Sergeeva et al 07
ISSN 1063-0740, Russian Journal of Marine Biology, 2007, Vol. 33, No. 1, pp. 30–42. © Pleiades Publishing, Ltd., 2007.
Original Russian Text © O.S. Sergeeva, T.V. Titlyanova, E.A. Titlyanov, 2007, published in Biologiya Morya.
ECOLOGY
Species Composition and Distribution of Algae
on the Fringing Coral Reef of Sesoko Island
(Ryukyu Archipelago) before and after
the Natural Catastrophe of 1998
O. S. Sergeevaa, c, T. V. Titlyanovab, c, and E. A. Titlyanovb, c
a Pacific Institute of Bioorganic Chemistry, Far East Division, Vladivostok 690022
bA.V. Zhirmunsky Institute of Marine Biology, Far East Division, Vladivostok 690041
cSesoko Station of the Tropical Biosphere Research Center, Okinawa 905–0227, Japan
e-mail: etitlyanov@mail.ru
Received September 21, 2006
Abstract—The species composition and distribution of marine plants on the fringing reef of Secoko Island
were studied before and after the mass coral mortality in 1998. The study showed that changes in the bottom
communities that occurred after bleaching of corals were caused by the presumed development of marine plants
substituting reef-building corals on the bottom. The number of algal species grew from 211 to 345. The projec-
tive cover (PC) of hard substrate with macroalgae increased: in 1998, it was 1–10% in the subtidal zone and
20–50% in the intertidal zone, while in 2002 through 2005, the PC reached 71% in the subtidal and 40–85% in
the intertidal zone. It is assumed that the phase of the “plant reef” on Sesoko Island is a temporary event, and
that the coral reef can recover within several decades, unless a natural catastrophe occurs again.
DOI: 10.1134/S1063074007010038
Key words: macroalgae, coral reef, bleaching, “phase shift,” competition.
The ecosystem of a coral reef is based on the vital of water temperature by 1–2°C in July–August caused
activity of hermatypic reef–building corals that produce extensive coral mortality even in the subtropical zone:
a hard carbonate substrate for the settling of benthic up to 80% of the total coral population died on Okinawa
organisms. On healthy reefs, corals usually occupy up Island [10].
to 80–90% of the bottom area; they are the main pri- Diaz-Pulido and McCook [4] show that immedi-
mary producers of organic matter at the expense of the ately after coral bleaching and mortality dead coral col-
photosynthesis of their intracellular symbionts, namely onies were colonized with marine algae and this colo-
dinoflagellate algae. Other primary producers of nization resulted in a shift from corals to algae. This
organic matter are benthic and planktonic marine “phase shift” after the mass mortality of corals was
plants; macrophytes among them yield the highest pro- observed on the Great Barrier Reef [4] and on Carib-
duction. On a healthy coral reef, macrophytes cover bean coral reefs [6]. Some authors believe that the
from 1 to 20% of the hard substrate of the bottom [8]. phase shift leads to the disappearance of reefs, as the
The algae of coral reefs present a diverse species com- algae destroy (rather than build, as corals do) the car-
position; they successfully compete with corals for sub- bonate substrate, the base of the reef. The “phase shift”
strate, space and other life resources [13]. could be a temporary event in an active reparative pro-
The total area of contemporary coral reefs amounts cesses, when corals settle on the substrate and old col-
to about 600 thousand sq. km [1]. In the last decades, a onies recover [13, 20].
catastrophic destruction of shallow–water coral reefs There is no way to predict the future fate of a coral
took place and, consequently, their productivity and reef without research into the contemporary structure
biological diversity were reduced [3]. The coral mortal- of the reef and its species composition, i.e., the number
ity and reef destruction characteristic of the entire trop- and distribution of organisms competing for substrate,
ical zone of the World Ocean depend mostly on water among them corals and benthic macro- and microalgae,
temperature increases that cause coral bleaching and as well as some invertebrate animals destroying the
expulsion of symbiotic algal cells from coral tissues substrate. It is no less important to study competitive
(often together with the host animal cells) [3]. abilities of reef-building corals and mass algal species
The most destructive consequences were recorded [4, 12].
in 1998 after events of elevated surface seawater tem- Notwithstanding the urgency of these studies, only a
perature in many areas of the World Ocean [11]. A rise few works deal with the study of the biological struc-
30
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 31
ture of coral reefs after catastrophes [5, 7, 8, 10, 11, 17]; Okinawa Is
these studies mostly describe changes in the species Sesoko Is
composition and projective cover of the bottom with
corals. A few works concern development of algae on
damaged coral reefs [4, 11]. During the period from
1995 to 2005, the species composition and distribution Naha
of algae were studied at the fringing reef of Sesoko
Sesoko Beach
Island. After the catastrophe in 1998, about 75 to 80%
of the corals died in shallow waters around the island
[10]. This study is aimed at a comparison of the compo- Sesoko Is
sition and distribution of algal species on the fringing
reef of Sesoko Island before and after the natural catas-
trophe in 1998.
Biostation
“Sesoko”
MATERIAL AND METHODS
The investigations were conducted at the fringing
reefs of the south-eastern shore (opposite the Biologi- Fig. 1. Schematic map of Sesoko Is.
cal Station of the University of Ryukyus) and the west-
ern shore (Sesoko Beach) of Sesoko Island, lying near
Okinawa (Japan) in the East- Chinese Sea (26°38′N, RESULTS
127°52′E) (Fig. 1). Algae were collected, herbarized
and identified from May to October in 1995, October to From 1995 until the natural catastrophe of 1998, our
December of 1997, January to April of 1998, March to studies revealed 211 species of marine plants, of them
December of 2002, January to March of 2003, July 78 green algae (36.9%), 23 brown algae (10.9%),
2004, and February to May of 2005. The coral reef near 96 red algae (45.5%), 9 blue-green algae (4.3%), 1 yel-
Sesoko Island, according to the classification of Veron low-green alga (0.5%), and 4 species of sea grasses
[21], is assigned to the fringing reef type. The coast is (1.9%). In the years 2002 through 2005, the list com-
formed by a fossil coral reef. The reef platform is 10 to prised 345 species (Table 1). It is interesting, that quan-
20 m broad; the lagoon is shallow, 1 to 3 m wide. Water titative relationship of species did not change signifi-
depth at the reef flat is about 1 m at a high tide. The reef cantly: we documented 99 species of green algae
slope is quite steep, stretches down to a depth of 30 m (30.1%), 36 brown algae (11%), 152 red algae (46.2%),
and passes into a sandy bottom. The surface water tem- 37 blue-green algae (11.2%), 1 yellow-green alga
peratures in the sea is, on the average, approximately (0.3%), and 4 species of seagrasses (1.2%). Both
+29°C (with 31°C as the maximum) in the summer and before and after the dramatic coral mortality (Fig. 2),
21°C in the winter (with 18°C as the minimum). Water the highest relative number of marine plant species was
salinity varies from 34.5 to 35.2‰, depending on the found in the intertidal collections (60%), a lower num-
season [14]. ber was collected in the subtidal zone (30%), and only
10% were recorded for the supralittoral zone. The por-
The object of study was algae collected by scuba- tion of epiphytic species also did not change, it made up
diving in the intertidal and subtidal zones at the fringing about 15% of the total number of species. About 50%
reef of Sesoko Island. of all algae collected during the years inhabited an algal
Marine plants were identified with the use of Olym- turf community, as they did before the catastrophe.
pus stereo and light microscopes and photographed Ulva spp., Gelidiella acerosa, Jania spp., Centro-
with a Olympus Camedia 5050C digital camera. The ceras clavulatum, Bostrychia tenella, and Digenea sim-
projective algal cover of the bottom in the supralittoral, plex dominated on the healthy coral reef. As well,
intertidal and subtidal zones was determined by the Enteromorpha spp., Codium spp., Ulva fasciata,
generally accepted hydrobiological method with the Boodlea composita, Bornetella sphaerica, Actinotri-
use of a 50x50 cm frame, in triplicate for each zone. chia fragilis, Tricleocarpa spp., Ganonema farinosum,
Algae in the frame were photographed, collected, and and Liagora ceranoides became new dominants after
identified in the laboratory, the number of specimens coral mortality. At the same time, Cladophora cate-
within the frame was counted for every species, and the nata, Boodlea coacta, Ceratodictyon intricatum and
mass of the algal species was weighed. some other species were no longer found on the dam-
aged reef.
Color prints of the algae in the frame were made on
a high-quality paper with the use of an Epson The projective cover (PC) of microalgae on the hard
KA450PM printer, cut and weighed. The “weight” substrate changed significantly after the catastrophe
method of was applied to calculate the projective cover (Table 2). The PC of algae on Sesoko and some other
area of algae on the bottom [20]. islands of the Ryukyus made up 1–10% in the subtidal
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
32 SERGEEVA et al.
Table 1. Algae collected on the fringing reef of Sesoko Island: before a natural catastrophe (1995–1998) and after the event
(2002–2005)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
CHLOROPHYTA
Micrasterias sp. – – – + –
Phaeophila dendroides (P. Crouan & H. Crouan) – – – + enl
Batters
Monostroma nitidum Wittrock up. int +++ int, up. int +++ M
Enteromorpha clathrata (Roth) Greville m. int ++ int +++ T, ep
E. compressa (Linnaeus) Nees int + int +++ T
E. flexuosa (Wulfen) J. Agardh – – int, l. int + T
E. kylinii Bliding – – int + T
E. prolifera (O.F. Muller) J. Agardh int + int + T
E. ralfsii Harvey – – int + T
Ulva conglobata Kjellman int +++ int +++ Ms(p)
U. fasciata Delile int, l. int – int, l. int +++ M
U. lactuca Linnaeus int – int ++ Ms(p)
U. pertusa Kjellman int, up. int +++ int, up. int +++ M
U. reticulata Forsskål l. int + washed + Ms(p)
Pringsheimiella scutata (Reinke) Marchewianka – – l. int + ep
Ulvella lens (P. Crouan & H. Crouan) sub + up. int + ep
Verdigellas sp. – – washed + –
Anadyomene wrightii Harvey ex J. Gray l. int ++ int, l. int ++ T
Acrochaete viridis (Reinke) Nielsen l. int + l. int + ep
(=Entocladia viridis Reinke)
Acrochaete sp. – – l. int + ep
Ectochaete leptochaete (Huber) Wille – – – + enph
Gomontia arrhiza Hariot l. int + l. int + ep
Microdictyon nigrescens (Yamada) Setchell inf. lit + inf. lit + T
M. okamurai Setchell inf. lit + inf. lit + T
M. japonicum Setchell int + int + T
Chaetomorpha basiretrorsa Setchell up. int + up. int + T
C. capillaris (Kützing) Børgesen l. int + l. int + T
C. linum (O.F. Müller) Kützing inf. lit + inf. lit + Ms(p)
C. pachynema Montagne – – l. int + Ms(p)
C. javanica Kützing – – l. int + T
Cladophora catenata (Linnaeus) Kützing l. int + – – T
C. fuscicularis (Martens ex C. Agardh) Kützing – – l. int + T
C. fuliginosa Kützing – – l. int + T
C. laetevirens (Dillwyn) Kützing l. int + l. int + T
C. vagabunda (Linnaeus) van den Hoek int + int ++ T
Rhizoclonium grande Børgesen int + int ++ T
R. implexum (Dillwyn) Kützing inf. lit + inf. lit ++ T, ep
Boodlea coacta (Dickie) G. Murray & De Toni int + – – T, f. sw
B. composita (Harvey) Brand int + int ++ T, f. sw
B. struveoides Howe – – int + T, f. sw
Struvea anastomosans (Harvey) int + int + T
Piccone & Grunow ex Piccone
Cladophoropsis herpestica (Montagne) Howe – – int + T
C. membranacea (Hofman Bang ex C. Agardh) – – int + T
Børgesen
C. sundanensis Reinbold int + int ++ T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 33
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
C. zollingeri (Kützing) Reinbold int + int ++ Mat
Cladophoropsis sp. int + int + T
Dictyosphaeria cavernosa (Forsskål) Børgesen int ++ int +++ Ms(p)
D. versluysii Weber-van Bosse int + int + Ms(p)
Siphonocladus rigidus Howe l. int + l. int + ep
Ventricaria ventricosa (J. Agardh) Olsen & J. West l. int ++ l. int + Ms(p)
Valonia aegagropila C. Agardh l. int ++ l. int + Mat
V. fastigiata Harvey ex J. Agardh l. int + l. int + Mat
V. macrophysa Kützing l. int + l. int + Ms(p)
V. utricularis (Roth) C. Agardh l. int + l. int + Ms(p)
Bryopsis harveyana J. Agardh l. int, inf. lit + l. int, inf. lit + T
B. indica A. Gepp & E. Gepp l. int, inf. lit + l. int, inf. lit + T, ep
B. pennata Lamouroux l. int + l. int + T
B. plumosa (Hudson) C. Agardh l. int, inf. lit + l. int, inf. lit + T
B. ryukyuensis Yamada – – l. int, inf. lit + T
Derbesia attenuata Dawson – – sub + T
D. fastigiata Taylor – – inf. lit + T
D. marina (Lyngbye) Solier inf. lit + inf. lit + T
Codium adhaerens (Cabrera) C. Agardh int, inf. lit ++ int, l. int ++ Ms(p)
C. intricatum Okamura l. int, inf. lit ++ l. int, inf. lit +++ Ms(p)
C. repens P. Crouan & H. Crouan l. int, inf. lit + l. int, inf. lit ++ Ms(p)
Caulerpa cupressoides (Vahl) C. Agardh l. int + l. int + T
C. fastigiata Montagne int + int + T
C. lentillifera J. Agardh – – int + T
C. macrophysa (Sonder ex Kützing) G. Murray int + int + T
C. microphysa (Weber-van Bosse) Feldmann l. int + l. int + T
C. nummularia Harvey ex J. Agardh int + int ++ T
C. racemosa (Forsskål) J. Agardh int + int + T
C. racemosa (Forsskål) Weber-van Bosse var. int + – – T
clavigera (Turn.) Weber-van Bosse
C. racemosa var. corynephora (Montagne) – – int + T
Weber-van Bosse
C. racemosa (Forsskål) J. Agardh var. int, inf. lit + int, l. int + T
peltata (Lamouroux) Eubank in Stephenson
C. serrulata (Forsskal) J. Agardh int, inf. lit + int, inf. lit + T
C. serrulata var. serrulata f. lata (Weber-van Bosse) int, inf. lit + int, inf. lit + T
Tseng
C. serrulata J. Agardh var. serrulata f. spiralis int, inf. lit ++ int, inf. lit ++ T
(Weber-van Bosse) Gilbert
C. sertularioides (S. Gmelin) Howe l. int, inf. lit + l. int ++ T
C. vickersiae Børgesen – – int + T
C. webbiana Montagne f. tomentella (Harvey) int + – – T
Weber-van Bosse
Caulerpella ambigua (Okamura) Prud'homme van l. int + l. int + T
Reine & Lokhorst
Ostreobium quekettii Bornet & Flahault – + – ++ enl
Penicillus sibogae Gepp – – – + ep
Avrainvillea erecta (Berkeley) A. Gepp & E. Gepp m. int + m. int + Ms(p)
Boodleopsis pusilla (Collins) W.R. Taylor, Joly & inf. lit + inf. lit + Ms(p)
Bernatowicz
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
34 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Chlorodesmis fastigiata (C. Agardh) Ducker int, m. int + int, m. int + Ms(p)
Pseudochlorodesmis furcellata (Zanardini) Borgesen – – l. int + Ms(p)
Halimeda discoidea Decaisne inf. lit + inf. lit + Ms(p)
H. macroloba Decaisne – – int + Ms(p)
H. macrophysa Askenasy – – inf. lit ++ Ms(p)
H. opuntia (Linnaeus) Lamouroux int, inf. lit + int, inf. lit Ms(p)
H. tuna (Ellis & Solander) Lamouroux l. int, inf. lit + l. int, inf. lit ++ Ms(p)
Tydemania expeditionis Weber-van Bosse inf. lit + – – Ms(p)
Rhipidosiphon javensis (Montagne) Gepp int, inf. lit +++ int, inf. lit +++ T
Cymopolia van-bosseae Solms-Laubach inf. lit sgl – – Ms(p)
Dasycladus vermicularis (Scopoli) Krasser l. int sgl – – Ms(p)
Bornetella nitida Sonder int, inf. lit + int, inf. lit + Ms(p)
B. oligospora Solms-Laubach int, inf. lit + int, inf. lit + Ms(p)
B. sphaerica (Zanardini) Solms-Laubach int, inf. lit ++ int, inf. lit +++ Ms(p)
Neomeris annulata Dickie l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
N. bilimbata Koster – – l. int, inf. lit + Ms(p)
Acetabularia clavata Yamada inf. lit + inf. lit + Ms(p)
A. dentata Solms- Laubach int, inf. lit ++ int, inf. lit +++ Ms(p)
A. exigua Solms-Laubach inf. lit ++ inf. lit ++ Ms(p)
A. parvula Solms- Laubach l. int, inf. lit + l. int, inf. lit ++ Ms(p)
A. pusilla (Howe) Collins inf. lit – inf. lit + Ms(p)
PHAEOPHYTA
Ectocarpus elachistaeformis Heydrich – – l. int + ep
E. siliculosus (Dillwyn) Lyngbye – – l. int + ep
Ectocarpus sp. – – l. int + ep
Feldmannia irregularis (Kützing) G. Hamel – – l. int, inf. lit ++ ep
Hincksia indica (Sonder) Papenfuss et Chihara l. int, inf. lit + l. int, inf. lit + ep
H. mitchelliae (Harvey) P. Silva l. int, inf. lit + l. int, inf. lit +++ T, ep
Pilayella littoralis (Linnaeus) Kjellman – – int + ep
Ralfsia expansa (J. Agardh) J. Agardh int + int ++ Ms(p)
Chilionema ocellata (Kützing) Kuckkuck – – l. int, inf. lit ++ ep
Chnoospora implexa J. Agardh inf. lit ++ inf. lit ++ Ms(p)
Colpomenia sinuosa (Mertens ex Roth) Derbes & l. int ++ l. int ++ Ms(p)
Solier
Hydroclathrus clathratus (C. Agardh) Howe inf. lit + inf. lit + Ms(p)
Sphacelaria novae-hollandiae Sonder l. int + l. int ++ T, ep
S. rigidula Kützing l. int ++ l. int ++ T, ep
S. tribuloides Meneghini l. int ++ l. int ++ T, ep
Dictyota dichotoma (Hudson) Lamouroux l. int + l. int + Ms(p)
D. friabilis Setchell – – l. int + T
D. humifusa Hörnig, Schnetter & Coppejans – – l. int ++ Ms(p)
D. linearis (C. Agardh) Greville l. int + l. int + T
D. patens J. Agardh l. int + l. int + T
Dictyota sp. – – int + T
Dictyopteris undulata Holmes – – up. int ++ T
Dictyopteris sp. – – up. int ++ T
Lobophora variegata (Lamouroux) Womersley ex l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Oliveira
Dictyerpa stage of Padina [Vaughaniella stage] int + int + T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 35
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Padina australis Hauck int. pl + int. pl + Ms(p)
P. boryana Thivy int. pl ++ int. pl ++ M
P. gymnospora (Kützing) Sonder int, int. pl + – – Ms(p)
P. minor Yamada int, inf. lit + int, inf. lit + Ms(p)
Cladosiphon okamuranus Tokida m. int + m. int + Ms(p)
Hormophysa cuneiformis (J. Gmelin) P. Silva inf. lit + inf. lit + Ms(p)
Sargassum crassifolium J. Agardh inf. lit + inf. lit ++ Ms(p)
S. cristaefolium (=duplicatum) C. Agardh – – int. pl ++ Ms(p)
S. feldmannii Pham Hoang Ho – – inf. lit ++ Ms(p)
S. polycystum C. Agardh – – inf. lit + Ms(p)
S. thunbergii (Mertens) C. Kuntze int, int. pl ++ int, int. pl ++ Ms(p)
Turbinaria ornata (Turner) J. Agardh l. int, inf. lit ++ l. int, inf. lit +++ Ms(p)
RHODOPHYTA
Stylonema alsidii (Zanardini) K. Drew l. int, inf. lit + l. int, inf. lit + ep
Chroodactylon ornatum (C. Agardh) Basson – + – + ep
Erytrotrichia carnea (Dillwyn) J. Agardh l. int, inf. lit + l. int, inf. lit + ep
Erythropeltis subintegra (Rosenvinge) – – l. int, inf. lit ++ ep
Kornmann et Sahling
Porphyra crispata Kjellman – – sub + Ms(p)
Acrochaetium catenulatum Howe – – l. int + ep
A. crassipes (Børgesen) Børgesen – – l. int + ep
A. gracile Børgesen – – l. int + ep
A. moniliforme (Rosenvinge) Børgessen l. int + l. int + ep
A. occidentale Børgessen – – l. int + ep
A. seriatum Børgesen – – l. int + ep
A. subseriatum Børgessen – – l. int + ep
A. virgatulum (Harvey) Bornet – – l. int + ep
Acrochaetium sp. l. int + l. int + ep
Rhodochorton sp. int + – – ep
Liagora ceranoides Lamouroux – – l. int, inf. lit ++ Ms(p)
Liagora sp. l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Ganonema farinosum (Lamouroux) Fan & Wang l. int, inf. lit + l. int, inf. lit + Ms(p)
Trichogloeopsis pedicellata (Howe) Abbott & Doty – – l. int, inf. lit sgl Ms(p)
Yamadaella caenomyce (Decaisne) Abbott inf. lit + inf. lit + Ms(p)
Trichogloea requienii (Montagne) Kützing inf. lit + inf. lit + Ms(p)
Actinotrichia fragilis (Forsskål) Børgesen inf. lit ++ inf. lit ++ Ms(p)
Galaxaura fasciculata Kjellman inf. lit + inf. lit ++ Ms(p)
G. marginata (Ellis et Solander) Lamouroux – – int ++ Ms(p)
G. obtusata (J. Ellis & Slander) J.V. Lamouroux – – inf. lit + Ms(p)
G. subfruticulosa Chou inf. lit + inf. lit ++ Ms(p)
Tricleocarpa fragilis (Linnaeus) Huisman & inf. lit + inf. lit ++ Ms(p)
Townsend (=Galaxaura oblongata)
T. cylindrica (Ellis et Solander) Huisman & inf. lit + inf. lit ++ Ms(p)
Borowitzka (=Galaxaura fastigiata)
Gelidiella acerosa (Forsskål) Feldmann et Hamel int ++ int ++ T
G. adnata Dawson int + int + T
G. pannosa (J. Feldmann) J. Feldmann & G. Hamel – – int + T
Gelidiella sp. int + int + T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
36 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Pterocladiella capillacea (Gmelin) Santelices & – – l. int + T
Hommersand
Gelidium pusillum (Stackhouse) Le Jolis int + int, up. int ++ T
G. divaricatum Martens int + int + T
Wurdemannia miniata (Sprengle) Feldmann & int, up. int + int, up. int ++ T
Hamel
Peyssonnelia conchicola Piccone & Grunow – – l. int, inf. lit + Ms(p)
in Piccone
P. inamoena Pilger – – l. int, inf. lit + Ms(p)
Jania adhaerens Lamouroux int, inf. lit +++ int, inf. lit +++ T, ep
J. capillacea (Yendo) Yendo int, inf. lit +++ int, inf. lit +++ T, ep
J. ungulata f. brevior (Yendo) Yendo int, inf. lit ++ int, inf. lit ++ T, ep
Amphiroa fragilissima (Linnaeus) J.V. Lamouroux l. int + l. int ++ Ms(p)
Hydrolithon farinosum (J.V. Lamouroux) Penrose & int + int ++ ep
Y.M. Chamberlain
Porolithon sp. sub – sub + Ms(p)
Pneophyllum conicum (E.Y. Dawson) Keats, – – int, inf. lit + Ms(p)
Y.M. Chamberlain & Baba
P. fragile Kützing int, inf. lit + int, inf. lit + ep
Mastophora rosea (C. Agardh) Setchell – – int, inf. lit ++ M
Titanophora pulchra Dawson – – washed sgl –
Gelidiopsis intricata (C. Agardh) Vickers inf. lit ++ inf. lit ++ T
G. scoparia (Montagne & Millardet) De Toni – – inf. lit + T
G. variabilis (J. Agardh) Schmitz l. int, inf. lit + l. int, inf. lit + T
Lomentaria corallicola Børgesen int + int + T
L. mauritiana Børgesen int + int + T
Chryzymenia okamurai Yamada et Segawa – + washed + –
Coelarthrum boergesenii Weber-van Bosse l. int, inf. lit + l. int, inf. lit + Ms(p)
(=C. coactum Okamura)
Botryocladia skottsbergii (Børgesen) Levring int + – – T
Coelothrix irregularis Børgesen int, inf. lit + int, inf. lit ++
Eucheuma denticulatum (Burman) Collins et Harvey l. int sgl washed sgl –
Gracilaria arcuata Zanardini int + int + Ms(p)
G. blodgettii Harvey – – int + Ms(p)
G. coronopifolia J. Agardh – – int + Ms(p)
G. salicornia (C. Agardh) Dawson int + int + Ms(p)
Ceratodictyon intricatum (C. Agardh) R.E. Norris int + – – Ms(p)
C. spongiosum Zanardini l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Caulacantus ustulatus (Mertens ex Turner) Kützing int + int ++ T
Hypnea cervicornis J. Agardh – – int + T, ep
H. charoides Lamouroux l. int + l. int + T
H. boergesenii Tanaka – – l. int + T
H. esperi Grunov int + int + T, ep
H. nidulans Setchell int + – – T
H. pannosa J. Agardh l. int, inf. lit + l. int, inf. lit ++ T
H. spinella (C. Agardh) Kützing int, inf. lit + int, inf. lit ++ T, ep
H. valentiae (Turner) Montagne l. int, inf. lit + l. int, inf. lit + T
Ahnfeltiopsis flabelliformis Harvey – – – + Ms(p)
Cruoriella sp. – – l. int sgl Ms(p)
Erythrodermis sp. – – l. int + Ms(p)
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 37
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Haematocelis sp. – – l. int sgl Ms(p)
Plocamium telfairiae (W. Hooker & Harvey) – – l. int, inf. lit + Ms(p)
Harvey ex Kützing
Chondracanthus intermedius (Suringar) Hommersand int + int + T
Rhodymenia coacta Okamura int + – – Ms(p)
R. anastomosans Weber-van Bosse – – int. pl + Ms(p)
Rhodymenia sp. – – int + Ms(p)
Rhodopeltis borealis Yamada – – inf. lit + Ms(p)
Portieria hornemanni (Lyngbye) P. Silva – – inf. lit + Ms(p)
Champia parvula (C. Agardh) Harvey int + int ++ T, ep
C. japonica Okamura int + int + T, ep
C. vieillardii Kützing – – l. int + T, ep
Asparogopsis taxiformis (Delile) Trevisan inf. lit + inf. lit + Ms(p)
Falkenbergia hillebrandii (Bornet) Falkenberg l. int, inf. lit + l. int, inf. lit ++ ep
(=sporophyte of A. taxiformis)
Dudresnaya japonica Okamura – – washed + –
D. hawaiiensis R. K. S. Lee – – washed + –
Gymnothamnion elegans (Schousbold ex C. Agardh) int – int + ep
J. Agardh
Antithamnion lherminieri (P. Crouan & H. Crouan) l. int + l. int + ep
Bornet ex Nasr
Antithamnion sp. l. int + l. int + ep
Antithamnionella sp. – – l. int + ep
Anotrichium tenue (C. Agardh) Nägeli int + int ++ T, ep
Aglaothamnion callophyllidicola Yamada int + int + ep
Wrangelia argus (Montagne) Montagne int +++ int +++ T
W. dumontii (Dawson) Abbott – – int + T
W. penicillata (C. Agardh) C. Agardh – – int + T
Spyridia filamentosa (Wulfen) Harvey int, int. pl ++ int, int. pl +++ ep
Corallophila apiculata (Yamada) R. Norris l. int ++ l. int ++ ep
(=Centroceras apiculatum Yamada)
Centroceras clavulatum (C. Agardh) Montagne int +++ int +++ T, ep
C. inerme Kützing int + int + T, ep
Ceramium aduncum Nakamura – – int + T, ep
C. cingulatum Weber-van Bosse l. int + l. int + T, ep
C. codii (Richards) Mazoyer – – l. int + T, ep
C. fastigiatum Harvey – – l. int ++ T, ep
C. fimbriatum Setchell & Gardner l. int + l. int + T, ep
C. flaccidum (Kützing) Ardissone l. int ++ l. int ++ T, ep
C. howei Dawson l. int + l. int + T, ep
C. macilentum Dawson – – l. int + T, ep
C. paniculatum Okamura – – l. int + T, ep
C. procumbens Setchell & Gardner – – l. int + T, ep
C. sympodiale Dawson – – l. int + T, ep
Pleonosporium borrieri (Smith) Nägeli – – l. int + ep
Spermothamnion sp. l. int + l. int + ep
Crouania attenuata (C. Agardh) J. Agardh int ++ int ++ T, ep
Crouania sp. – – int + T, ep
Griffithsia metcalfii Tseng int ++ int ++ T, ep
G. subcylindrica Okamura int + int + T, ep
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
38 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
G. japonica Okamura – – int + Ms(p)
G. weber-van-bosseae Børgesen – – int + T, ep
Haloplegma duperreyi Montagne – – washed + –
Dasya mollis Harvey int + int + Ms(p)
Dasya sp. – – int + Ms(p)
Heterosiphonia crispella (C. Agardh) Wynne l. int + l. int + T, ep
Hypoglossum sp. l. int + l. int + ep
Martensia pavonia (J. Agardh) J. Agardh – – washed sgl –
Taenioma perpusillum J. Agardh (J. Agardh) l. int + l. int ++ ep
Nitophyllum adhaerens Wynne – – – ++ T, ep
Polysiphonia ferulacea Suhr ex J. Agardh l. int + l. int + T, ep
P. japonica Harvey var. savatieri (Hariot) Yoon l. int + l. int + T, ep
Polysiphonia sp. up. int + up. int + T, ep
Bostrychia tenella (Lamouroux) J. Agardh up. int, +++ up. int, +++ M
sup. lit sup. lit
Herposiphonia parca Setchell int + int + ep
H. secunda (C. Agardh) Ambronn f. secunda int ++ int ++ ep
(C. Agardh) Wynne
H. secunda (C. Agardh) Ambronn f. tenella int ++ int ++ ep
(C. Agardh) Wynne
Lophosiphonia villum (J. Agardh) Setchell & Gardner l. int + l. int ++ T, ep
Tolypiocladia glomerulata (C. Agardh) Schmitz l. int ++ l. int ++ T, ep
Acanthophora muscoides (Linnaeus) – – int + T
Bory de Saint-Vincent
A. spicifera (Vahl) Børgesen int. pl ++ int. pl ++ T
Leveillea jungermannioides (Martens et Hering) int + int ++ T, ep
Harvey
Laurencia brongniartii J. Agardh l. int + l. int + T
L. cartilaginea Yamada – – l. int + T
L. implicata J. Agardh – – l. int + T
L. obtusa (Hudson) J.V. Lamouroux int + int ++ T
L. okamurae Yamada – – int +++ M
L. parvipapillata Tseng int + int + T
L. papillosa (C. Agardh) Greville int + int +++ M
L. perforata (Bory de Saint-Vincet) Monagne – – int + T
L. saitoi Perestenko l. int + – – T
L. yamadana Howe l. int + – – T
Chondria repens Børgesen l. int ++ l. int ++ T
C. dasyphylla (Woodward) C. Agardh int + int + T
C. minutula Weber-van Bosse – – int + T
Chondria sp. int + int + T
Digenea simplex (Wulfen) C. Agardh l. int, inf. lit +++ l. int, inf. lit +++ T
Acrocystis nana Zanardini int + int + T, ep
CYANOPHYTA
Dermocarpella clavata (Setchell & Gardner) – – – + ep
Pham Hoang Ho
Dermocarpa acervata (Setchell & Gardner) – – – + ep
Pham Hoang Ho
Aphanocapsa littoralis Hansgirg – – – ++ ep
Symploca hydnoides (Harvey) Kützing sup. lit + sup. lit + Ms(p)
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 39
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Lyngbya bouillonii Holffmann & Demoulin – – int + T
L. epiphytica Hieronymus int + int + ep
L. confervoides C. Agardh int + int + T
L. majuscula (Dillwyn) Harvey – – int ++ T
L. polychroa (Meneghini) Rabenhorst int + int + T
(=L. sordida Gomont)
L. semiplena (C. Agardh) J. Agardh – – int + T
Lyngbya sp. int + int + T
Oscillatoria limnetica Lemmermann – – int + T
O. margaritifera (Kützing) Gomont – – l. int + T
O. miniata (Zanardini) Gomont – – l. int + T
O. tenuis C. Agardh – – l. int + T
Oscillatoria sp. int + int + T
Phormidium corium (C. Agardh) Kützing – – l. int + T
P. crosbyanum Tilden – – l. int + T
P. tenue (Menighini) Gomont – – l. int ++ T
Phormidium sp. – – l. int + T
Spirulina major Kützing – – int sgl T
S. subsalsa Oersted int + int + T
S. subtilissima Kützing – – int + T
Spirulina sp. – – int + T
Calothrix confervicola (Dillwyn) C. Agardh – – int + ep
C. crustacea Thuret – – int + ep
C. parasitica (Chauvin) Thuret – – int + ep
C. scopulorum (Weber et Mohr) C. Agardh – – int + ep
Calothrix sp. 1 int + int ++ ep
Calothrix sp. 2 int + int ++ ep
Schizothrix sp. – – int + T
Nostoc commune Vaucher – – int + T
Hormothamnion sp. – – int + T
Rivularia bornetiana? – – int + T
Rivularia spp. – – int + T
Dichothrix sp. – – int ++ T
Brachytrichia quoyi (C. Agardh) Bornet & Flahault – – int + T
XANTHOPHYTA
Pseudodichotomosiphon constricta (Yamada) int + int + T
Yamada
ANTHOPHYTA
Thalassia hemprichii (Ehrenberg) Ascherson m. int + m. int + Ms(p)
Cymodocea serrulata (R. Brown) Ascherson et m. int + m. int + Ms(p)
Magnus
Halophila ovalis (R. Brown) Hook m. int + m. int + Ms(p)
Syringodium isoetifolium (Ascherson) Dandy – + washed +
Note: Zones: int, intertidal; up. int, upper intertidal; m. int, middle intertidal; l. int, low intertidal; sub, subtidal; inf. lit, infralittoral;
sup. lit, supralittoral; int. pl, intertidal pools; washed, washed ashore. Communities: ep, epiphytic; enph, endophytic; enl, endolithic;
Ms(p), mosaic in polydominant community; M, monodominant; T, algal turf (algal community widespread in tropical waters, usu-
ally less than 3 cm high); f. sw, free-swimming; Mat, algal community growing as mat. Occurrence: –, not found; +++, more than
10 specimens per 1 cm2; ++, less than 10 specimens per 1 cm2; +, less than 1 specimen per 1 cm2; sgl, single.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
40 SERGEEVA et al.
may later lead to a reduction of the number of species
at the expense of non-competitive settlers. It is neces-
sary to conduct another survey of algae on the reef of
Sesoko Island after three or five years, in order to check
this assumption.
Presently, the projective cover of algae on the bot-
tom amounts to 40–85% in the intertidal zone and 50–
80% in the subtidal zone (compared with 50% in the
intertidal zone and no more than 10% in the subtidal
zone before the catastrophe in 1998). Similar catastro-
phes in other areas of the World Ocean were also fol-
lowed by an increase of the PC of the bottom: e.g., a
(‡) 75% rise in waters of the western Sumatra [2] and a
90% rise on the reefs of Mayotte Island, in the south-
western Indian Ocean [16]. The increase in the projec-
tive algal cover of the bottom and the increase in spe-
cies diversity did not destroy a quantitative relationship
between species of the main taxonomic groups of
marine plants. Both before the catastrophe and after it,
the relationship between algae types on the Sesoko
Island was as follows (average records): 31% for green
algae, 46.1% for red algae, 10.7% for brown algae,
10.7% for blue-green algae, and 1.5% for other species.
No changes were noted in the relative number of spe-
(b) cies inhabiting different parts of the phytal: 60% were
found in the intertidal zone, 30% in the subtidal, and
Fig. 2. Reef flat of the fringing reef of Sesoko Is., opposite 10% in the supralittoral zone. The type of algal commu-
Sesoko beach locality in 1995 (a) and 2005 (b). nities did not change either: algal turf mats and mosaic
algal communities including large–thallus plants Turbi-
naria ornata, Sargassum spp., Codium spp., and Ulva
zone and 20–50% in the intertidal zone before the spp. remained the most widespread on the reef of
catastrophe and markedly increased after the catastro- Sesoko Island, as it was before.
phe to reach up to 40–85% in the intertidal zone and up
to 71% in the subtidal zone. The biomass of mass algal Thus, it was established that bleaching and mass
species inhabiting the lower intertidal zone in 2005was mortality of corals at the fringing reef of Sesoko Island
as high as 310.8 g/m2 for Ulva, 246.8 g/m2 for Digenea was followed by a “phase shift”, and, as a result, marine
simplex, and 85.32 g/m2 for Codium sp. plants occupied practically the entire area of a newly-
formed substrate (the surface of dead coral colonies and
their fragments that covered the bottom), the number of
DISCUSSION algal species and their total biomass distinctly
increased. If the documented trend lasts for a longer
The fringing reef of Sesoko Island was character-
time (a few decades) and surviving coral colonies and
ized by a relatively high species diversity of marine
planulae settling on the substrate loose the competition
plants: 211 species were found during the period from
with algae for the substrate, the coral reef of Sesoko
1995 to 1998. For comparison, coral reefs in the south-
Island, overgrown with algae and unable to build hard
ern Pacific are inhabited by about 360 algal and sea-
substrate (i.e. its own base) is likely to be destroyed.
grass species [9]. After the mass coral mortality and
However, studies on competitive relationships between
algal colonization of the newly formed substrate (dead
corals and algae on the damaged reef of Sesoko Island
corals), the number of marine plants at the reef of
[19, 20] showed that, in most cases, corals win the
Sesoko Island increased by 134 species. Further, the
struggle between coral polyps and algal communities.
number of dominant algal species increased. Before the
Thus, for example, in artificial injuries inflicted on mas-
catastrophe, a major portion of the bottom was occu-
sive and branched corals, polyps overgrew more than
pied by Gelidiella acerosa, Digenea simplex and Jania
100 algal species. Only toxic cyanobacteria of the
spp.; after the catastrophe Ulva, Codium, Galaxaura
genus Lyngbya were an insuperable hindrance to coral
and other species were added. We assume that the
growth.
appearance of algal species new to the reef of Sesoko
Island resulted from the absence of competition for In 2005, we found young colonies of massive and
substrate and other resources with both competitive branched corals in the intertidal and subtidal zones of
algal species typical for the area and, probably, corals. Sesoko Island, this observation indicates a recovery of
Very likely, the competition for substrate and resources the reef not only through regeneration of old injured
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 41
Table 2. Projective cover (PC) of hard substrate with macroalgae before and after the nature catastrophe on the Ryukyus
PC of algae on hard Zones and depths
Locality Reference
substrate in % of algae growths
1997
Opposite Sesoko Biological From 1 to 20 No data Nonaka, 2004
Station
Before 1998
Western part of Sesoko Island ~5 Sublittoral, 2 m Titlyanov (unpublished data)
Opposite Sesoko Biological <30 No data Loya et al., 2001
Station ~50 Intertidal zone Titlyanov (unpublished data)
~10 Sublittoral, 2 m Ditto
North of Daito Is. <1 No data Nonaka, 2004
Miyako Islands From 2 to 20, grasses and No data Kajiwara, Matsumoto, 2004
algae
After 1998
Opposite Sesoko Biological <85 No data Sakai, 2004
Station <85 No data Loya et al., 2001
Akajima <65 No data Iwao, 2004
Minnajima and Iejima <75 No data Sakai, 2004
Western coasts of Okinawa Is. <95 No data Sakai (unpublished data)
2005
Opposite Sesoko Biological 40.22 ± 29.7 Upper intertidal zone Our data
Station 78.99 ± 11.67 Middle intertidal zone "
62.06 ± 6.6 Lower intertidal zone "
71.63 ± 8.43 Sublittoral zone 1.5 m "
Western Sesoko Is. 38.40 ± 14.8 Infralittoral zone "
33.41 ± 2.03 Middle intertidal zone "
49.21 ± 10.4 Lower intertidal zone "
corals, but also as a result of the settlement of new col- REFERENCES
onies [see also 17]. Evidently, the “phase shift” on the 1. Sorokin, Yu.I., Ekosistemy korallovykh rifov (Ecosys-
reef of Sesoko Island is a temporary event, and the coral tems of Coral Reefs), 3/4.: Nauka, 1990.
reef is able to recover in its original or modified state, 2. Abrar, M. and Efendy, Y., Coral Recovery After Bleach-
unless a catastrophe occurs again. ing in 1998 at West Sumatra Waters, Indonesia,
Abstracts. 10th Int. Coral Reef Symp., 2004.
3. Brown, B.E., Coral Bleaching: Causes and Conse-
ACKNOWLEDGEMENTS quences, Coral Reefs, 1997, vol. 16, pp. 129–138.
4. Diaz-Pulido, G. and McCook, L.J., The Fate of Bleached
We thank Prof. Moshin Morita, the President of the Corals: Patterns and Dynamics of Algal Recruitment,
University of the Ryukyus and Prof. Minoru Murai, the Mar. Ecol. Progr. Ser., 2002, vol. 232, pp. 115–128.
Scientific Leader of the Sesoko Marine Biological Sta- 5. Hasegawa, H. and Yamano, H., Ishigaki Island, Coral
tion for their kind invitation to work at the Sesoko Sta- Reefs of Japan. Ministry of the Environment; Jap. Coral
Reef Soc., 2004, pp. 212–218.
tion. We thank also the staff of the Sesoko Station of the
6. Hughes, T.P., Catastrophes, Phase Shifts, and Large-
Tropical Biosphere Research Center for their valuable Scale Degradation of Caribbean Coral Reefs, Science,
help and technical assistance. 1994, vol. 265, pp. 1547–1551.
This study was supported by the Russian Founda- 7. Iwao, K., Kerama Islands, Coral Reefs of Japan. Minis-
try of the Environment; Jap. Coral Reef Soc., 2004,
tion for Basic Research (Project 05-04-49901 “Com- pp. 185–189.
petitive Relations among Plant and Animal Organisms 8. Kajiwara, K. and Matsumoto, H., Miyako Archipelago,
in Mono- and Polydominant Communities of Sea- Coral Reefs of Japan. Ministry of the Environment; Jap.
weeds”). Coral Reef Soc., 2004, pp. 204–208.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
42 SERGEEVA et al.
9. Littler, D.S. and Littler, M.M., South Pacific Reef Plants, 16. Pichon, M., Seguin, F., Hernandez, S. et al., Status of the
Offshore Graphics, Inc., 2003. Coral Reefs of Mayotte Islands (SW Indian Ocean) Five
10. Loya, Y., Sakai, K., Yamazato, K. et al., Coral Bleaching: Years After the 1998 Bleaching Events, Abstracts. 10th
the Winners and the Losers, Ecol. Lett., 2001, vol. 4, Int. Coral Reef Symp, 2004.
pp. 122–131. 17. Sakai, K., Okinawa Island, Coral Reefs of Japan. Minis-
11. McClanahan, T.R., Muthiga, N.A., and Mangi, S., Coral try of the Environment; Jap. Coral Reef Soc., 2004,
and Algal Changes After the 1998 Coral Bleaching: pp. 182–184.
Interaction with Reef Management and Herbivores on
Kenyan Reefs, Coral Reefs, 2001, vol. 19, no. 4, 18. Sakai, K., Muko, S., Nishikawa, A. et al., Coral Recruit-
pp. 380–399. ment and Recovery of Coral Communities After 1998
12. McCook, L.J., Competition Between Corals and Algal Mass Coral Bleaching Around Okinawa Island,
Turfs Along a Gradient of Terrestrial Influence in the Abstracts, 10th Int. Coral Reef Symp., 2004, p. 135.
Nearshore Central Great Barrier Reef, Coral Reefs, 19. Titlyanov, E.A., Titlyanova, T.V., and Yakovleva, I.M.,
2001, vol. 19, pp. 419–425. Competitive Relationships Between Algae and Coral
13. McCook, L.J., Jompa, J., and Diaz-Pulido, G., Competi- Polyps Communities Under Direct and Indirect Contacts
tion Between Corals and Algae on Coral Reefs: a Review on Damaged Corals, Abstracts, 10th Int. Coral Reef
of Evidence and Mechanisms, Coral Reefs, 2001, Symp., 2004, p.135.
vol. 19, pp. 400–417.
14. Nakano, Y. and Nakamura, S., Annual Record of Coastal 20. Titlyanov, E.A., Titlyanova, T.V., Yakovleva, I.M. et al.,
Observation at Sesoko Marine Science Center in 1991, Regeneration of Artificial Injuries on Scleractinian Corals
Galaxea, 1993, vol. 11, pp. 173–181. and Coral/Algal Competition for Newly Formed Sub-
strate, J. Exp. Mar. Biol. Ecol., 2005, vol. 323, pp. 27–42.
15. Nonaka, M., Daito Islands, Coral Reefs of Japan. Minis-
try of the Environment; Jap. Coral Reef Soc., 2004, 21. Veron, J.E.N., Corals of Australia and the Indo-Pacific,
pp. 199–201. Angus and Robertson Publishers, 1986.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
Original Russian Text © O.S. Sergeeva, T.V. Titlyanova, E.A. Titlyanov, 2007, published in Biologiya Morya.
ECOLOGY
Species Composition and Distribution of Algae
on the Fringing Coral Reef of Sesoko Island
(Ryukyu Archipelago) before and after
the Natural Catastrophe of 1998
O. S. Sergeevaa, c, T. V. Titlyanovab, c, and E. A. Titlyanovb, c
a Pacific Institute of Bioorganic Chemistry, Far East Division, Vladivostok 690022
bA.V. Zhirmunsky Institute of Marine Biology, Far East Division, Vladivostok 690041
cSesoko Station of the Tropical Biosphere Research Center, Okinawa 905–0227, Japan
e-mail: etitlyanov@mail.ru
Received September 21, 2006
Abstract—The species composition and distribution of marine plants on the fringing reef of Secoko Island
were studied before and after the mass coral mortality in 1998. The study showed that changes in the bottom
communities that occurred after bleaching of corals were caused by the presumed development of marine plants
substituting reef-building corals on the bottom. The number of algal species grew from 211 to 345. The projec-
tive cover (PC) of hard substrate with macroalgae increased: in 1998, it was 1–10% in the subtidal zone and
20–50% in the intertidal zone, while in 2002 through 2005, the PC reached 71% in the subtidal and 40–85% in
the intertidal zone. It is assumed that the phase of the “plant reef” on Sesoko Island is a temporary event, and
that the coral reef can recover within several decades, unless a natural catastrophe occurs again.
DOI: 10.1134/S1063074007010038
Key words: macroalgae, coral reef, bleaching, “phase shift,” competition.
The ecosystem of a coral reef is based on the vital of water temperature by 1–2°C in July–August caused
activity of hermatypic reef–building corals that produce extensive coral mortality even in the subtropical zone:
a hard carbonate substrate for the settling of benthic up to 80% of the total coral population died on Okinawa
organisms. On healthy reefs, corals usually occupy up Island [10].
to 80–90% of the bottom area; they are the main pri- Diaz-Pulido and McCook [4] show that immedi-
mary producers of organic matter at the expense of the ately after coral bleaching and mortality dead coral col-
photosynthesis of their intracellular symbionts, namely onies were colonized with marine algae and this colo-
dinoflagellate algae. Other primary producers of nization resulted in a shift from corals to algae. This
organic matter are benthic and planktonic marine “phase shift” after the mass mortality of corals was
plants; macrophytes among them yield the highest pro- observed on the Great Barrier Reef [4] and on Carib-
duction. On a healthy coral reef, macrophytes cover bean coral reefs [6]. Some authors believe that the
from 1 to 20% of the hard substrate of the bottom [8]. phase shift leads to the disappearance of reefs, as the
The algae of coral reefs present a diverse species com- algae destroy (rather than build, as corals do) the car-
position; they successfully compete with corals for sub- bonate substrate, the base of the reef. The “phase shift”
strate, space and other life resources [13]. could be a temporary event in an active reparative pro-
The total area of contemporary coral reefs amounts cesses, when corals settle on the substrate and old col-
to about 600 thousand sq. km [1]. In the last decades, a onies recover [13, 20].
catastrophic destruction of shallow–water coral reefs There is no way to predict the future fate of a coral
took place and, consequently, their productivity and reef without research into the contemporary structure
biological diversity were reduced [3]. The coral mortal- of the reef and its species composition, i.e., the number
ity and reef destruction characteristic of the entire trop- and distribution of organisms competing for substrate,
ical zone of the World Ocean depend mostly on water among them corals and benthic macro- and microalgae,
temperature increases that cause coral bleaching and as well as some invertebrate animals destroying the
expulsion of symbiotic algal cells from coral tissues substrate. It is no less important to study competitive
(often together with the host animal cells) [3]. abilities of reef-building corals and mass algal species
The most destructive consequences were recorded [4, 12].
in 1998 after events of elevated surface seawater tem- Notwithstanding the urgency of these studies, only a
perature in many areas of the World Ocean [11]. A rise few works deal with the study of the biological struc-
30
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 31
ture of coral reefs after catastrophes [5, 7, 8, 10, 11, 17]; Okinawa Is
these studies mostly describe changes in the species Sesoko Is
composition and projective cover of the bottom with
corals. A few works concern development of algae on
damaged coral reefs [4, 11]. During the period from
1995 to 2005, the species composition and distribution Naha
of algae were studied at the fringing reef of Sesoko
Sesoko Beach
Island. After the catastrophe in 1998, about 75 to 80%
of the corals died in shallow waters around the island
[10]. This study is aimed at a comparison of the compo- Sesoko Is
sition and distribution of algal species on the fringing
reef of Sesoko Island before and after the natural catas-
trophe in 1998.
Biostation
“Sesoko”
MATERIAL AND METHODS
The investigations were conducted at the fringing
reefs of the south-eastern shore (opposite the Biologi- Fig. 1. Schematic map of Sesoko Is.
cal Station of the University of Ryukyus) and the west-
ern shore (Sesoko Beach) of Sesoko Island, lying near
Okinawa (Japan) in the East- Chinese Sea (26°38′N, RESULTS
127°52′E) (Fig. 1). Algae were collected, herbarized
and identified from May to October in 1995, October to From 1995 until the natural catastrophe of 1998, our
December of 1997, January to April of 1998, March to studies revealed 211 species of marine plants, of them
December of 2002, January to March of 2003, July 78 green algae (36.9%), 23 brown algae (10.9%),
2004, and February to May of 2005. The coral reef near 96 red algae (45.5%), 9 blue-green algae (4.3%), 1 yel-
Sesoko Island, according to the classification of Veron low-green alga (0.5%), and 4 species of sea grasses
[21], is assigned to the fringing reef type. The coast is (1.9%). In the years 2002 through 2005, the list com-
formed by a fossil coral reef. The reef platform is 10 to prised 345 species (Table 1). It is interesting, that quan-
20 m broad; the lagoon is shallow, 1 to 3 m wide. Water titative relationship of species did not change signifi-
depth at the reef flat is about 1 m at a high tide. The reef cantly: we documented 99 species of green algae
slope is quite steep, stretches down to a depth of 30 m (30.1%), 36 brown algae (11%), 152 red algae (46.2%),
and passes into a sandy bottom. The surface water tem- 37 blue-green algae (11.2%), 1 yellow-green alga
peratures in the sea is, on the average, approximately (0.3%), and 4 species of seagrasses (1.2%). Both
+29°C (with 31°C as the maximum) in the summer and before and after the dramatic coral mortality (Fig. 2),
21°C in the winter (with 18°C as the minimum). Water the highest relative number of marine plant species was
salinity varies from 34.5 to 35.2‰, depending on the found in the intertidal collections (60%), a lower num-
season [14]. ber was collected in the subtidal zone (30%), and only
10% were recorded for the supralittoral zone. The por-
The object of study was algae collected by scuba- tion of epiphytic species also did not change, it made up
diving in the intertidal and subtidal zones at the fringing about 15% of the total number of species. About 50%
reef of Sesoko Island. of all algae collected during the years inhabited an algal
Marine plants were identified with the use of Olym- turf community, as they did before the catastrophe.
pus stereo and light microscopes and photographed Ulva spp., Gelidiella acerosa, Jania spp., Centro-
with a Olympus Camedia 5050C digital camera. The ceras clavulatum, Bostrychia tenella, and Digenea sim-
projective algal cover of the bottom in the supralittoral, plex dominated on the healthy coral reef. As well,
intertidal and subtidal zones was determined by the Enteromorpha spp., Codium spp., Ulva fasciata,
generally accepted hydrobiological method with the Boodlea composita, Bornetella sphaerica, Actinotri-
use of a 50x50 cm frame, in triplicate for each zone. chia fragilis, Tricleocarpa spp., Ganonema farinosum,
Algae in the frame were photographed, collected, and and Liagora ceranoides became new dominants after
identified in the laboratory, the number of specimens coral mortality. At the same time, Cladophora cate-
within the frame was counted for every species, and the nata, Boodlea coacta, Ceratodictyon intricatum and
mass of the algal species was weighed. some other species were no longer found on the dam-
aged reef.
Color prints of the algae in the frame were made on
a high-quality paper with the use of an Epson The projective cover (PC) of microalgae on the hard
KA450PM printer, cut and weighed. The “weight” substrate changed significantly after the catastrophe
method of was applied to calculate the projective cover (Table 2). The PC of algae on Sesoko and some other
area of algae on the bottom [20]. islands of the Ryukyus made up 1–10% in the subtidal
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
32 SERGEEVA et al.
Table 1. Algae collected on the fringing reef of Sesoko Island: before a natural catastrophe (1995–1998) and after the event
(2002–2005)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
CHLOROPHYTA
Micrasterias sp. – – – + –
Phaeophila dendroides (P. Crouan & H. Crouan) – – – + enl
Batters
Monostroma nitidum Wittrock up. int +++ int, up. int +++ M
Enteromorpha clathrata (Roth) Greville m. int ++ int +++ T, ep
E. compressa (Linnaeus) Nees int + int +++ T
E. flexuosa (Wulfen) J. Agardh – – int, l. int + T
E. kylinii Bliding – – int + T
E. prolifera (O.F. Muller) J. Agardh int + int + T
E. ralfsii Harvey – – int + T
Ulva conglobata Kjellman int +++ int +++ Ms(p)
U. fasciata Delile int, l. int – int, l. int +++ M
U. lactuca Linnaeus int – int ++ Ms(p)
U. pertusa Kjellman int, up. int +++ int, up. int +++ M
U. reticulata Forsskål l. int + washed + Ms(p)
Pringsheimiella scutata (Reinke) Marchewianka – – l. int + ep
Ulvella lens (P. Crouan & H. Crouan) sub + up. int + ep
Verdigellas sp. – – washed + –
Anadyomene wrightii Harvey ex J. Gray l. int ++ int, l. int ++ T
Acrochaete viridis (Reinke) Nielsen l. int + l. int + ep
(=Entocladia viridis Reinke)
Acrochaete sp. – – l. int + ep
Ectochaete leptochaete (Huber) Wille – – – + enph
Gomontia arrhiza Hariot l. int + l. int + ep
Microdictyon nigrescens (Yamada) Setchell inf. lit + inf. lit + T
M. okamurai Setchell inf. lit + inf. lit + T
M. japonicum Setchell int + int + T
Chaetomorpha basiretrorsa Setchell up. int + up. int + T
C. capillaris (Kützing) Børgesen l. int + l. int + T
C. linum (O.F. Müller) Kützing inf. lit + inf. lit + Ms(p)
C. pachynema Montagne – – l. int + Ms(p)
C. javanica Kützing – – l. int + T
Cladophora catenata (Linnaeus) Kützing l. int + – – T
C. fuscicularis (Martens ex C. Agardh) Kützing – – l. int + T
C. fuliginosa Kützing – – l. int + T
C. laetevirens (Dillwyn) Kützing l. int + l. int + T
C. vagabunda (Linnaeus) van den Hoek int + int ++ T
Rhizoclonium grande Børgesen int + int ++ T
R. implexum (Dillwyn) Kützing inf. lit + inf. lit ++ T, ep
Boodlea coacta (Dickie) G. Murray & De Toni int + – – T, f. sw
B. composita (Harvey) Brand int + int ++ T, f. sw
B. struveoides Howe – – int + T, f. sw
Struvea anastomosans (Harvey) int + int + T
Piccone & Grunow ex Piccone
Cladophoropsis herpestica (Montagne) Howe – – int + T
C. membranacea (Hofman Bang ex C. Agardh) – – int + T
Børgesen
C. sundanensis Reinbold int + int ++ T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 33
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
C. zollingeri (Kützing) Reinbold int + int ++ Mat
Cladophoropsis sp. int + int + T
Dictyosphaeria cavernosa (Forsskål) Børgesen int ++ int +++ Ms(p)
D. versluysii Weber-van Bosse int + int + Ms(p)
Siphonocladus rigidus Howe l. int + l. int + ep
Ventricaria ventricosa (J. Agardh) Olsen & J. West l. int ++ l. int + Ms(p)
Valonia aegagropila C. Agardh l. int ++ l. int + Mat
V. fastigiata Harvey ex J. Agardh l. int + l. int + Mat
V. macrophysa Kützing l. int + l. int + Ms(p)
V. utricularis (Roth) C. Agardh l. int + l. int + Ms(p)
Bryopsis harveyana J. Agardh l. int, inf. lit + l. int, inf. lit + T
B. indica A. Gepp & E. Gepp l. int, inf. lit + l. int, inf. lit + T, ep
B. pennata Lamouroux l. int + l. int + T
B. plumosa (Hudson) C. Agardh l. int, inf. lit + l. int, inf. lit + T
B. ryukyuensis Yamada – – l. int, inf. lit + T
Derbesia attenuata Dawson – – sub + T
D. fastigiata Taylor – – inf. lit + T
D. marina (Lyngbye) Solier inf. lit + inf. lit + T
Codium adhaerens (Cabrera) C. Agardh int, inf. lit ++ int, l. int ++ Ms(p)
C. intricatum Okamura l. int, inf. lit ++ l. int, inf. lit +++ Ms(p)
C. repens P. Crouan & H. Crouan l. int, inf. lit + l. int, inf. lit ++ Ms(p)
Caulerpa cupressoides (Vahl) C. Agardh l. int + l. int + T
C. fastigiata Montagne int + int + T
C. lentillifera J. Agardh – – int + T
C. macrophysa (Sonder ex Kützing) G. Murray int + int + T
C. microphysa (Weber-van Bosse) Feldmann l. int + l. int + T
C. nummularia Harvey ex J. Agardh int + int ++ T
C. racemosa (Forsskål) J. Agardh int + int + T
C. racemosa (Forsskål) Weber-van Bosse var. int + – – T
clavigera (Turn.) Weber-van Bosse
C. racemosa var. corynephora (Montagne) – – int + T
Weber-van Bosse
C. racemosa (Forsskål) J. Agardh var. int, inf. lit + int, l. int + T
peltata (Lamouroux) Eubank in Stephenson
C. serrulata (Forsskal) J. Agardh int, inf. lit + int, inf. lit + T
C. serrulata var. serrulata f. lata (Weber-van Bosse) int, inf. lit + int, inf. lit + T
Tseng
C. serrulata J. Agardh var. serrulata f. spiralis int, inf. lit ++ int, inf. lit ++ T
(Weber-van Bosse) Gilbert
C. sertularioides (S. Gmelin) Howe l. int, inf. lit + l. int ++ T
C. vickersiae Børgesen – – int + T
C. webbiana Montagne f. tomentella (Harvey) int + – – T
Weber-van Bosse
Caulerpella ambigua (Okamura) Prud'homme van l. int + l. int + T
Reine & Lokhorst
Ostreobium quekettii Bornet & Flahault – + – ++ enl
Penicillus sibogae Gepp – – – + ep
Avrainvillea erecta (Berkeley) A. Gepp & E. Gepp m. int + m. int + Ms(p)
Boodleopsis pusilla (Collins) W.R. Taylor, Joly & inf. lit + inf. lit + Ms(p)
Bernatowicz
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
34 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Chlorodesmis fastigiata (C. Agardh) Ducker int, m. int + int, m. int + Ms(p)
Pseudochlorodesmis furcellata (Zanardini) Borgesen – – l. int + Ms(p)
Halimeda discoidea Decaisne inf. lit + inf. lit + Ms(p)
H. macroloba Decaisne – – int + Ms(p)
H. macrophysa Askenasy – – inf. lit ++ Ms(p)
H. opuntia (Linnaeus) Lamouroux int, inf. lit + int, inf. lit Ms(p)
H. tuna (Ellis & Solander) Lamouroux l. int, inf. lit + l. int, inf. lit ++ Ms(p)
Tydemania expeditionis Weber-van Bosse inf. lit + – – Ms(p)
Rhipidosiphon javensis (Montagne) Gepp int, inf. lit +++ int, inf. lit +++ T
Cymopolia van-bosseae Solms-Laubach inf. lit sgl – – Ms(p)
Dasycladus vermicularis (Scopoli) Krasser l. int sgl – – Ms(p)
Bornetella nitida Sonder int, inf. lit + int, inf. lit + Ms(p)
B. oligospora Solms-Laubach int, inf. lit + int, inf. lit + Ms(p)
B. sphaerica (Zanardini) Solms-Laubach int, inf. lit ++ int, inf. lit +++ Ms(p)
Neomeris annulata Dickie l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
N. bilimbata Koster – – l. int, inf. lit + Ms(p)
Acetabularia clavata Yamada inf. lit + inf. lit + Ms(p)
A. dentata Solms- Laubach int, inf. lit ++ int, inf. lit +++ Ms(p)
A. exigua Solms-Laubach inf. lit ++ inf. lit ++ Ms(p)
A. parvula Solms- Laubach l. int, inf. lit + l. int, inf. lit ++ Ms(p)
A. pusilla (Howe) Collins inf. lit – inf. lit + Ms(p)
PHAEOPHYTA
Ectocarpus elachistaeformis Heydrich – – l. int + ep
E. siliculosus (Dillwyn) Lyngbye – – l. int + ep
Ectocarpus sp. – – l. int + ep
Feldmannia irregularis (Kützing) G. Hamel – – l. int, inf. lit ++ ep
Hincksia indica (Sonder) Papenfuss et Chihara l. int, inf. lit + l. int, inf. lit + ep
H. mitchelliae (Harvey) P. Silva l. int, inf. lit + l. int, inf. lit +++ T, ep
Pilayella littoralis (Linnaeus) Kjellman – – int + ep
Ralfsia expansa (J. Agardh) J. Agardh int + int ++ Ms(p)
Chilionema ocellata (Kützing) Kuckkuck – – l. int, inf. lit ++ ep
Chnoospora implexa J. Agardh inf. lit ++ inf. lit ++ Ms(p)
Colpomenia sinuosa (Mertens ex Roth) Derbes & l. int ++ l. int ++ Ms(p)
Solier
Hydroclathrus clathratus (C. Agardh) Howe inf. lit + inf. lit + Ms(p)
Sphacelaria novae-hollandiae Sonder l. int + l. int ++ T, ep
S. rigidula Kützing l. int ++ l. int ++ T, ep
S. tribuloides Meneghini l. int ++ l. int ++ T, ep
Dictyota dichotoma (Hudson) Lamouroux l. int + l. int + Ms(p)
D. friabilis Setchell – – l. int + T
D. humifusa Hörnig, Schnetter & Coppejans – – l. int ++ Ms(p)
D. linearis (C. Agardh) Greville l. int + l. int + T
D. patens J. Agardh l. int + l. int + T
Dictyota sp. – – int + T
Dictyopteris undulata Holmes – – up. int ++ T
Dictyopteris sp. – – up. int ++ T
Lobophora variegata (Lamouroux) Womersley ex l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Oliveira
Dictyerpa stage of Padina [Vaughaniella stage] int + int + T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 35
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Padina australis Hauck int. pl + int. pl + Ms(p)
P. boryana Thivy int. pl ++ int. pl ++ M
P. gymnospora (Kützing) Sonder int, int. pl + – – Ms(p)
P. minor Yamada int, inf. lit + int, inf. lit + Ms(p)
Cladosiphon okamuranus Tokida m. int + m. int + Ms(p)
Hormophysa cuneiformis (J. Gmelin) P. Silva inf. lit + inf. lit + Ms(p)
Sargassum crassifolium J. Agardh inf. lit + inf. lit ++ Ms(p)
S. cristaefolium (=duplicatum) C. Agardh – – int. pl ++ Ms(p)
S. feldmannii Pham Hoang Ho – – inf. lit ++ Ms(p)
S. polycystum C. Agardh – – inf. lit + Ms(p)
S. thunbergii (Mertens) C. Kuntze int, int. pl ++ int, int. pl ++ Ms(p)
Turbinaria ornata (Turner) J. Agardh l. int, inf. lit ++ l. int, inf. lit +++ Ms(p)
RHODOPHYTA
Stylonema alsidii (Zanardini) K. Drew l. int, inf. lit + l. int, inf. lit + ep
Chroodactylon ornatum (C. Agardh) Basson – + – + ep
Erytrotrichia carnea (Dillwyn) J. Agardh l. int, inf. lit + l. int, inf. lit + ep
Erythropeltis subintegra (Rosenvinge) – – l. int, inf. lit ++ ep
Kornmann et Sahling
Porphyra crispata Kjellman – – sub + Ms(p)
Acrochaetium catenulatum Howe – – l. int + ep
A. crassipes (Børgesen) Børgesen – – l. int + ep
A. gracile Børgesen – – l. int + ep
A. moniliforme (Rosenvinge) Børgessen l. int + l. int + ep
A. occidentale Børgessen – – l. int + ep
A. seriatum Børgesen – – l. int + ep
A. subseriatum Børgessen – – l. int + ep
A. virgatulum (Harvey) Bornet – – l. int + ep
Acrochaetium sp. l. int + l. int + ep
Rhodochorton sp. int + – – ep
Liagora ceranoides Lamouroux – – l. int, inf. lit ++ Ms(p)
Liagora sp. l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Ganonema farinosum (Lamouroux) Fan & Wang l. int, inf. lit + l. int, inf. lit + Ms(p)
Trichogloeopsis pedicellata (Howe) Abbott & Doty – – l. int, inf. lit sgl Ms(p)
Yamadaella caenomyce (Decaisne) Abbott inf. lit + inf. lit + Ms(p)
Trichogloea requienii (Montagne) Kützing inf. lit + inf. lit + Ms(p)
Actinotrichia fragilis (Forsskål) Børgesen inf. lit ++ inf. lit ++ Ms(p)
Galaxaura fasciculata Kjellman inf. lit + inf. lit ++ Ms(p)
G. marginata (Ellis et Solander) Lamouroux – – int ++ Ms(p)
G. obtusata (J. Ellis & Slander) J.V. Lamouroux – – inf. lit + Ms(p)
G. subfruticulosa Chou inf. lit + inf. lit ++ Ms(p)
Tricleocarpa fragilis (Linnaeus) Huisman & inf. lit + inf. lit ++ Ms(p)
Townsend (=Galaxaura oblongata)
T. cylindrica (Ellis et Solander) Huisman & inf. lit + inf. lit ++ Ms(p)
Borowitzka (=Galaxaura fastigiata)
Gelidiella acerosa (Forsskål) Feldmann et Hamel int ++ int ++ T
G. adnata Dawson int + int + T
G. pannosa (J. Feldmann) J. Feldmann & G. Hamel – – int + T
Gelidiella sp. int + int + T
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
36 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Pterocladiella capillacea (Gmelin) Santelices & – – l. int + T
Hommersand
Gelidium pusillum (Stackhouse) Le Jolis int + int, up. int ++ T
G. divaricatum Martens int + int + T
Wurdemannia miniata (Sprengle) Feldmann & int, up. int + int, up. int ++ T
Hamel
Peyssonnelia conchicola Piccone & Grunow – – l. int, inf. lit + Ms(p)
in Piccone
P. inamoena Pilger – – l. int, inf. lit + Ms(p)
Jania adhaerens Lamouroux int, inf. lit +++ int, inf. lit +++ T, ep
J. capillacea (Yendo) Yendo int, inf. lit +++ int, inf. lit +++ T, ep
J. ungulata f. brevior (Yendo) Yendo int, inf. lit ++ int, inf. lit ++ T, ep
Amphiroa fragilissima (Linnaeus) J.V. Lamouroux l. int + l. int ++ Ms(p)
Hydrolithon farinosum (J.V. Lamouroux) Penrose & int + int ++ ep
Y.M. Chamberlain
Porolithon sp. sub – sub + Ms(p)
Pneophyllum conicum (E.Y. Dawson) Keats, – – int, inf. lit + Ms(p)
Y.M. Chamberlain & Baba
P. fragile Kützing int, inf. lit + int, inf. lit + ep
Mastophora rosea (C. Agardh) Setchell – – int, inf. lit ++ M
Titanophora pulchra Dawson – – washed sgl –
Gelidiopsis intricata (C. Agardh) Vickers inf. lit ++ inf. lit ++ T
G. scoparia (Montagne & Millardet) De Toni – – inf. lit + T
G. variabilis (J. Agardh) Schmitz l. int, inf. lit + l. int, inf. lit + T
Lomentaria corallicola Børgesen int + int + T
L. mauritiana Børgesen int + int + T
Chryzymenia okamurai Yamada et Segawa – + washed + –
Coelarthrum boergesenii Weber-van Bosse l. int, inf. lit + l. int, inf. lit + Ms(p)
(=C. coactum Okamura)
Botryocladia skottsbergii (Børgesen) Levring int + – – T
Coelothrix irregularis Børgesen int, inf. lit + int, inf. lit ++
Eucheuma denticulatum (Burman) Collins et Harvey l. int sgl washed sgl –
Gracilaria arcuata Zanardini int + int + Ms(p)
G. blodgettii Harvey – – int + Ms(p)
G. coronopifolia J. Agardh – – int + Ms(p)
G. salicornia (C. Agardh) Dawson int + int + Ms(p)
Ceratodictyon intricatum (C. Agardh) R.E. Norris int + – – Ms(p)
C. spongiosum Zanardini l. int, inf. lit ++ l. int, inf. lit ++ Ms(p)
Caulacantus ustulatus (Mertens ex Turner) Kützing int + int ++ T
Hypnea cervicornis J. Agardh – – int + T, ep
H. charoides Lamouroux l. int + l. int + T
H. boergesenii Tanaka – – l. int + T
H. esperi Grunov int + int + T, ep
H. nidulans Setchell int + – – T
H. pannosa J. Agardh l. int, inf. lit + l. int, inf. lit ++ T
H. spinella (C. Agardh) Kützing int, inf. lit + int, inf. lit ++ T, ep
H. valentiae (Turner) Montagne l. int, inf. lit + l. int, inf. lit + T
Ahnfeltiopsis flabelliformis Harvey – – – + Ms(p)
Cruoriella sp. – – l. int sgl Ms(p)
Erythrodermis sp. – – l. int + Ms(p)
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 37
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Haematocelis sp. – – l. int sgl Ms(p)
Plocamium telfairiae (W. Hooker & Harvey) – – l. int, inf. lit + Ms(p)
Harvey ex Kützing
Chondracanthus intermedius (Suringar) Hommersand int + int + T
Rhodymenia coacta Okamura int + – – Ms(p)
R. anastomosans Weber-van Bosse – – int. pl + Ms(p)
Rhodymenia sp. – – int + Ms(p)
Rhodopeltis borealis Yamada – – inf. lit + Ms(p)
Portieria hornemanni (Lyngbye) P. Silva – – inf. lit + Ms(p)
Champia parvula (C. Agardh) Harvey int + int ++ T, ep
C. japonica Okamura int + int + T, ep
C. vieillardii Kützing – – l. int + T, ep
Asparogopsis taxiformis (Delile) Trevisan inf. lit + inf. lit + Ms(p)
Falkenbergia hillebrandii (Bornet) Falkenberg l. int, inf. lit + l. int, inf. lit ++ ep
(=sporophyte of A. taxiformis)
Dudresnaya japonica Okamura – – washed + –
D. hawaiiensis R. K. S. Lee – – washed + –
Gymnothamnion elegans (Schousbold ex C. Agardh) int – int + ep
J. Agardh
Antithamnion lherminieri (P. Crouan & H. Crouan) l. int + l. int + ep
Bornet ex Nasr
Antithamnion sp. l. int + l. int + ep
Antithamnionella sp. – – l. int + ep
Anotrichium tenue (C. Agardh) Nägeli int + int ++ T, ep
Aglaothamnion callophyllidicola Yamada int + int + ep
Wrangelia argus (Montagne) Montagne int +++ int +++ T
W. dumontii (Dawson) Abbott – – int + T
W. penicillata (C. Agardh) C. Agardh – – int + T
Spyridia filamentosa (Wulfen) Harvey int, int. pl ++ int, int. pl +++ ep
Corallophila apiculata (Yamada) R. Norris l. int ++ l. int ++ ep
(=Centroceras apiculatum Yamada)
Centroceras clavulatum (C. Agardh) Montagne int +++ int +++ T, ep
C. inerme Kützing int + int + T, ep
Ceramium aduncum Nakamura – – int + T, ep
C. cingulatum Weber-van Bosse l. int + l. int + T, ep
C. codii (Richards) Mazoyer – – l. int + T, ep
C. fastigiatum Harvey – – l. int ++ T, ep
C. fimbriatum Setchell & Gardner l. int + l. int + T, ep
C. flaccidum (Kützing) Ardissone l. int ++ l. int ++ T, ep
C. howei Dawson l. int + l. int + T, ep
C. macilentum Dawson – – l. int + T, ep
C. paniculatum Okamura – – l. int + T, ep
C. procumbens Setchell & Gardner – – l. int + T, ep
C. sympodiale Dawson – – l. int + T, ep
Pleonosporium borrieri (Smith) Nägeli – – l. int + ep
Spermothamnion sp. l. int + l. int + ep
Crouania attenuata (C. Agardh) J. Agardh int ++ int ++ T, ep
Crouania sp. – – int + T, ep
Griffithsia metcalfii Tseng int ++ int ++ T, ep
G. subcylindrica Okamura int + int + T, ep
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
38 SERGEEVA et al.
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
G. japonica Okamura – – int + Ms(p)
G. weber-van-bosseae Børgesen – – int + T, ep
Haloplegma duperreyi Montagne – – washed + –
Dasya mollis Harvey int + int + Ms(p)
Dasya sp. – – int + Ms(p)
Heterosiphonia crispella (C. Agardh) Wynne l. int + l. int + T, ep
Hypoglossum sp. l. int + l. int + ep
Martensia pavonia (J. Agardh) J. Agardh – – washed sgl –
Taenioma perpusillum J. Agardh (J. Agardh) l. int + l. int ++ ep
Nitophyllum adhaerens Wynne – – – ++ T, ep
Polysiphonia ferulacea Suhr ex J. Agardh l. int + l. int + T, ep
P. japonica Harvey var. savatieri (Hariot) Yoon l. int + l. int + T, ep
Polysiphonia sp. up. int + up. int + T, ep
Bostrychia tenella (Lamouroux) J. Agardh up. int, +++ up. int, +++ M
sup. lit sup. lit
Herposiphonia parca Setchell int + int + ep
H. secunda (C. Agardh) Ambronn f. secunda int ++ int ++ ep
(C. Agardh) Wynne
H. secunda (C. Agardh) Ambronn f. tenella int ++ int ++ ep
(C. Agardh) Wynne
Lophosiphonia villum (J. Agardh) Setchell & Gardner l. int + l. int ++ T, ep
Tolypiocladia glomerulata (C. Agardh) Schmitz l. int ++ l. int ++ T, ep
Acanthophora muscoides (Linnaeus) – – int + T
Bory de Saint-Vincent
A. spicifera (Vahl) Børgesen int. pl ++ int. pl ++ T
Leveillea jungermannioides (Martens et Hering) int + int ++ T, ep
Harvey
Laurencia brongniartii J. Agardh l. int + l. int + T
L. cartilaginea Yamada – – l. int + T
L. implicata J. Agardh – – l. int + T
L. obtusa (Hudson) J.V. Lamouroux int + int ++ T
L. okamurae Yamada – – int +++ M
L. parvipapillata Tseng int + int + T
L. papillosa (C. Agardh) Greville int + int +++ M
L. perforata (Bory de Saint-Vincet) Monagne – – int + T
L. saitoi Perestenko l. int + – – T
L. yamadana Howe l. int + – – T
Chondria repens Børgesen l. int ++ l. int ++ T
C. dasyphylla (Woodward) C. Agardh int + int + T
C. minutula Weber-van Bosse – – int + T
Chondria sp. int + int + T
Digenea simplex (Wulfen) C. Agardh l. int, inf. lit +++ l. int, inf. lit +++ T
Acrocystis nana Zanardini int + int + T, ep
CYANOPHYTA
Dermocarpella clavata (Setchell & Gardner) – – – + ep
Pham Hoang Ho
Dermocarpa acervata (Setchell & Gardner) – – – + ep
Pham Hoang Ho
Aphanocapsa littoralis Hansgirg – – – ++ ep
Symploca hydnoides (Harvey) Kützing sup. lit + sup. lit + Ms(p)
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 39
Table 1. (Contd.)
Before catastrophe After catastrophe
List of species Community
zone occurrence zone occurrence
Lyngbya bouillonii Holffmann & Demoulin – – int + T
L. epiphytica Hieronymus int + int + ep
L. confervoides C. Agardh int + int + T
L. majuscula (Dillwyn) Harvey – – int ++ T
L. polychroa (Meneghini) Rabenhorst int + int + T
(=L. sordida Gomont)
L. semiplena (C. Agardh) J. Agardh – – int + T
Lyngbya sp. int + int + T
Oscillatoria limnetica Lemmermann – – int + T
O. margaritifera (Kützing) Gomont – – l. int + T
O. miniata (Zanardini) Gomont – – l. int + T
O. tenuis C. Agardh – – l. int + T
Oscillatoria sp. int + int + T
Phormidium corium (C. Agardh) Kützing – – l. int + T
P. crosbyanum Tilden – – l. int + T
P. tenue (Menighini) Gomont – – l. int ++ T
Phormidium sp. – – l. int + T
Spirulina major Kützing – – int sgl T
S. subsalsa Oersted int + int + T
S. subtilissima Kützing – – int + T
Spirulina sp. – – int + T
Calothrix confervicola (Dillwyn) C. Agardh – – int + ep
C. crustacea Thuret – – int + ep
C. parasitica (Chauvin) Thuret – – int + ep
C. scopulorum (Weber et Mohr) C. Agardh – – int + ep
Calothrix sp. 1 int + int ++ ep
Calothrix sp. 2 int + int ++ ep
Schizothrix sp. – – int + T
Nostoc commune Vaucher – – int + T
Hormothamnion sp. – – int + T
Rivularia bornetiana? – – int + T
Rivularia spp. – – int + T
Dichothrix sp. – – int ++ T
Brachytrichia quoyi (C. Agardh) Bornet & Flahault – – int + T
XANTHOPHYTA
Pseudodichotomosiphon constricta (Yamada) int + int + T
Yamada
ANTHOPHYTA
Thalassia hemprichii (Ehrenberg) Ascherson m. int + m. int + Ms(p)
Cymodocea serrulata (R. Brown) Ascherson et m. int + m. int + Ms(p)
Magnus
Halophila ovalis (R. Brown) Hook m. int + m. int + Ms(p)
Syringodium isoetifolium (Ascherson) Dandy – + washed +
Note: Zones: int, intertidal; up. int, upper intertidal; m. int, middle intertidal; l. int, low intertidal; sub, subtidal; inf. lit, infralittoral;
sup. lit, supralittoral; int. pl, intertidal pools; washed, washed ashore. Communities: ep, epiphytic; enph, endophytic; enl, endolithic;
Ms(p), mosaic in polydominant community; M, monodominant; T, algal turf (algal community widespread in tropical waters, usu-
ally less than 3 cm high); f. sw, free-swimming; Mat, algal community growing as mat. Occurrence: –, not found; +++, more than
10 specimens per 1 cm2; ++, less than 10 specimens per 1 cm2; +, less than 1 specimen per 1 cm2; sgl, single.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
40 SERGEEVA et al.
may later lead to a reduction of the number of species
at the expense of non-competitive settlers. It is neces-
sary to conduct another survey of algae on the reef of
Sesoko Island after three or five years, in order to check
this assumption.
Presently, the projective cover of algae on the bot-
tom amounts to 40–85% in the intertidal zone and 50–
80% in the subtidal zone (compared with 50% in the
intertidal zone and no more than 10% in the subtidal
zone before the catastrophe in 1998). Similar catastro-
phes in other areas of the World Ocean were also fol-
lowed by an increase of the PC of the bottom: e.g., a
(‡) 75% rise in waters of the western Sumatra [2] and a
90% rise on the reefs of Mayotte Island, in the south-
western Indian Ocean [16]. The increase in the projec-
tive algal cover of the bottom and the increase in spe-
cies diversity did not destroy a quantitative relationship
between species of the main taxonomic groups of
marine plants. Both before the catastrophe and after it,
the relationship between algae types on the Sesoko
Island was as follows (average records): 31% for green
algae, 46.1% for red algae, 10.7% for brown algae,
10.7% for blue-green algae, and 1.5% for other species.
No changes were noted in the relative number of spe-
(b) cies inhabiting different parts of the phytal: 60% were
found in the intertidal zone, 30% in the subtidal, and
Fig. 2. Reef flat of the fringing reef of Sesoko Is., opposite 10% in the supralittoral zone. The type of algal commu-
Sesoko beach locality in 1995 (a) and 2005 (b). nities did not change either: algal turf mats and mosaic
algal communities including large–thallus plants Turbi-
naria ornata, Sargassum spp., Codium spp., and Ulva
zone and 20–50% in the intertidal zone before the spp. remained the most widespread on the reef of
catastrophe and markedly increased after the catastro- Sesoko Island, as it was before.
phe to reach up to 40–85% in the intertidal zone and up
to 71% in the subtidal zone. The biomass of mass algal Thus, it was established that bleaching and mass
species inhabiting the lower intertidal zone in 2005was mortality of corals at the fringing reef of Sesoko Island
as high as 310.8 g/m2 for Ulva, 246.8 g/m2 for Digenea was followed by a “phase shift”, and, as a result, marine
simplex, and 85.32 g/m2 for Codium sp. plants occupied practically the entire area of a newly-
formed substrate (the surface of dead coral colonies and
their fragments that covered the bottom), the number of
DISCUSSION algal species and their total biomass distinctly
increased. If the documented trend lasts for a longer
The fringing reef of Sesoko Island was character-
time (a few decades) and surviving coral colonies and
ized by a relatively high species diversity of marine
planulae settling on the substrate loose the competition
plants: 211 species were found during the period from
with algae for the substrate, the coral reef of Sesoko
1995 to 1998. For comparison, coral reefs in the south-
Island, overgrown with algae and unable to build hard
ern Pacific are inhabited by about 360 algal and sea-
substrate (i.e. its own base) is likely to be destroyed.
grass species [9]. After the mass coral mortality and
However, studies on competitive relationships between
algal colonization of the newly formed substrate (dead
corals and algae on the damaged reef of Sesoko Island
corals), the number of marine plants at the reef of
[19, 20] showed that, in most cases, corals win the
Sesoko Island increased by 134 species. Further, the
struggle between coral polyps and algal communities.
number of dominant algal species increased. Before the
Thus, for example, in artificial injuries inflicted on mas-
catastrophe, a major portion of the bottom was occu-
sive and branched corals, polyps overgrew more than
pied by Gelidiella acerosa, Digenea simplex and Jania
100 algal species. Only toxic cyanobacteria of the
spp.; after the catastrophe Ulva, Codium, Galaxaura
genus Lyngbya were an insuperable hindrance to coral
and other species were added. We assume that the
growth.
appearance of algal species new to the reef of Sesoko
Island resulted from the absence of competition for In 2005, we found young colonies of massive and
substrate and other resources with both competitive branched corals in the intertidal and subtidal zones of
algal species typical for the area and, probably, corals. Sesoko Island, this observation indicates a recovery of
Very likely, the competition for substrate and resources the reef not only through regeneration of old injured
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
SPECIES COMPOSITION AND DISTRIBUTION OF ALGAE 41
Table 2. Projective cover (PC) of hard substrate with macroalgae before and after the nature catastrophe on the Ryukyus
PC of algae on hard Zones and depths
Locality Reference
substrate in % of algae growths
1997
Opposite Sesoko Biological From 1 to 20 No data Nonaka, 2004
Station
Before 1998
Western part of Sesoko Island ~5 Sublittoral, 2 m Titlyanov (unpublished data)
Opposite Sesoko Biological <30 No data Loya et al., 2001
Station ~50 Intertidal zone Titlyanov (unpublished data)
~10 Sublittoral, 2 m Ditto
North of Daito Is. <1 No data Nonaka, 2004
Miyako Islands From 2 to 20, grasses and No data Kajiwara, Matsumoto, 2004
algae
After 1998
Opposite Sesoko Biological <85 No data Sakai, 2004
Station <85 No data Loya et al., 2001
Akajima <65 No data Iwao, 2004
Minnajima and Iejima <75 No data Sakai, 2004
Western coasts of Okinawa Is. <95 No data Sakai (unpublished data)
2005
Opposite Sesoko Biological 40.22 ± 29.7 Upper intertidal zone Our data
Station 78.99 ± 11.67 Middle intertidal zone "
62.06 ± 6.6 Lower intertidal zone "
71.63 ± 8.43 Sublittoral zone 1.5 m "
Western Sesoko Is. 38.40 ± 14.8 Infralittoral zone "
33.41 ± 2.03 Middle intertidal zone "
49.21 ± 10.4 Lower intertidal zone "
corals, but also as a result of the settlement of new col- REFERENCES
onies [see also 17]. Evidently, the “phase shift” on the 1. Sorokin, Yu.I., Ekosistemy korallovykh rifov (Ecosys-
reef of Sesoko Island is a temporary event, and the coral tems of Coral Reefs), 3/4.: Nauka, 1990.
reef is able to recover in its original or modified state, 2. Abrar, M. and Efendy, Y., Coral Recovery After Bleach-
unless a catastrophe occurs again. ing in 1998 at West Sumatra Waters, Indonesia,
Abstracts. 10th Int. Coral Reef Symp., 2004.
3. Brown, B.E., Coral Bleaching: Causes and Conse-
ACKNOWLEDGEMENTS quences, Coral Reefs, 1997, vol. 16, pp. 129–138.
4. Diaz-Pulido, G. and McCook, L.J., The Fate of Bleached
We thank Prof. Moshin Morita, the President of the Corals: Patterns and Dynamics of Algal Recruitment,
University of the Ryukyus and Prof. Minoru Murai, the Mar. Ecol. Progr. Ser., 2002, vol. 232, pp. 115–128.
Scientific Leader of the Sesoko Marine Biological Sta- 5. Hasegawa, H. and Yamano, H., Ishigaki Island, Coral
tion for their kind invitation to work at the Sesoko Sta- Reefs of Japan. Ministry of the Environment; Jap. Coral
Reef Soc., 2004, pp. 212–218.
tion. We thank also the staff of the Sesoko Station of the
6. Hughes, T.P., Catastrophes, Phase Shifts, and Large-
Tropical Biosphere Research Center for their valuable Scale Degradation of Caribbean Coral Reefs, Science,
help and technical assistance. 1994, vol. 265, pp. 1547–1551.
This study was supported by the Russian Founda- 7. Iwao, K., Kerama Islands, Coral Reefs of Japan. Minis-
try of the Environment; Jap. Coral Reef Soc., 2004,
tion for Basic Research (Project 05-04-49901 “Com- pp. 185–189.
petitive Relations among Plant and Animal Organisms 8. Kajiwara, K. and Matsumoto, H., Miyako Archipelago,
in Mono- and Polydominant Communities of Sea- Coral Reefs of Japan. Ministry of the Environment; Jap.
weeds”). Coral Reef Soc., 2004, pp. 204–208.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007
42 SERGEEVA et al.
9. Littler, D.S. and Littler, M.M., South Pacific Reef Plants, 16. Pichon, M., Seguin, F., Hernandez, S. et al., Status of the
Offshore Graphics, Inc., 2003. Coral Reefs of Mayotte Islands (SW Indian Ocean) Five
10. Loya, Y., Sakai, K., Yamazato, K. et al., Coral Bleaching: Years After the 1998 Bleaching Events, Abstracts. 10th
the Winners and the Losers, Ecol. Lett., 2001, vol. 4, Int. Coral Reef Symp, 2004.
pp. 122–131. 17. Sakai, K., Okinawa Island, Coral Reefs of Japan. Minis-
11. McClanahan, T.R., Muthiga, N.A., and Mangi, S., Coral try of the Environment; Jap. Coral Reef Soc., 2004,
and Algal Changes After the 1998 Coral Bleaching: pp. 182–184.
Interaction with Reef Management and Herbivores on
Kenyan Reefs, Coral Reefs, 2001, vol. 19, no. 4, 18. Sakai, K., Muko, S., Nishikawa, A. et al., Coral Recruit-
pp. 380–399. ment and Recovery of Coral Communities After 1998
12. McCook, L.J., Competition Between Corals and Algal Mass Coral Bleaching Around Okinawa Island,
Turfs Along a Gradient of Terrestrial Influence in the Abstracts, 10th Int. Coral Reef Symp., 2004, p. 135.
Nearshore Central Great Barrier Reef, Coral Reefs, 19. Titlyanov, E.A., Titlyanova, T.V., and Yakovleva, I.M.,
2001, vol. 19, pp. 419–425. Competitive Relationships Between Algae and Coral
13. McCook, L.J., Jompa, J., and Diaz-Pulido, G., Competi- Polyps Communities Under Direct and Indirect Contacts
tion Between Corals and Algae on Coral Reefs: a Review on Damaged Corals, Abstracts, 10th Int. Coral Reef
of Evidence and Mechanisms, Coral Reefs, 2001, Symp., 2004, p.135.
vol. 19, pp. 400–417.
14. Nakano, Y. and Nakamura, S., Annual Record of Coastal 20. Titlyanov, E.A., Titlyanova, T.V., Yakovleva, I.M. et al.,
Observation at Sesoko Marine Science Center in 1991, Regeneration of Artificial Injuries on Scleractinian Corals
Galaxea, 1993, vol. 11, pp. 173–181. and Coral/Algal Competition for Newly Formed Sub-
strate, J. Exp. Mar. Biol. Ecol., 2005, vol. 323, pp. 27–42.
15. Nonaka, M., Daito Islands, Coral Reefs of Japan. Minis-
try of the Environment; Jap. Coral Reef Soc., 2004, 21. Veron, J.E.N., Corals of Australia and the Indo-Pacific,
pp. 199–201. Angus and Robertson Publishers, 1986.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 33 No. 1 2007