Green tides occur every year in the Yellow Sea (YS), and numerous investigations are proceeding on various aspects of the phenomenon. We have identified bloom-forming species collected from diverse locations in the YS using morphological traits and the chloroplast gene for the large subunit of ribulose-1,5-bisphosphate carboxylase (
rbc
L). Morphological and
rbc
L sequence data analyses characterized the blooming species on both sides of the YS as belonging to the
Ulva linza-procera-prolifera
(LPP) complex clade or
U. prolifera
of earlier reports. However,
U. procera
within the LPP complex must be regarded as synonym of
U. linza
. Moreover,
U. prolifera
in free-floating samples collected from the Qingdao coast in 2009 was clearly in a distinct clade from that of the blooming species. Therefore,
U. linza
is the main green tide alga in the YS and has the
procera
-morphology. The green drift mats in the southeastern part of the YS (southwest sea of Korea) consisted predominantly of
U. linza
and rarely of
U. compressa
or
U. prolifera
.
INTRODUCTION
Macroalgal blooms occur worldwide, but the green tide that occurred on the Qingdao coast in late June 2008 was unprecedented, as it formed the largest green algal bloom recorded. Massive floating green mats covered about 1,200 km
2
of coastal water, and the Qingdao shoreline on the northeastern coast of China. This phenomenon reoccurred in the same region in July 2009, covering much of the same area as the previous year (
Zhang et al. 2011
). It has subsequently become an annual phenomenon.
The origin of the floating green mats off the east coast of China from 2007 to 2009 has been studied extensively, and different explanations have been a source of considerable controversy.
Liu et al. (2009
,
2010
) suggested that the floating green mats originated from
Porphyra
cultivation systems, whereas
Pang et al. (2010)
hypothesized a land-based pond origin associated with animal aquaculture. Despite these differences in opinion, the fundamental cause of these green algal blooms was eutrophication. Accordingly, a consensus was reached that the green tides in the Yellow Sea (YS) are caused by high nutrient conditions.
Green tide-forming species occur in two forms, such as attached thalli or free-floating thalli. These forms are based on substratum availability and environmental conditions.
Ulva
spp. have high intraspecific morphological plasticity associated with seasonal and environmental conditions (
Blomster et al. 1998
,
1999
). This plasticity reflects competition in complex and varying environments where survival depends on adaptation to limited nutrient, light, salinity, and temperature conditions. A consequence of the morphological plasticity is that some
Ulva
spp. (e.g.,
Ulva compressa
and
U. intestinalis
) cannot be identified using morphological characters, e.g., changes in branching induced by low salinity or salinity shock (
Blomster et al. 1998
). Furthermore, laboratory culture experiments show that bacteria and their exudates associated with
Ulva
may induce extensive morphological changes that cross supposedly well-defined species boundaries (
Provasoli and Pintner 1980
,
Marshall et al. 2006
). Thus, identifying
Ulva
spp. based on morphological characters can be problematic. For this reason, the
Ulva
sp. that appeared in the YS was not identified correctly, and some researchers attempted to identify the species based on molecular phylogenetic characters.
A molecular phylogenetic evaluation of
Ulva
isolated from the 2008 Qingdao bloom also showed conflicting results.
Leliaert et al. (2009)
concluded that the species from 2008 Qingdao was part of the
Ulva linza-procera-prolifera
(LPP) complex, whereas
Wang et al. (2010)
concluded that the alga was
U. prolifera
.
Zhang et al. (2011)
reported that the blooming species forming the floating mats in the YS in 2008 and 2009 was
U. prolifera
based on a 5S rDNA spacer sequence analysis.
Following the Qingdao bloom a similar event, albeit on a smaller scale, occurred near the Jeju Island coast in 2008. Green macroalgal patches appeared to the west of Ieodo Ocean Research Station and were 100-200 m wide and 200-800 m long in 2008 (
Choi et al. 2010
). The same phenomenon occurred in the southwest sea of Korea (the southeastern part of the YS) in 2009, and the green mats were senescent with reduced physiological activity (
Kim et al. 2011
). The green tide reoccurred in the southwest sea of Korea in July 2011, and off the coasts of China (the western part of the YS), and this has become an annual event in the YS.
Green tides in the southwest sea of Korea were similar to the Chinese blooms, but have not been studied to the same extent as those in China. Nevertheless, satellite images from the southeastern part of the YS suggest that the green patches on the west coast of Korea originated from the east coast of China (
Son et al. 2015
). It is clear that the green tides in the YS have been reoccurring every year since 2007. A key step to understand the reason behind this nuisance phenomenon and to potentially manage it is to identify the species involved. In this study, we attempted to identify the bloom-forming species off the Korean coast using both morphological approaches and a phylogenetic analysis of plastid ribulose-1,5-bisphosphate carboxylase (
rbc
L) gene sequences. In addition, we re-evaluated the identity of the YS green tide species.
MATERIALS AND METHODS
Over 700 specimens of
Ulva
spp. were collected on and off the coasts of Korea and China including bloom-forming species in the YS from 2008 to 2012 (
Table 1
). The floating and benthic
Ulva
samples from the Chinese coasts were collected in the summer of 2009 when floating algal mats appeared on the southwestern sea of Korea. The samples were rinsed in deionized water, conspicuous epiphytes were removed, and the samples were preserved in silica gel until DNA extraction. Voucher specimens were prepared as herbarium specimens and deposited at Chonnam National University.
Sites and dates of collectingUlvaspecies on the Korean coastal area and in different areas of the world from 2008 to 2012
Sample No. in bold type indicates Yellow Sea floating samples.
Morphological characters, such as cell shape, size, and arrangement, as well as frond margin shape and number of pyrenoids, were determined by light microscopy. Most samples were examined from fresh material and dried samples were observed after rehydration in seawater.
Genomic DNA from silica-dried samples was ground with a mortar and pestle in liquid nitrogen and extracted using a DNeasy Plant Mini Kit (Qiagen, Hilden, Germany). The plastid-encoded
rbc
L gene was amplified by the polymerase chain reaction (PCR) using the RH1, 1385r, SHF1, SHR4, rbc590, rbc571, and KF2 primers (
Table 2
) and a general PCR reaction mixture (TaKaRa ExTaq DNA polymerase; Takara Bio Inc., Shiga, Japan). The PCR products were purified using a PCR Gel Purification Kit (Qiagen) and a Labo Pass PCR Purification Kit (Cosmo Genetech, Seoul, Korea). PCR products were sequenced by Cosmo Genetech.
Primers used for the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL) sequence amplification
Primers used for the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL) sequence amplification
Sequence data were edited using the SeqEd DNA sequence editor software package, and the edited DNA sequence alignment was conducted manually using SeqPup (
Gilbert 1995
) and MacClade v.4.06 (
Maddison and Maddison 2003
) after adding other
rbc
L sequences retrieved from GenBank (
Table 3
). Bayesian phylogenetic trees were constructed with MrBayes 3.0b4 (
Huelsenbeck and Ronquist 2001
). The GTR + Г + I model was used and 5,000,000 generations of four chains were run sampling every 100 generations. The neighbor joining (NJ), maximum parsimony (MP), and maximum likelihood (ML) methods were implemented using PAUP 4.0b10 for the Macintosh (
Swofford 2002
). We used Modeltest 3.7 (
Posada and Crandall 1998
) for ML and distance analyses to determine a suitable model for our data. The best-fit model was TrN + I + G selected by hLRTs. The ML analysis was completed using the heuristic search algorithm with five random additions. The NJ analysis was subjected to 1,000 rounds of bootstrap resampling, and the MP analysis used 5,000 resampling rounds with 10 random addition replicates per bootstrap replicate.
Ulvaand outgroup species GenBank accession numbers and collection areas for therbcL sequences
Ulva and outgroup species GenBank accession numbers and collection areas for the rbcL sequences
RESULTS
- Morphological characters ofUlvaspecies from the floating green mats
The major bloom-forming species,
U. linza
, generally showed
procera
-morphology. This morphotype of
U. linza
had a narrow tubular shape, was highly branched throughout all thalli, and had central cavities in most thalli and branches (
Fig. 1
).
U. linza
thalli were <2 mm wide and had rectangular or quadrangular cells arranged in longitudinal and transverse rows. Each cell had one, or rarely, two pyrenoids.
Ulva linza (UL394) collected near Heuksando, Korea in 2009. Scale bars represent: A, 1 cm; B & C, 20 µm.
U. compressa
had tubular thalli with irregularly spaced regions of greater or lesser inflation (
Fig. 2
). Some thalli were highly branched or unbranched. The rounded cells were arranged irregularly but were occasionally found in longitudinal rows. The cells had one large pyrenoid.
Ulva compressa (UL555) collected from Qingdao, China in 2009. Scale bars represent: A, 1 cm; B, 20 µm.
U. prolifera
was very morphologically similar to the
procera
-morphology of
U. linza
.
U. prolifera
thalli were branched intensively with a narrow primary axis and tubular thalli, and all branches had central cavities. Thalli were <2 mm wide, and the quadrangular cells were arranged in longitudinal rows. The cells had one pyrenoid.
- Molecular phylogenetic analysis
All
Ulva
spp. belonged to a monophyletic group with strong bootstrap support. A phylogenetic tree based on the
rbc
L sequence data of
Ulva
spp. distinguished 10 clades, including one unidentified
Ulva
sp. collected from the Korean coast (UL430, 431) (
Fig. 3
). Eight species were identified from samples collected from the Korean and Chinese coasts, and one of them was recorded from the floating green mat off the Qingdao coast (UL669, 670).
Tree constructed with Bayesian inference for the rbcL. Values at branches represent Bayesian posterior probabilities (left), and 1,000 bootstrap replicates for neighbor joining (mid) and 5,000 bootstrap replicates for maximum parsimony (right). Lacking values received less than 50% support. Taxa names in bold type indicate samples collected near type locality of the species. Sample numbers are described in Table 1. Samples in bold type indicate free-floating samples from the Yellow Sea. Bold box A and B indicates Ulva linza group (reported as U. procera and U. prolifera by various authors) and U. prolifera group, respectively. aUL618, 691, 695, 700, CH2538, 2543, 2544. b383, 394, 410, 413, 526, 532, 535, 592, 595, 596, 663, 664, 672, 705, 707.
The floating green mats consisted
U. linza, U. compressa
, and
U. prolifera
(
Fig. 3
). The main floating green mat species in the YS from 2008 to 2011 was
U. linza
, which was identified by
rbc
L analysis (e.g., UL380, 382, 388, 715, 720). These samples were identified as
U. prolifera
in previous studies, which belongs to the same clade as the YS green tide species from 2008 and 2009 (e.g., HM046604, HM584763) (
Liu et al. 2010
,
Duan et al. 2012
). The floating green mats from the Qingdao coast (UL592, 596) and culture-derived samples from the YS (UL663, 664) were identified as
U. linza
. This clade also included attached
Ulva
specimens from the Korean and Chinese coasts (e.g., UL072, 308, 549, 607).
A small number of
U. compressa
specimens were found in the floating green mats from the Korean and Chinese coasts in 2009 (e.g., UL376, 555) (
Fig. 3
).
U. compressa
appeared as a distinct monotypic clade but floating and attached specimens were not distinguished in the tree.
U. prolifera
was also collected from the Qingdao coast floating green mats (UL669, 670) (
Fig. 3
). The
U. prolifera
clade, including
rbc
L data from Scotland (AY255864) and New Zealand (EF110202, EF110207, EF110213), was strongly supported by bootstrap values (Bayesian posterior probabilities, 100%; neighbor joining, 86%; and maximum parsimony, 92%).
U. prolifera
did not occur on the Korean coasts from 2009 to 2012 and did not form a green tide in the YS.
DISCUSSION
Based on morphological evidence and the
rbc
L sequence data of 106 samples collected from the YS, including the east coast of China and southwest coast of Korea, the massive green mats were comprised of three species (
U. linza, U. prolifera
, and
U. compressa
).
U. linza
and
U. compressa
occurred on both sides of the YS (the east coast of China and the southwest coast of Korea), whereas
U. prolifera
only occurred along the east coast of China. The green tide-forming species in the YS have been regarded as
U. prolifera
in many studies (e.g.,
Wang et al. 2010
,
Zhang et al. 2011
). However,
U. linza
was the dominant species, and it was mixed with some other
Ulva
spp. in our study.
The typical form of
U. linza
is strap-shaped, with oblong, oblanceolate, and sheet-like thalli and ruffled blade margins (
Bliding 1963
,
Koeman 1985
,
Brodie et al. 2007
). However,
U. linza
does not have a consistent morphology because of extensive phenotypic plasticity induced by the environment (
Bliding 1963
).
Ulva
spp. are not always distinguishable based on morphology (
Blomster et al. 1998
,
1999
). We also found that identifying
Ulva
spp. based on morphological characters, such as thallus form, cell shape, and arrangement, was problematic (
Figs 1
&
2
). Bloom-forming
U. linza
in the YS were similar in morphology to that of
U. prolifera
and
U. procera
(regarded as a synonym of
U. linza
) (
Tan et al. 1999
,
Brodie et al. 2007
, Heesch et al. 2007). According to
Brodie et al. (2007)
,
U. linza
has two primary morphological forms, i.e., the
linza
-morphology and the
procera
-morphology. Most floating bloom samples from the YS were confirmed to be
U. linza
the
rbc
L sequence data, and it manifested the
procera
-morphology under these conditions (
Fig. 1
).
The morphological characters of bloom species collected from Korean coastal waters were similar to those of the bloom species from the coasts and offshore of China (
Fig. 1
). Our the
rbc
L sequence data showed that not only did the species west and southeast of the YS (e.g., UL380, UL592, UL072, HM046608) occur in the same clade but that both morphological types (i.e.,
linza
- and
procera
-morphologies) were present within this clade (
Fig. 3
).
Many studies of the YS green tide species have attempted to clarify the identity of the species and its origin. Early studies that identified the YS green tide species concluded that the bloom species belonged to the LPP complex based on difficulties using internal transcribed spacer (ITS) and
rbc
L gene sequences (
Leliaert et al. 2009
,
Liu et al. 2010
,
2010
). Although
U. procera
is included in the LPP complex,
U. procera
is regarded as a synonym of
U. linza
; thus, it is more accurate to classify
U. procera
in
Ulva linza-prolifera
(LP) complex (
Tan et al. 1999
,
Brodie et al. 2007
,
Guiry and Guiry 2014
). Nevertheless, many researchers concluded that the YS green tide species was
U. prolifera
based on morphological traits and that it belonged to the LPP complex (e.g.,
Pang et al. 2010
,
Wang et al. 2010
,
Zhang et al. 2011
,
Liu et al. 2012
). However, phylogenetic results show that
U. prolifera
is in the LP complex, and we believe that many researchers are unaware that the LPP complex is an artificial assemblage.
Wang et al. (2010)
concluded that the YS bloom species was
U. prolifera
based on a ribotype network analysis of ITS sequences in which the bloom-forming material was closely related to Japanese
U. prolifera
from brackish water, rather than that of Europe and New Zealand. This was despite the fact that this material could be ascribed to the LPP complex based on the ITS gene.
Shimada et al. (2008)
first suggested the LPP complex originated from an ITS phylogenetic tree because the phylogenetic tree showed no substantive differences between
U. linza
and
U. prolifera
. However, the LPP complex in their results did not include
U. prolifera
samples, and
U. prolifera
from Europe was separated in another clade from the LPP complex. Therefore, it is possible that Japanese
U. prolifera
in brackish water was mis-identified.
Hiraoka et al. (2011)
noted potential problems identifying the YS bloom species based on the ITS marker. The 5S rDNA spacer sequence within the LPP complex has been used because the 5S rDNA spacer is 10 times more variable than that of the ITS region (
Hiraoka et al. 2011
,
Zhang et al. 2011
,
Han et al. 2013
,
Huo et al. 2013
). However, these studies did not include specimens from the
U. prolifera
clade in Europe.
Shimada et al. (2008)
used the 5S rDNA spacer to elucidate the phylogenetic and phylogeographic relationships of Japanese
U. prolifera
within the LPP complex from fresh and brackish water.
Hiraoka et al. (2011)
carried out a hybridization study with Japanese
U. linza
and two strains of
U. prolifera
from Qingdao and Japan.
U. prolifera
from the Qingdao strain hybridized successfully with the Japanese strain, but did not mate with
U. linza
. They insisted that the YS green tidecausing species was a
U. prolifera
subspecies based on 5S rDNA spacer sequences and crossing experiments. As mentioned earlier,
U. prolifera
is identified primarily using morphological traits, and
U. prolifera
from Japan had the same ITS and 5S rDNA spacer sequences as some samples from
Shimada et al. (2008)
, which may have been based on a mis-identification. Our analysis showed that
U. linza
and
U. prolifera
were in distinct clades (
Fig. 3
).
U. prolifera
(UL699, 670) in our results belonged to the same clade as
U. prolifera
samples from Europe (AY255864 and UL698) and New Zealand (EF110202, EF110207, and EF110213) (
Fig. 3
). Thus, we could not conclude that the major strain causing the green tide was
U. prolifera
. We hypothesize that the YS green tide species is a new ecotype of
U. linza
based on reproductive isolation from attached
U. linza
and their morphological differences.
The algae forming the YS green tide were not unialgal species. This green tide included
U. linza
as the predominant species. In addition,
U. compressa
was also found in the floating green mats on the western and southeastern coasts of the YS, even though there was much less material. We also found
U. prolifera
in the Qingdao coast mats. However, it was difficult to distinguish
U. compressa
and
U. prolifera
from
U. linza
based on morphology, and
U. compressa
was highly morphologically variable, including tubular, inflated, and branched forms. Floating green mats include several
Ulva
spp., including
U. compressa
,
U. flexuosa
,
U. linza
, and
U. prolifera
(
Han et al. 2013
,
Huo et al. 2013
). These species may have dispersed from coastal areas and intruded the drifting green mats. Therefore, the floating green mats may include other
Ulva
spp. after moving offshore.
Massive green algal blooms have occurred annually in the YS since 2007, and the blooms off the southwest coast of Korea subsequently appeared 2-3 months after the massive bloom off the coast of China. The bloom-causing species in Korean coastal waters is the same species as the Chinese
U. linza
identified by
rbc
L sequence data, and it has the same
procera
-morphology. The LPP complex of
U. prolifera
referred to in previous studies is
U. linza
, not
U. prolifera
. Even a type locality
U. prolifera
sample has not been considered in
Ulva
phylogenetic studies to date (including this study). Some minor components of the green tide are
U. compressa
and
U. prolifera
, and these are mixed with the primary mat forming entity. We conclude that the green tide-forming species is not
U. prolifera
, but
U. linza
. According to recent studies from New Zealand, Australia, and the USA,
U. prolifera
is monophyletic regardless of the genes (
Heesch et al. 2009
,
Kraft et al. 2010
,
Guidone et al. 2013
,
Kirkendale et al. 2013
). Several
Ulva
spp. phylogenetic studies regard
U. procera
as a separate species from
U. linza
(
Heesch et al. 2009
,
Saunders and Kucera 2010
,
Kirkendale et al. 2013
). However, we conclude that the main bloom-causing species is another ecotype of
U. linza
with
procera
-morphology, because
U. procera
is accepted as a synonym of
U. linza
.
The YS green algal bloom is an annual environmental problem for China and Korea. There are still unanswered questions regarding the bloom-forming species because of their unusual physiological and ecological characteristics. Given the ecological importance of this bloom, an understanding of the causation and potential management of this nuisance phenomenon must begin with correct identification of the algae involved.
Acknowledgements
We are grateful to Moon-Yong Jung of KOPRI for technical assistance. We also thank to Dr. Fabio Rindi of NUI, Galway for some samples from Ireland. This study was supported by the program on “Management plan study for harmful Ulvoid macroalgal bloom in southwest and Jeju coasts (2009-2013)” and “Management of marine organisms causing ecological disturbance and harmful effects” funded by KIMST/MOF.
Bliding C.
1963
A critical survey of European taxa in Ulvales. Part I. Capsosiphon, Percursaria, Blidingia, Enteromorpha
Opera Bot
8
1 -
160
Blomster J.
,
Maggs C. A.
,
Stanhope M. J.
1998
Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles
J. Phycol.
34
319 -
340
DOI : 10.1046/j.1529-8817.1998.340319.x
Blomster J.
,
Maggs C. A.
,
Stanhope M. J.
1999
Extensive intraspecific morphological variation in Enteromorpha muscoides (Chlorophyta) revealed by molecular analysis
J. Phycol.
35
575 -
586
DOI : 10.1046/j.1529-8817.1999.3530575.x
Brodie J.
,
Maggs C. A.
,
John D. M.
2007
Green seaweeds of Britain and Ireland
British Phycological Society
London
94 -
97
Choi D.-L.
,
Noh J.-H.
,
Ryu J.-H.
,
Lee J.-H.
,
Jang P.-K.
,
Lee T.
,
Choi D.-H.
2010
Occurrence of green macroalgae (Ulva prolifera) blooms in the northern east China Sea in summer 2008
Ocean Polar Res.
32
351 -
359
DOI : 10.4217/OPR.2010.32.4.351
Duan W.
,
Guo L.
,
Sun D.
,
Zhu S.
,
Chen X.
,
Zhu W.
,
Xu T.
,
Chen C.
2012
Morphological and molecular characterization of free-floating and attached green macroalgae Ulva spp. in the Yellow Sea of China
J. Appl. Phycol.
24
97 -
108
DOI : 10.1007/s10811-011-9654-7
Gilbert D. G.
1995
SeqPub, a biosequence editor and analysis application
Biological Department, Indiana University
Bloomington, IN
Guidone M.
,
Thornber C.
,
Wysor B.
,
O'Kelly C. J.
2013
Molecular and morphological diversity of Narragansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations
J. Phycol.
49
979 -
995
Guiry M. D.
,
Guiry G. M.
2014
AlgaeBase
World-wide electronic publication, National University of Ireland
Galway
Available from:
Han W.
,
Chen L.-P.
,
Zhang J.-H.
,
Tian X.-L.
,
Hua L.
,
He Q.
,
Huo Y.-Z.
,
Yu K.-F.
,
Shi D.-J.
,
Ma J.-H.
,
He P.-M.
2013
Seasonal variation of dominant free-floating and attached Ulva species in Rudong coastal area, China.
Harmful Algae
28
46 -
54
DOI : 10.1016/j.hal.2013.05.018
Hayden H. S.
,
Blomster J.
,
Maggs C. A.
,
Silva P. C.
,
Stanhope M. J.
,
Waaland J. R.
2003
Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera
Eur. J. Phycol.
38
277 -
294
DOI : 10.1080/1364253031000136321
Heesch S.
,
Broom J.
,
Neill K.
,
Farr T.
,
Dalen J.
,
Nelson W.
2007
Genetic diversity and possible origins of New Zealand populations of Ulva
Ministry of Agriculture and Forestry
Wellington
Biosecurity New Zealand technical paper No. 2007/01
70 -
80
Heesch S.
,
Broom J. E. S.
,
Neill K. F.
,
Farr T. J.
,
Dalen J. L.
,
Nelson W. A.
2009
Ulva, Umbraulva and Gemina: genetic survey of New Zealand taxa reveals diversity and introduced species
Eur. J. Phycol.
44
143 -
154
DOI : 10.1080/09670260802422477
Hiraoka M.
,
Ichihara K.
,
Zhu W.
,
Ma J.
,
Shimada S.
2011
Culture and hybridization experiments on an Ulva clade including the Qingdao strain blooming in the Yellow Sea
PLoS ONE
6
e19371 -
DOI : 10.1371/journal.pone.0019371
Huo Y.
,
Zhang J.
,
Chen L.
,
Hu M.
,
Yu K.
,
Chen Q.
,
He Q.
,
He P.
2013
Green algae blooms caused by Ulva prolifera in the southern Yellow Sea: identification of the original bloom location and evaluation of biological processes occurring during the early northward floating period
Limnol. Oceanogr.
58
2206 -
2218
DOI : 10.4319/lo.2013.58.6.2206
Kim J.-H.
,
Kang E. J.
,
Park M. G.
,
Lee B.-G.
,
Kim K. Y.
2011
Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea
J. Appl. Phycol.
23
421 -
432
DOI : 10.1007/s10811-010-9590-y
Kirkendale L.
,
Saunders G. W.
,
Winberg P.
2013
A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism
J. Phycol.
49
69 -
81
DOI : 10.1111/jpy.12016
Koeman R. P. T.
1985
The taxonomy of Ulva Linnaeus, 1753, and Enteromorpha Link, 1820, (Chlorophyceae) in the Netherlands. Ph.D. dissertation
University of Groningen
Groningen, The Netherlands
201 -
Kraft L. G. K.
,
Kraft G. T.
,
Waller R. F.
2010
Investigations into southern Australian Ulva (Ulvophyceae, Chlorophyta) taxonomy and molecular phylogeny indicate both cosmopolitanism and endemic cryptic species
J. Phycol.
46
1257 -
1277
DOI : 10.1111/j.1529-8817.2010.00909.x
Leliaert F.
,
Zhang X.
,
Ye N.
,
Malta E.
,
Engelen A. H.
,
Mineur F.
,
Verbruggen H.
,
De Clerck O.
2009
Identity of the Qingdao algal bloom
Phycol. Res.
57
147 -
151
DOI : 10.1111/j.1440-1835.2009.00532.x
Liu D.
,
Keesing J. K.
,
Dong Z.
,
Zhen Y.
,
Di B.
,
Shi Y.
,
Fearns P.
,
Shi P.
2010
Recurrence of the world’s largest greentide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms
Mar. Pollut. Bull.
60
1423 -
1432
DOI : 10.1016/j.marpolbul.2010.05.015
Liu D.
,
Keesing J. K.
,
Xing Q.
,
Shi P.
2009
World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China
Mar. Pollut. Bull.
58
888 -
895
DOI : 10.1016/j.marpolbul.2009.01.013
Liu F.
,
Pang S. J.
,
Chopin T.
,
Xu N.
,
Shan T. F.
,
Gao S. Q.
,
Sun S.
2010
The dominant Ulva strain of the 2008 green algal bloom in the Yellow Sea was not detected in the coastal waters of Qingdao in the following winter
J. Appl. Phycol.
22
531 -
540
DOI : 10.1007/s10811-009-9489-7
Liu F.
,
Pang S. J.
,
Xu N.
,
Shan T. F.
,
Sun S.
,
Hu X.
,
Yang J. Q.
2010
Ulva diversity in the Yellow Sea during the large-scale green algal blooms in 2008-2009
Phycol. Res.
58
270 -
279
DOI : 10.1111/j.1440-1835.2010.00586.x
Liu F.
,
Pang S. J.
,
Zhao X. B.
,
Hu C. M.
2012
Quantitative, molecular and growth analyses of Ulva microscopic propagules in the coastal sediment of Jiangsu province where green tides initially occurred
Mar. Environ. Res.
74
56 -
63
DOI : 10.1016/j.marenvres.2011.12.004
Maddison D. R.
,
Maddison W. P.
2003
MacClade, 4.06
Sinauer Associates
Sunderland, MA
Marshall K.
,
Joint I.
,
Callow M. E.
,
Callow J. A.
2006
Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green Alga Ulva linza
Microb. Ecol.
52
302 -
310
DOI : 10.1007/s00248-006-9060-x
Pang S. J.
,
Liu F.
,
Shan T. F.
,
Xu N.
,
Zhang Z. H.
,
Gao S. Q.
,
Chopin T.
,
Sun S.
2010
Tracking the algal origin of the Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses
Mar. Environ. Res.
69
207 -
215
DOI : 10.1016/j.marenvres.2009.10.007
Saunders G. W.
,
Kucera H.
2010
An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae
Cryptogam. Algol.
31
487 -
528
Shimada S.
,
Yokoyama N.
,
Arai S.
,
Hiraoka M.
2008
Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa
J. Appl. Phycol.
20
979 -
989
DOI : 10.1007/s10811-007-9296-y
Son Y. B.
,
Choi B. -J.
,
Kim Y. H.
,
Park Y. -G.
2015
Tracing floating green algae blooms in the Yellow Sea and the East China Sea using GOCI satellite data and Lagrangian transport simulations
Remote Sens. Environ.
156
21 -
33
DOI : 10.1016/j.rse.2014.09.024
Swofford D. L.
2002
PAUP*: phylogenetic analysis using parsimony (*and other methods)
Sinauer Associates
Sunderland, MA
Tan I. H.
,
Blomster J.
,
Hansen G.
,
Leskinen E.
,
Maggs C. A.
,
Mann D. G.
,
Sluiman H. J.
,
Stanhope M. J.
1999
Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha
Mol. Biol. Evol.
16
1011 -
1018
DOI : 10.1093/oxfordjournals.molbev.a026190
Wang J.
,
Jiang P.
,
Cui Y.
,
Li N.
,
Wang M.
,
Lin H.
,
He P.
,
Qin S.
2010
Molecular analysis of green-tide-forming macroalgae in the Yellow Sea
Aquat. Bot.
93
25 -
31
DOI : 10.1016/j.aquabot.2010.03.001
Zhang X.
,
Xu D.
,
Mao Y.
,
Li Y.
,
Xue S.
,
Zou J.
,
Lian W.
,
Liang C.
,
Zhuang Z.
,
Wang Q.
,
Ye N.
2011
Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom
Limnol. Oceanogr.
56
233 -
242
DOI : 10.4319/lo.2011.56.1.0233