). The characteristics that Cao et al. (2016) proposed to distinguish G. variata from G. asiatica (i.e., branching pattern and texture) appeared to fall within the range of intraspecific polymorphisms in G. asiatica (Fig. 1). For example, Kawaguchi et al. (2001) specified the texture of this species as mucilaginous, but we had specimens in our collection that were somewhat cartilaginous (Fig. 1I & K, Supplementary Fig. S1C). Therefore, characteristics, such as branching pattern and texture, cannot be used as key characters to distinguish G. variata from G. asiatica.
On the other hand, the sequences downloaded from GenBank under the name G. sorocarpus W. -X. Li & Z. -F. Ding (MN809604-11), and G. constricta W. -X. Li & Z. -F. Ding (MN412709-16) are same with rbcL sequences as G. asiatica, postulating on synonymous with G. asiatica. Since the possibility of simple misidentification for several species from China cannot be ruled out either so far, we look forward to further studies in China to shed light on this problem. In this study, therefore, the taxonomic treatment of synonyms is deferred to Chinese phycologists.
G. acuminata has been reported from Korea by several phycologists (Lee 1987, Kim and Park 2006, Nam and Kang 2013) and axial width has been used as a key character to distinguish G. acuminata from G. asiatica (less than 10 mm for G. asiatica, over 10 mm for G. acuminata) (Nam and Kang 2013). That key may have been based on the first description of G. asiatica (specified an axial width range as 2–5 mm for G. asiatica) (Kawaguchi et al. 2001). However, our exhaustive collection revealed several G. asiatica individuals with a wider axis (~20 mm) (Fig. 1K & L). In other words, regardless of whether the width of the axis is narrow (less than 10 mm) or wide (over 10 mm), they were monophyletic as in G. asiatica and distinguished from G. acuminata, which was collected from the type locality (140328-36 Enoshima, Kanagawa, Japan) (Figs 2 & 4). In addition, G. acuminata has a restricted distribution along the Pacific coast of central Japan and is not abundant (Kawaguchi 1991, Iima et al. 1995). Despite our efforts to find G. acuminata in Korea, it has never been observed. Therefore, the previous records of G. acuminata from Korea were actually the morphological variants of G. asiatica with a wide axis.
The typical gross morphology of G. divaricata was somewhat different from that of G. subpectinata and G. asiatica, but the morphological characteristics overlapped (Fig. 1O & P). This morphological ambiguity between G. asiatica and G. divaricata was also noted by Verlaque et al. (2005). G. divaricata has not been reported since the first description, except some sequences as a part of another subject (i.e., Lee et al. 2009, Yang and Kim 2015). In this study, the occurrence of G. divaricata was confirmed, as a result of collecting and analyzing 10 specimens from the east coast of Korea (Supplementary Table S1). Interestingly, the distribution of this species was very limited to the northeast coast of Korea (only one exception is in Pohang) (Fig. 4). The collection sites of previously published sequences also limited this species to Gangneung, Sokcho (north-east coast of Korea), and Hokkaido, Japan (Fig. 4). Although we could not obtain any of the rbcL sequences or the actual study, this species was reported from Vladivostok, Russia (Guiry and Guiry 2022). This species is considered to be restricted to the East Sea surrounded by Korea, Japan, and Russia, while the others are broader in distribution (Figs 35). We suppose that G. divaricata may have adjusted to the cold water rather than warm water based on our collection and the published rbcL sequences (Fig. 4). Therefore, the reports of G. divaricata from Southeast Asia, such as the Philippines (Ang et al. 2014) and Vietnam (Nguyen et al. 2013), should be re-confirmed.

Grateloupia sensu stricto clade

The Grateloupia sensu stricto clade was consistently monophyletic but the bootstrap values varied depending on the taxa included. This clade includes Grateloupia catenata, G. ramosissima Okamura, G. tenuis L. Yu, H. W. Wang & R. X. Luan, G. orientalis S. M. Lin & H. Y. Liang, G. huanghaiensis Wang, H. W., Guan, Y., Zhao, F. Q. & Zhao, D., G. ramosa H. W. Wang & R. X. Luan, G. yinggehaiensis H. W. Wang et R. X. Luan, G. yangjiangensis W. -X. Li & Z. -F. Ding, and many specimens formerly known as G. filicina from various regions (refer to De Clerck et al. 2005 for the detail).
The latitudinal distribution range of G. catenata was similar to that of G. subpectinata and wider (from Zhelang Island, Guangdong, China to Hakodate, Hokkaido, Japan) than that of G. asiatica (Figs 3 & 5). However, it was still restricted to Korea, Japan, and China except the introduced cases (Fig. 5). Chellamanimegalai et al. (2020) recently reported G. catenata, G. filicina, and G. orientalis from India. However, all of their sequences designated as G. catenata, G. filicina, G. orientalis, and G. lithophila (refer to the group named as “Grateloupia spp. from India” in Fig. 5) were monophyletic with AJ868485 (“G. filicina” from Papua New Guinea) in the rbcL tree (97% BTS) (Fig. 5) and distantly related from the original sequences of each species (G. catenata, G. filicina, and G. orientalis). As the type locality of G. lithophila is India and some of the specimens were identified as G. lithophila, their genuine identity is likely to be G. lithophila. Nevertheless, the new records of G. catenata, G. filicina, and G. orientalis from India should be rejected.
Grateloupia ramosissima is a sister species to G. catenata and also similar in morphology. G. ramosissima specimens was found in southern Japan (Pacific side), China (Taiwan), and Vietnam (located on the south side of the map) based on the rbcL sequence (Fig. 5). In contrast to G. divaricata, this species has adapted to tropical rather than cold water. Therefore, the records of this species in Korea (Lee and Kang 1986) are considered as misidentifications of G. catenata.
Wang et al. (2014) described Grateloupia huanghaiensis sp. nov. as having a folios thallus after comparing this species to G. filicina, G. yinggehaiensis, and G. orientalis, which have G. filicina-like morphology. The phylogenetic relationships of this species have not been resolved within this clade based on rbcL sequences (Figs 2 & 5). Given the genetic distance of this species from several species within this clade, it is an independent species (2–2.1% with G. ramosa, 2.6% with G. tenuis, 2.8–3.3% G. orientalis) (Supplementary Table S3). However, it is clear that the characteristics, such as proliferation on the thallus, body size, and leaf width proposed by Wang et al. (2014) to distinguish G. huanghaiensis from other Grateloupia species, cannot be used for a species delimitation key, as shown above. In addition, this species is also known only from Luxun Park (Qingdao, China), like G. serra and variata. Analyzing more specimens of this species and related species from various sites will improve our knowledge of the speciation and evolution of this clade.
The Grateloupia sensu stricto clade also includes five G. filicina-like species mainly distributed in southern China (G. orientalis, G. ramosa, G. tenuis, G. yangjiangensis, and G. yinggehaiensis; distribution sites were not shown in Fig. 5). G. ramosa and G. tenuis are only distributed on Hainan Island, China, whereas G. yinggehaiensis and G. orientalis are distributed not only in southern China but also geographically far away. G. yinggehaiensis has been described based on the samples collected from Yinggehai (Hainan, China) (Zhao et al. 2012). Subsequently, this species was confirmed from Guangdong Province, China by Peng et al. (2018) as “G. filicina”. In addition, two more sequences fell within the same species from Dikwella (Sri Lanka), Tuler (Madagascar) which was identified as G. filicina before (Fig. 5). Therefore, the distribution range of this species is from Madagascar in the south to Guangdong, China in the north. The distribution report of this species in Italy, has been known as introduced case by Wolf et al. (2014).
G. orientalis was described based on the samples collected from Taiwan with a comment that this species possesses G. filicina-like thalli (Lin et al. 2008). We considered that several specimens known as “G. filicina” from various regions (not only from China but United States, Brazil, and French Polynesia as well) (Fig. 5) are con-specific with G. orientalis as mentioned by Wolf et al. (2014). Considering the generally limited distribution of the G. filicina-like species in the Northwest Pacific (refer to Figs 3 & 4) and the many species introduction reports from the Northwest Pacific to worldwide (e.g., Verlaque et al. 2005, Bolton et al. 2016), it is highly probable that this species was also introduced to the USA and Brazil from the Northwest Pacific as a cryptic introduction.
Last, it is necessary to confirm whether G. yangjiangensis and G. hawaiiana are conspecifics. G. hawaiiana was described as a folious Grateloupia species from the Hawaiian Islands by Dawson in 1958. G. yangjiangensis was described as a new species with G. filicina-type morphology from China (Xia 2004). Subsequently, this species was re-examined by Wang et al. (2014) using the rbcL sequences of four specimens collected from Yangjiang (the type locality of G. yangjiangensis), and Hainan Island, China. The base difference between the two species was only 0.2% (3 bp out of 1,286 bp), which is reasonable to consider as an intraspecific not interspecific variation (Wang et al. 2001). However, there was no information or discussion about G. hawaiiana or G. yangjiangensis in the study by Wang et al. (2014).

Numerous misidentifications of Grateloupia filicina-like species based on gross morphology

As shown by the many examples described above, many misidentifications have been made of G. filicina-like species in the Northwest Pacific. The most likely reason is a lack of understanding of the ranges in the gross morphological variations of each species. In particular, the overall range of gross morphological variations was much wider in G. asiatica than was known or expected (Fig. 1). Typical G. asiatica has flat, narrow axes, with finely pinnate lateral branches and a mucilaginous texture (Kawaguchi et al. 2001). However, we observed many gross morphological variations within this species, such as width of the axis, the branching pattern, proliferation, and texture (Fig. 1). The overall thallus shape of G. asiatica has numerous pinnate proliferations along the margin that taper upwards (Kawaguchi et al. 2001), as shown in Fig. 1H, but we found many individuals that may not be pinnate (Fig. 1F, J, L, M & N). The branching patterns are hard to define in one category. In addition, Kawaguchi et al. (2001) specified the texture of G. asiatica as mucilaginous, soft, and gelatinous, but we observed several individuals with a somewhat cartilaginous texture (Fig. 1I & K, Supplementary Fig. S1C). These high-level morphological variations in G. asiatica have been observed based on individuals introduced to France (Verlaque et al. 2005). Our study demonstrated that this high level of morphological variation is the nature of this species and could not be the result of inbreeding or interspecific hybridization in the introduced habitats as suggested by a previous study (Verlaque et al. 2005).
The gross morphological similarities between phylogenetically distant species have led to many misidentifications. The gross morphology of G. subpectinata (Fig. 1A–E) is similar to that of G. asiatica (Fig. 1F–N). Based on our observations, we considered that distinguishing G. subpectinata from G. asiatica based solely on gross morphology is almost impossible in the field. Although Faye et al. (2004) suggested several morphological differences between G. subpectinata and G. asiatica (i.e., fleshy texture, wider axes, generally longer proliferations that are constricted at the base), they were difficult to apply.

Several issues with the rbcL sequences in some Grateloupiaceae species

We found sequences from several species (i.e., Grateloupia dalianensis, G. huanghaiensis, G. ramosa, G. serra, G. tenuis, G. variata, and G. yinggehaiensis) with some issues. First, the middle part of the G. dalianensis (HQ385503–385506) sequence encoded completely different amino acids compared to other red algae rbcL sequences extracted from published plastid genomes of various red algal linages (Supplementary Fig. S2). Although Zhao et al. (2012) reported no insertions or deletions, there were two insertions at positions 661 (1 adenine-insertion) and 1,165 (2 adenine-insertion) of the rbcL gene. These two sites were polyadenine sites. When the additional adenines were deleted, assuming a sequencing error, the amino acid sequence changed to be similar to other halymenialean species sequences, but two stop codons appeared in the middle of the gene (refer to the sequence named as “HQ385504 “Grateloupiadalianensis (corrected)” in the Supplementary Fig. S2). In addition, particularly high genetic divergence was detected between G. dalianensis and other the Prionitis species (7.3–10.4%) (Supplementary Table S3) and it appeared as a long branch in the ML tree compared to the other species (Fig. 2). Zhao et al. (2012) mentioned that there is a great difference in size between G. dalianensis and G. asiatica. They suggested the range of the length of the thallus was 14–24 cm for G. asiatica and 20–30 cm for G. dalianensis. However, the range was different in a table and the text (Zhao et al. 2012, Table 2: 7–75 cm for G. asiatica and 15–30 cm for G. dalianensis). Therefore, confirmation is required because the peculiar range of length (7–75 cm) was also assigned to G. acuminata and G. livida. However, whether it is 15–30 cm or 20–30 cm, the range of G. dalianensis length overlaps with that of G. asiatica (10–30 cm) (Kawaguchi et al. 2001), and is not a large difference. The thallus length of G. asiatica based on our collection (87 specimens) was 5–32 cm, which was almost consistent with the first description (10–30 cm) by Kawaguchi et al. (2001). No additional sequences have been published since the first description of G. dalianensis using four specimens collected from Dalian, China. Therefore, confirmation is necessary to clarify the true status of this species.
Some peculiar nucleotide sequences were detected at the beginning and end of the several species (Grateloupia huanghaiensis, G. ramosa, G. serra, G. tenuis, G. variata, and G. yinggehaiensis) based on the amino acid comparison with various red algal lineages (Supplementary Fig. S3). As shown in Supplementary Figs S2 & S3, the rbcL gene is very conserved among all red algal lineages, even Cyanidiales, which are known as the most primitive red algal lineage (Yang et al. 2016). Therefore, the rbcL sequences of these species should be checked. As the peculiar nucleotide sequences were located only at the beginning and end of the sequences, it seems that they have not been sufficiently excluded to avoid ambiguous base pairs at both ends of the electropherograms. Fortunately, those sequences, even if excluded, would not affect their taxonomic status or phylogenetic position within the Grateloupiaceae. Nevertheless, these sequences should be verified again using additional samples because most of the species have been based on only a few specimens.


In this study, G. filicina-like species from the Northwest Pacific were comprehensively collected and analyzed based on rbcL sequences. G. asiatica was the most common species in the Northwest Pacific. We unexpectedly found various gross morphological variations causing many misidentifications with other species. In particular, G. dalianensis, G. serra, and G. variata should be re-considered as conspecifics with G. asiatica using more specimens from China. By contrast, G. oligoclora should be considered a synonym of G. subpectinata based on our extended sampling. In addition, G. constricta, G. sorocarpus, G. corymbcladia, and G. yangjiangensis need to be confirmed. The distribution of G. divaricata and G. ramosissima were noteworthy. The former was restricted to the Donghae (East Sea) affected by the cold current, and the latter was found on the Pacific side of Japan, Taiwan, and Vietnam affected by the warm current. We believe that the occurrence of G. ramosissima, G. acuminata, and G. livida in Korea should be considered misidentifications with other similar species.
This study contributes to a better understanding of the identification and distribution of G. filicina-like species in the Northwest Pacific, which is likely a center of species diversity for Garetloupiaceae. Comparison of rbcL sequences based on comprehensive sampling demonstrated that even species described by the rbcL sequences and/or morphology can still have nomenclature problems. Our study sends a message of warning on the blind faith for the names deposited in GenBank. In addition, a detailed investigation of the published rbcL sequences compared to other red algal lineages revealed issues with the sequences itself. Thus, a more thorough investigation of related species is essential when considering the identities of these species.


We thank Drs. Eun Chan Yang and Hyung Woo Lee for collecting precious algal samples and allowing their use for this study. This work was partly supported by the National Research Foundation of Korea (NRF), NRF-2022R1C1C2004043 to SYK and NRF-2020R1I1A2069706 to MSK.


The authors declare that they have no potential conflicts of interest.


Supplementary Fig. S1
Specimens that have numerous surface proliferations on the thallus (https://www.e-algae.org).
Supplementary Fig. S2
Amino acid sequence alignment of rbcL gene. Grateloupia dalianensis show totally different amino acid sequence compared to representatives of all red algal orders (https://www.e-algae.org).
Supplementary Fig. S3
Amino acid sequence alignment of rbcL gene. Several species show peculiar amino acid compared to representatives of all red algal orders at the beginning and end of the sequence (https://www.e-algae.org).
Supplementary Table S1
Voucher number and collection information of newly analyzed sequences (https://www.e-algae.org).
Supplementary Table S2
Sequence information of downloaded from GenBank (https://www.e-algae.org)
Supplementary Table S3
Genetic distance of several species within each clade using rbcL gene (https://www.e-algae.org)

Fig. 1
Habits of Grateloupia filicina-like species in the Northwest Pacific. (A–E) G. subpectinata. (F–N) G. asiatica. (O & P) G. divaricata. (Q & R) G. catenata. Scale bars represent: A–R, 3 cm.
Fig. 2
Maximum likelihood phylogenetic tree of Grateloupia filicina-like species in the Northwest Pacific using rbcL sequences. Maximum likelihood bootstrap value and Bayesian posterior probability are shown near the branches. Gray boxes indicate the 29 G. filicina-like species names in the Northwest Pacific. The 21 species included in the Result and discussion section are in bold. Species that need confirmation are marked with an asterisk (*). The species or genus names in quotation marks indicate that the name should be changed.
Fig. 3
Maximum likelihood phylogeny of the Grateloupia subpectinata clade with a distribution map of G. subpectinata based on rbcL sequences. Asterisk (*) indicates sequences known to have been introduced to outside of the Northwest Pacific. Sharp (#) indicates sequences extracted from published plastid genomes. Red dots on the map indicate collection locations of new sequences and black dots indicate collection locations of published sequences with the following reference number: 1, Faye et al. (2004); 2, Lee et al. (2009); 3, Nelson et al. (2013); 4, Kim et al. (2013); 5, Yang and Kim (2015); 6, Liu et al. (2017); 7, Peng et al. (2018); 8, Zhang et al. (2018); 9, Sumikawa et al. (2020); 10, Duan et al. (2022).
Fig. 4
Maximum likelihood phylogeny of the Prionitis clade with distribution map of Grateloupia acuminata, G. divaricata, and G. livida based on rbcL sequences. Pale red taxa indicate newly analyzed G. asiatica sequences. The southernmost and northernmost G. asiatica collection sites are marked with red stars due to too many collection sites. Asterisk (*) indicates the sequences known to be introduced outside of the Northwest Pacific. Purple, blue, and green dots indicate collection locations for new sequences of each species, and black dots indicate collection locations for published sequences with the following reference number: 1, Wang et al. (2000); 2, Mateo-Cid et al. (2005); 3, Lee et al. (2009); 4, Kim et al. (2013); 5, Yang and Kim (2015); 6, Kawaguchi et al. (2001); 7, Gavio and Frederiq (2002); 8, Peng et al. (2018).
Fig. 5
Maximum likelihood phylogeny of the Grateloupia sensu stricto clade with a distribution map of Grateloupia catenata, G. huanghaiensis, and G. ramosissima based on rbcL sequences. Asterisk (*) indicates the sequences known to be introduced to outside of the Northwest Pacific. Red dots indicate collection locations of new sequences and black dots indicate collection locations of published sequences with the following reference number: 1, Wang et al. (2000); 2, Lee et al. (2009); 3, Sheng et al. (2012); 4, Kim et al. (2013); 5, Yang and Kim (2015); 6, Yang et al. (2016); 7, Peng et al. (2018); 8, Wang et al. (2001); 9, Gavio and Frederiq (2002); 10, Wang et al. (2015).
Table 1
List of 29 Grateloupia filicina-like species in the Northwest Pacific
Species Taxonomic note (reference) Clade Distribution (based on rbcL)
G. didymecladia Synonimized to G. subpectinata (Liu et al. 2017 in Chinese) G. subpectinata clade CH
G. fastigiata Synonimized to G. asiatica (Li et al. 2016 in Chinese), sequence problem Prionitis clade CH
G. qingdaoensis Synonimized to G. asiatica (Liu et al. 2020) Prionitis clade CH
Sinotubimorpha catenata Synonimized to G. catenata (Sheng et al. 2012) Grateloupia sensu stricto CH
S. claviformis Synonimized to G. catenata (Sheng et al. 2012) Grateloupia sensu stricto CH
S. guangdongensis Synonimized to G. catenata (Sheng et al. 2012) Grateloupia sensu stricto CH
S. ramosissima Synonimized to G. catenata (Sheng et al. 2012) Grateloupia sensu stricto CH
S. qingdaoensis Synonimized to G. catenata (Sheng et al. 2012) Grateloupia sensu stricto CH
G. sorocarpusa Unpublished, same sequence with G. asiatica Prionitis clade CH
G. constrictaa Unpublished, same sequence with G. asiatica Prionitis clade CH
G. corymbcladiaa Unpublished, same sequence with G. subpectinata G. subpectinata clade CH
G. acuminatab Prionitis clade JP (South)
G. asiaticab Prionitis clade KR, JP, CH
G. catenatab Resurrected (Wang et al. 2000) Grateloupia sensu stricto KR, JP, CH
G. dalianensisa Sequence problem, G. asiatica complex Prionitis clade CH
G. divaricatab Prionitis clade KR (East), JP
G. huanghaiensis Sequence problem Grateloupia sensu stricto CH
G. lividab Prionitis clade JP, CH
G. luxurians Synonimized to G. subpectinata (Verlaque et al. 2005), AY435175-6: not monophyletic with G. subpectinata G. subpectinata clade UK, AUS
G. oligoclora Synonym with G. subpectinata (this study) G. subpectinata clade CH (South)
G. orientalis Grateloupia sensu stricto CH (South)
G. ramosa JF810597: sequence problem Grateloupia sensu stricto CH (South)
G. ramosissima Grateloupia sensu stricto JP (South), CH (South), VN
G. serraa Sequence problem, G. asiatica complex Prionitis clade CH
G. subpectinatab Resurrected (Faye et al. 2004) G. subpectinata clade KR, JP, CH
G. tenuis Sequence problem Grateloupia sensu stricto CH (South)
G. variataa Sequence problem, G. asiatica complex Prionitis clade CH
G. yangjiangensisa Only 3 bp difference with G. hawaiiana: AY772030 Grateloupia sensu stricto CH (South), ML, USA (Hawaii)
G. yinggehaiensis Sequence problem Grateloupia sensu stricto CH (South), SL

Bold indicates the 21 species discussed in the Results and Discussion section.

CH, China; JP, Japan; KR, Korea; UK, United Kingdom; Aus, Australia; VN, Vietnam; ML, Malaysia; SL, Sri Lanka.

a Species that have to be confirmed.

b A species that was sequenced in this study.


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