Marine plant communities of upwelling areas within the Arabian Sea: a taxonomic, ecological and biogeographic case study on the marine flora of the Socotra Archipelago (Yemen) and Masirah Island (Oman)

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Cover illustration: Nizamuddinia zanardinii (Schiffner) P. Silva
MARINE PLANT COMMUNITIES OF UPWELLING AREAS WITHIN THE ARABIAN SEA
A taxonomic, ecological and biogeographic case study on the marine flora of the
Socotra Archipelago (Yemen) and Masirah Island (Oman)
M
ARIENE PLANTENGEMEENSCHAPPEN IN OPWELLINGSGEBIEDEN VAN DE
ARABISCHE ZEE
Een taxonomische, ecologische en biogeografische casestudy naar de mariene
flora van de Socotra Archipel (Jemen) en het eiland Masirah (Oman)
Tom S
CHILS
Proefschrift ingediend tot het
behalen van de graad van Doctor
in de Wetenschappen (Biologie)
Promotor: Prof. Dr E. Coppejans
GHENT UNIVERSITY
Biology Department
Phycology Research Group
Krijgslaan 281 (S8)
B 9000 G
HENT - BELGIUM
U
NIVERSITEIT GENT
Faculteit Wetenschappen
Academiejaar 2002-2003

JURY
Supervisor
Prof. Dr E. Coppejans
Ghent University, Belgium
Additional members of the reading committee
Dr O. De Clerck
Ghent University, Belgium
Prof. Dr A. Meinesz
University of Nice-Sophia Antipolis, France
Dr W.F. Prud’homme van Reine
Leiden University, The Netherlands
Additional members of the examination committee
Prof. Dr M. De Dapper
Ghent University, Belgium
Prof. Dr H.J. Dumont
Ghent University, Belgium
Prof. Dr P. Goetghebeur
Ghent University, Belgium
Prof. Dr M. Vincx
Ghent University, Belgium
Prof. Dr W. Vyverman
Ghent University, Belgium
Project start: October 1, 1999
Thesis submitted: October 16, 2002
Thesis defense: December 20, 2002
This study was carried out in the Phycology Research Group, Biology Department, Ghent
University (Belgium). The Fund for Scientific Research - Flanders (F.W.O.) is acknowledged
for the assistance in providing a research assistant grant and a travel grant to Murdoch
University (Western Australia).

DANKWOORD - ACKNOWLEDGEMENTS
Unrooted Tree 'Merci'
Hoewel het hier geenszins een proefschrift met een fylogenetische inslag betreft, is deze
dankbetuiging (the tree 'merci') gericht aan een diverse groep van clades, allen van
onmiskenbaar belang in hun specifieke bijdrage tot het volbrengen van dit proefschrift
('unrooted' dus).
Allereerst dank aan mijn promotor Eric Coppejans, als het ware de pilootvis van het
Indische Oceaanonderzoek in onze groep. Zijn inzet om ieders onderzoek vlot te laten
verlopen en een goede logistieke ondersteuning te waarborgen is een stimulans van formaat.
Verder stonden zijn gemoedelijke uitstraling en grapjes garant voor de uiterst aangename
sfeer in de onderzoeksgroep. Eric, je hebt ook mijn volle bewondering om tijdens de laatste
weken de bundeltjes lectuur met grote zorg en de nodige spoed na te kijken.
Next in line, de vrolijke compagnons van het wiersnuisteren. Olivier, onze vraagbaak van
duizend en één algologiebekommernissen en moderator van evenveel conversaties die wel
eens poogden te verglijden in redevoeringen over boeddhisme of een cursus fietsagressie
voor beginners. Maestro, dank voor de vele goede tips, trucs en hulp doorheen het verloop
van dit proefschrift. Zijn metgezel Frederik, de enige echte huisfilosoof van Dodonaea Inc.:
een immer goedlachse gabber, van alle markten thuis en met een tomeloze inzet voor
iedereen. Zijn doorgedreven verkenningstocht op Socotra en de bijbehorende 'rijke oogst',
zorgde ervoor dat ik vanaf de eerste werkdag onmiddellijk een vliegende start kon nemen.
Muchos graçias Freddie! Mister Engledow, the man of universal wisdom. Altijd gereed om
een leuk weetje of interessante zienswijze te lanceren. Ook bureaugenoot eerste klas: het
afvuren van vrolijke muziek- en gemoedsnoten maakten van elke dag een Henrydag. Voorts
een magnifiek reviewer die zonder verpinken zijn welwillend oog op de Engelse tekst van dit
proefschrift heeft laten vallen om te besluiten dat het geen Shakespeare was. Merci Henry!
The new kid in town, Heroeneman, oftewel de nieuwe fourierwervelwind met een amplitude
van Rammstein Unplugged. Plezante bureaugenoot die ontegensprekelijk zijn penningen zal
verdienen met de show 'statistiek magiek' waarin het bevallige penningwier (Halimeda voor
de die-hards) figureert als trouwe assistente. Enrico, from downtown Cape Town to the
intergalactic sandwich bar in his office on the Sterre, was a fun toiling comrade during the
final weeks. Ook dank aan de collega's protistologen voor het animo in de gang.
The collection of the studied vegetarian delicacies and their subsequent treatment
according to phycological standards could not have been possible without the help of fellow
workers and organizations. I am grateful to the Senckenberg Institute, Germany, (Michael
Apel and Friedhelm Krupp) and the Ardoukoba Association, France, for the excellent field
trip preparations to Socotra and Masirah. John Huisman is an inspiring phycologist and I
greatly appreciated his hospitality during my stay in Western Australia. I thank Michael
Wynne for his dedicated discussions on Omani algae. Barry Jupp and Simon Wilson are
great colleagues that shared their marine knowledge on site and electronically thereafter.
Hartelijke dank aan Paul Goetghebeur om mijn eerste escapades in het Asterix-Latijn om te
toveren tot oerdegelijke Latijnse beschrijvingen. Dank aan de voltallige jury voor hun
interesse en inzet tot het voleindigen van dit proefschrift. De steun van het Fonds voor
Wetenschappelijk Onderzoek - Vlaanderen is overduidelijk: het fonds bood de mogelijkheid
om me te verdiepen in een groeiende passie en financierde het studieverblijf in Australië.

John Huisman, Gerry Kraft, Max Hommersand and the anonymous referees, which invested
their time to improve certain manuscripts, are acknowledged for their commitment. Wim
was een aangename student die met glans de Amansieae voor de bijl kreeg. Cathy en
Christelle verzorgen het dagdagelijks reilen en zeilen in de onderzoeksgroep. Daarnaast
destilleert Cathy met veel toewijding onze dagelijkse portie black fuel om de namiddag in
vijfde vitesse te kunnen beëindigen en Christelle behartigt met fleur het papierwerk en de
karaokebar. Dank aan allen.
Rinaldo, comrad van het eerste biologie-uur, stond garant voor de amusante uitlaatklep
tijdens de avondsessies klimmen, squash, enz. Rein en Jill vormden samen onze vrolijke
huisgenoten aan de pitsstop in de Martelaarslaan. De activiteiten met de klasgenoten van
weleer vormden ook steeds fijne intermezzo’s. Gert fungeerde doorheen de boerenzonen-op-
speed-periodes als counteractieve boksbal wanneer het ADHD-gevoel hoogtij vierde. Ghent
by night en sportweekend waren de geliefkoosde bezigheden in onze agenda. De leutige
bende van de duikclub en de onderwaterhockeyfanatiekelingen maakten van deze
bijeenkomsten een waar festijn, dank je wel Tim & Mieke, Dieter & Elke, Gregory & Ann,
Jeroen, Kenneth, Koen, Stefan, enz.
De madre, padre en Ine: in de eerste plaats bedankt om er zo'n prettig gezin van te maken.
Samen met Dave, de meest recente aanwinst op de Weg naar Bijloos-sofa, is elke
samenkomst met dit kwartet een zalig moment van plezier. Verder, mijn uiterste appreciatie
voor jullie continue steun, open geest en de hulp doorheen de jaren. Ondanks de dalende lijn
in Houthalenexcursies stonden de makkers Bert, Tom, Jimmy en Johan borg voor de
broodnodige leuke weekendmomenten. Forza Limburgia!
Londerzeel is intussen een tweede thuishaven geworden. Anne-Marie en Walter maken
met vele kleine en evenveel grote attenties het leven van alledag fleurig en uiterst genietbaar.
Koen en Heidi vervolledigen dit plezierige gezin in bijbehorende stijl. Klasse!
'El Sea' of 'Sweetlips', neen niet de titel van een goedkope B-film uit verjaarde
videotheekrekken, maar de magistrale levensgezel die de gehele trip van kleur voorzag. Else,
dank je voor de vele leuke momenten en de weelde aan goede zorgen die een apart
dankwoord verdienen, op een andere plaats, onder een andere vorm. The greatest!

CONTENTS
Acknowledgements - Dankwoord
Chapter 1 Introduction and objectives 1
Chapter 2 Gelatinous red algae of the Arabian Sea, including Platoma
heteromorphum sp. nov. (Gigartinales, Rhodophyta)
Published as: Schils T. & Coppejans E. 2002. Gelatinous red algae of the
Arabian Sea, including Platoma heteromorphum sp. nov. (Gigartinales,
Rhodophyta). Phycologia 41(3): 254-267 (and cover photo).
25
Chapter 3 The red algal genus Reticulocaulis from the Arabian Sea, including
R. obpyriformis sp. nov., with comments on the family Naccariaceae
Published as: Schils T., De Clerck O. & Coppejans E. 2003. The red algal
genus Reticulocaulis from the Arabian Sea, including R. obpyriformis sp. nov.,
with comments on the family Naccariaceae. Phycologia 42(1): in press (and
cover photo).
47
Chapter 4 Chamaebotrys erectus sp. nov. (Rhodymeniales, Rhodophyta) from the
Socotra Archipelago, Yemen
Published as: Schils T., Huisman J.M. & Coppejans E. 2003. Chamaebotrys
erectus sp. nov. (Rhodymeniales, Rhodophyta) from the Socotra Archipelago,
Yemen. Botanica Marina 46(1): in press.
67
Chapter 5 A re-assessment of the genus Izziella Doty (Liagoraceae, Rhodophyta)
Published as: Huisman J.M. & Schils T. 2002. A re-assessment of the genus
Izziella Doty (Liagoraceae, Rhodophyta). Cryptogamie Algologie 23(3): 237-
249.
77
Chapter 6 Spatial variation in subtidal plant communities around the Socotra
Archipelago and their biogeographic affinities within the Indian Ocean
To be published as: Schils T. & Coppejans E. 2003. Spatial variation in
subtidal plant communities around the Socotra Archipelago and their
biogeographic affinities within the Indian Ocean. Marine Ecology Progress
Series: accepted.
89
Chapter 7 Phytogeography of upwelling areas in the Arabian Sea
Submitted as: Schils T. & Coppejans E. Phytogeography of upwelling areas in
the Arabian Sea.
109
Chapter 8 Synthesis and perspectives 131
Chapter 9 Synthese en perspectieven 139

Introduction and objectives 1
CHAPTER 1
G
ENERAL INTRODUCTION
Study area defined
Arabian Sea
The Arabian Sea is situated in the northwestern Indian Ocean and comprises the Gulf of
Aden, the Arabian Sea sensu stricto (from the southern Arabian Peninsula down to the Horn
of Africa and the southern tip of India), the Gulf of Oman and the Persian Gulf (Fig. 1). In
this study we focus on the upwelling areas off the coasts of the southern Arabian Peninsula,
using the restricted definition of the Arabian Sea sensu Wilson (2000): the Arabian Peninsula
and the Gulf of Oman define the Arabian Sea to the north, the African continent and the Gulf
of Aden to the west, South-West Asia to the east, and the southern boundary is generally
considered to be the 8°N parallel. The following geographical localities are used for a clear-
cut delimitation of the Arabian Sea sensu stricto (hereafter Arabian Sea; Wilson 2000): to
the west between Ra’s Asir (11°50’N, 51°16.9’E; Somalia) and Ra’s Fartak (15°35’N,
52°13.8’E; Yemen); to the north between Ra’s Al Hadd (22°30’N, 59°48’E; Oman) and Ra’s
Al Fasteh (25°04’N, 61°23’E; Iran); and from the Iran-Pakistan border (25°12’N, 61°36’E)
in the east to the southern limit (8°N). In total seven nations border the Arabian Sea:
Somalia, Yemen, Oman, Iran, Pakistan, India and the Maldives.
Both investigated island groups, Socotra and Masirah, are located in the Arabian Sea s.s.
Since the Cenozoic Era (65 Ma BP-present) Arabia drifted away from Africa, giving rise to
the Red Sea and the Gulf of Aden (Fig. 2). As a result, the Socotra Archipelago and Masirah
Island are located on two distinct tectonic plates. Both Islands are of a unique geological
composition. Mies & Printzen (1997) stressed the presence of a granite core (Haghier
Mountains) on Socotra Island, which has been above sea level since the Cretaceous, and the
island has been referred to as one of the most isolated landmasses since that period (Kossmat
1907). This long period of isolation is reflected in the pronounced level of endemism of the
terrestrial biota on Socotra (about one third of the terrestrial plants from the archipelago is
considered to be endemic, Wranik 2002) and has important biogeographic consequences
(Mies 1998; Wranik 1998, 2002). Masirah, on the other hand, forms a distinct structural
element within the Arabian Plate, the Masirah Ophiolite Uplift. Ophiolites provide the best
exposure in the world to study the oceanic lithosphere.

2 Chapter 1

Introduction and objectives 3
Fig. 1. World map showing the large marine ecosystems of the world, demarcated by yellow lines and
indicated with numbers. The Arabian Sea (No 32) is colored in red. Numbers correspond with: 1, East
Bering Sea; 2, Gulf of Alaska; 3, California Current; 4, Gulf of California; 5, Gulf of Mexico; 6, Southeast
U.S. Continental Shelf; 7, Northeast U.S. Continental Shelf; 8, Scotian Shelf; 9, Newfoundland-Labrador
Shelf; 10, Insular Pacific-Hawaiian; 11, Pacific Central-American Coastal; 12, Caribbean Sea; 13,
Humboldt Current; 14, Patagonian Shelf; 15, South Brazil Shelf; 16, East Brazil Shelf; 17, North Brazil
Shelf; 18, West Greenland Shelf; 19, East Greenland Shelf; 20, Barents Sea; 21, Norwegian Shelf; 22,
North Sea; 23, Baltic Sea; 24, Celtic-Biscay Shelf; 25, Iberian Coastal; 26, Mediterranean Sea; 27, Canary
Current; 28, Guinea Current; 29, Benguela Current; 30, Agulhas Current; 31, Somali Coastal Current; 32,
Arabian Sea; 33, Red Sea; 34, Bay of Bengal; 35, Gulf of Thailand; 36, South China Sea; 37, Sulu-Celebes
Sea; 38, Indonesian Sea; 39, North Australian Shelf; 40, Northeast Australian Shelf/Great Barrier Reef;
41, East-Central Australian Shelf; 42, Southeast Australian Shelf; 43, Southwest Australian Shelf; 44,
West-Central Australian Shelf; 45, Northwest Australian Shelf; 46, New Zealand Shelf; 47, East China
Sea; 48, Yellow Sea; 49, Kuroshio Current; 50, Sea of Japan; 51, Oyashio Current; 52, Sea of Okhotsk; 53,
West Bering Sea; 54, Chukchi Sea; 55, Beaufort Sea; 56, East Siberian Sea; 57, Laptev Sea; 58, Kara Sea;
59, Iceland Shelf; 60, Faroe Plateau; 61, Antarctica; 62, Black Sea; 63, Hudson Bay; 64, Arctic Ocean.
After LME (2002).
Fig. 2. Arabia detached from Africa and
soon began to collide with Eurasia in
mid-Tertiary time, when most ophiolite
complexes emplaced at the close of the
Cretaceous onto its northern margin
were incorporated in the Biltis-Zagros
suture zone. Only the Sama’il and
Masirah ophiolite belts of southeast
Arabia escaped later continental-collision
events and still preserve most of their
original obduction-related features. After
Garzanti et al. (2002).
Socotra Archipelago
The Socotra Archipelago (12.47°N, 53.87°E; Fig. 2) is positioned in the southwestern part of
the Arabian Sea, proximate to the Gulf of Aden. Despite being only 100 km from Somalia,
Socotra politically belongs to Yemen. The archipelago comprises four islands: the main
island Socotra; Abd al-Kuri; Samha and Darsa, the latter two smaller islands are also known
as “The Brothers”. The archipelago sits on the Carlsberg Ridge (from the archipelago,
running southeast) and shallow seas connect the islands, whereas a deep trench separates the
archipelago from mainland Africa. The islands have been relatively little affected by human
activities due to the reduced accessibility caused by the southwest monsoon, the harsh
climate, the sparse fertile grounds and stringent traveling policies. In addition to the long
isolation, traditional community rules limit the exploitation to sustainable levels and make
Socotra comparatively untouched.

4 Chapter 1
Socotra Island is the largest Arabian island (Al-Hity 1998) and measures approximately
120 by 40 km, covering an area of about 3600 km
2
. The geological composition consists of a
basement complex of igneous and metamorphic rock from the Precambrian, which are
overlain by sedimentary, mainly limestone and sandstone. Topographically, the island
consists of three main zones: (i) the alluvial coastal plains (e.g. the Nojid Plain), (ii) a
limestone plateau, with an altitude range from 300-700 m, which covers most of the island,
and (iii) the Haghier mountains rising to an elevation of 1519 m. Abd al-Kuri and “The
Brothers” are smaller and subject to more extreme conditions due to the absence or limited
availability of fresh water, less topographical variation and fewer sheltered sites. The second
largest island, Abd al-Kuri (36 by 6 km), is positioned about half way in between Socotra
and Somalia. Samha and Darsa are both flat topped limestone plateaus with sheer sides, the
former being inhabited by a small human population and the latter uninhabited but sustaining
a large rat population (Al-Saghier & Porter 1998; Wranik 1998). Additionally, a few isolated
rocky stacks, Kal Farun (literally “balls of the Farao”), Sabuniya and Hertha, occur within
the archipelago, their remoteness being beneficial for certain species, e.g. breeding seabirds
(Al-Saghier et al. 2000), and particular biotic communities that are protected from natural
and anthropogenic threats: e.g. coral bleaching due to the elevated temperatures of coastal
waters, fishing.
Masirah Island
Masirah Island is located in the northern part of the Arabian Sea (20.42°N, 58.79°E; Fig. 2),
the island is about 65 km long and 15 km wide, covering an area of 1095 km
2
. Politically, the
island belongs to the Sultanate of Oman. The island has a peculiar geological history, being
an excellent geological field laboratory due to the distinct obducted ophiolite sequences that
were part of a Proto-Indian Ocean basin in the Late Jurassic (Marquer et al. 1998; Garzanti
et al. 2002). The ophiolite covers most of Masirah Island and presumably forms the bedrock
of the Masirah Channel.
The Masirah Channel separates the island from Barr al-Hikman on the Arabian Peninsula.
Barr al-Hikman and Masirah Island constitute an important biotic haven on the southern
Arabian shores. Together they total about 240 km
2
of exposed mudflats, which are important
for the passage and wintering of water birds and for nesting and feeding of sea turtles
(Gallagher et al. 2002). Masirah Island supports the largest loggerhead turtle (Caretta caretta
Linnaeus) nesting grounds in the world, which mainly depend on seagrass for nourishment
(Pilcher 2002). These extensive intertidal mudflats occur along the central and northern part
of Masirah’s west coast. Seagrass beds are especially well developed around Shaghaf Island
off Masirah’s west coast. This small island also harbours the only mangrove stands,
Avicennia marina (Forsskål) Vierhapper, for Masirah island and its surrounding islets.
Fringing and isolated coral communities also occur in the Masirah Channel. Off Barr al-
Hikman, a remarkably large, and so-called monospecific reef (perhaps the largest
monospecific coral stand known on Earth, Paulay & Meyer 2001) has developed almost
exclusively made up of a cabbage coral (Montipora sp.). The phenomenon of coral stands
that are largely dominated by one species also occurs in other parts of the world where coral
development is hindered by harsh environmental conditions, e.g. large temperature variation,
high sedimentation, high salinities, etc. The east coast of Masirah is exposed, consisting of
sandy beaches and rocky outcrops. The terrestrial vegetation of Masirah Island is dominated
by small shrubs such as Arthrocnemum, Limonium and Suaeda (Gallagher et al. 2002).

Introduction and objectives 5
The mean annual rainfall is 110 mm, but is erratic and, since 1956, has varied from 0 mm
to over four times the mean figure. The mean air temperature in July is 33°C and that of
January is 20°C. The mean tidal variation (MHHW to MLLW) is about 1.5 m (Gallagher et
al. 2002).
Oceanography and marine ecology of the Arabian Sea
The oceanography of the Arabian Sea is driven by the alternation of two opposing monsoon
winds: the southwest monsoon during summer (June–September; hereafter SW monsoon)
and the northeast monsoon during winter (November–February; hereafter NE monsoon). The
periodic reversals in the wind drive corresponding inversions in the currents of the upper
ocean. The strong wind velocities during the SW monsoon in summer (Fig. 3), initiate the
Somali Current with surface velocities of 3.7 m s
-1
(Düing et al. 1980). The Somali Current
has perhaps the most dramatic seasonal variation of any current in the world oceans. Its
volume transport is comparable to that of the Gulf Stream but changes direction with
monsoon winds: towards the poles during the SW monsoon and towards the equator during
the NE monsoon (Subrahmanyam 1998). In summer, the Somali Current spins off south of
Socotra and is continued along the southern Arabian shores to the mouth of the Gulf of
Oman (Figs 4, 5; Currie 1992). South of Socotra, the Somali Current originates a northern
eddy, the “Great Whirl” (Warren et al. 1966), and contiguous with the latter another
anticyclonic circulation evolves east of Socotra, the “Socotra Eddy” (Bruce & Beatty 1985;
Currie 1992). The Somali Current, its derived eddies and the current along the southern
Arabian shores generate wind-induced upwelling of cold nutrient-rich water (Figs 4-6). The
currents arise from winds that blow over the sea parallel to the coasts. Seawater, however, is
not pushed directly in front of the wind, but moves at about 45° to the right of the wind's
motion in the northern hemisphere (to the left in the southern hemisphere) due to the Coriolis
force, an effect caused by the rotation of the earth. Further down in the water column, the
direction of flow continues to be deflected rightward (or leftward), until ultimately a three-
dimensional spiral is formed vertically in the water. The net transport of water, i.e. Ekman
transport (Figs 6, 7), is at an angle of roughly 90° to the direction of the wind. The removal
of these surface waters, to a depth of a few hundred meters, off the coast is replaced with
cold and nutrient-rich waters from the deep. During the NE monsoon in winter, some areas
in the eastern Arabian Sea are subject to upwelling (Fig. 4). During the SW monsoon high
nutrient levels, being 3-5 times greater than those during the NE monsoon, are recorded for
the upwelling waters of Oman (Barrat et al. 1986): 5-20 mg NO
3
m
-3
; 1.5-2.5 mg PO
4
m
-3
.
Phytoplankton is the first to take advantage of the nutrients brought up by upwelling and
initiate a quick increase in productivity, reflected by high chlorophyll a concentrations (5-20
mg m
-3
, Savidge et al. 1988). In a second phase, zooplankton feeds on the abundant
phytoplankton, the former falling prey to larger plankton and small fish. Whales, large fish
and sea birds feed upon the smaller predators, resulting in very rich fishing grounds. The NE
monsoon has received less scientific attention as it is less energetic than the SW monsoon,
but the near surface circulation is still dominated by the wind system during this period
(Subrahmanyam 1998). During the NE monsoon the current flows southwards along the
Somali coast all the way to the equator. This southward cross-equatorial flow, however, is
very shallow relative to the deep northward flow during the SW monsoon (Schott 1986). In
the transition months, offshore Ekman transport is lacking, as the winds are not strong
enough (Subrahmanyam 1998).

6 Chapter 1
Fig. 3. Monsoonal wind speed in the northwestern Indian Ocean (15°N, 60°E). Wind speed data are
monthly averages of daily measurements from 1986-1990. One knot = 0.51 m s
-1
. From Mies & Beyhl
(1998).
Fig. 4. Surface water circulation in the northern part of the Indian Ocean (a) in July (maximum of the
SW monsoon) and (b) in February (maximum of the NE monsoon). Open arrows show the direction of
monsoons; filled arrows show the direction of surface currents. 1, the zones of seasonal upwelling; 2, the
zones of episodic upwelling. The major open arrow represents the direction of the latent heat transfer
from the southern subtropical Indian Ocean maximum to the Asian continent with the Findlater jet flow.
From Ivanova (2002).

Introduction and objectives 7
Fig. 5. Sea surface temperatures
(°C) of Arabian Sea waters in
August 1993 (SW monsoon).
The Equatorial Jet (EJ), Great
Whirl (GW), Somali Current
(SC), Socotra Eddy (SE) and
the South Equatorial Current
(SEC) are indicated. After
Subrahmanyam (1998) and
Kantha et al. (2002).
Fig. 6. Wind blowing parallel to
the shore in the northern
hemisphere during the SW
monsoon, inducing a surface
current (Somali Current) and
upwelling by means of surface
water transport through the
Ekman spiral. After Thurman
(1996).
Fig. 7. Ekman transport (Sv) in the Arabian Sea during (a) the peak SW monsoon (July 1993) and (b) the
peak NE monsoon (January 1993). From Subrahmanyam (1998).

8 Chapter 1
The upwelling phenomenon creates extreme marine conditions in the Arabian Sea. Coastal
sea surface temperatures (SST) vary by an average of 10°C (Wilson 2000). Savidge et al.
(1990) even recorded a minimum SST of 15.9°C during the SW monsoon of 1989 in the
Arabian Sea, whereas Salm (1993) reports on a maximum SST of 39°C in 1990 for the Gulf
of Oman. The deeper waters of the Arabian Sea, below 100 m deep, are also extreme in
having critically low levels of dissolved oxygen. Arabian Sea water is higher in salinity than
the surrounding Indian Ocean due to surface evaporation and intensified by intrusions of
higher salinity water from the Persian Gulf at 300 m deep and from the Red Sea at 800 m
deep (Wyrtki 1973). Vertical mixing of these layers results in a thick layer of high salinity
water, which extends to depths of 2000 m. The isolation of this water together with a high
pelagic productivity creates a large mass of water with a very low oxygen concentration
from 200 to 2000 m deep. The O
2
values of this layer in the Arabian Sea (0.2-1 ml l
-1
) are 2-
4 times lower in comparison to other Indian Ocean waters at this depth (Sheppard et al.
1992). Following upwelling this suboxic layer reaches the surface with widespread mortality
among fish as a result. The effects were perceived during the field trip to Masirah Island
(November 1999, the aftermath of the SW monsoon), where great numbers of triggerfish
(Balistidae), apparently particularly prone to low oxygen concentrations, washed ashore.
The investigated islands, Socotra and Masirah, are both subjected to intense upwelling
during the SW monsoon. Both harbour a similar diversity in marine habitats, but differ in
their geographical position within the Arabian Sea and the corresponding upwelling areas.
Socotra Archipelago
The upwelling at the Socotra Archipelago results from the Somali Current, which flows
northwards in summer and initiates the “Great Whirl” and the “Socotra Eddy” (Fig. 5; Currie
1992; Bruce & Beatty 1985). The Great Whirl mainly affects the southern coasts of the
Socotra Archipelago and the Socotra Eddy influences the east coast of the main island. At
the end of the SW monsoon (October) the Great Whirl decays into a series of complex
current patterns around the archipelago.
Masirah Island
Masirah Island is located in the upwelling area off the southern Arabian Peninsula. The
southwestern winds blow parallel to the shores, initiating strong upwelling along the coasts
of Hadramout (Yemen) and Dhofar (Oman) to Ra’s al Hadd (Oman). The east coast of
Masirah is the exposed shore subjected to upwelling. The west coast, from Masirah Channel
to Barr al-Hikman, is on the leeward side of the strong surface currents during the SW
monsoon. As a result this protected channel shows monsoonal currents of less than half a
knot (Gallagher et al. 2002).
Biogeography and paleoceanography of the Arabian Sea
The biota associated with the lower water temperatures during upwelling periods, generally
occur in the temperate waters at higher latitudes, a phenomenon that has been termed the
“pseudo-high latitude effect” (Sheppard et al. 1992; Kemp 1998b). The Arabian Sea is
characterized by a seasonal peak in productivity and a patchy distribution of different
biocoenoses consisting of scarce coral reefs, scattered coral communities and macroalgal

Introduction and objectives 9
dominated subtidal communities. The Arabian Sea is generally regarded as part of the larger
Arabian region, being a biogeographic sub-region of the Indian Ocean and comprising the
Red Sea, Gulf of Aden, Arabian Sea, Gulf of Oman and Persian Gulf (Sheppard et al. 1992).
These authors note that a subdivision in sub-provinces might be useful for certain groups of
fish, but they concluded that it cannot be justified for the marine plants. Sheppard et al.
(1992), however, largely based their opinion on restricted information, i.e. the seagrasses,
mangroves and some seaweeds of the Red Sea.
The biodiversity within the upwelling areas of the Arabian Sea has gradually been
revealed over the past two decades. The location of these upwelling areas between the Red
Sea, the Persian Gulf and the “parent” Indian Ocean (Sheppard et al. 1992) makes the
Arabian Sea an area of sympatry for biota from these water bodies (Kemp 1998b). During
the Late Pleistocene Glaciation (17 Ka BP, the peak of the last glaciation) sea level was
about 130 m below present (Hopley 1982), which dried out the Persian Gulf and potentially
the Red Sea, or turning the latter hypersaline. About 15 Ka BP global surface temperatures
increased markedly, resulting in the Holocene transgression during which macroscopic
marine life recruited both seas via the northern Indian Ocean. During the early part of the
transgression and about 3-4 Ka years thereafter, the intensity of the monsoons and the
Arabian Sea upwelling were considerably reduced. On the contrary, 9±2 Ka BP upwelling
was considerably stronger than today and from that time on the upwelling intensity gradually
declined to its present, moderate state. So, the recruitment of biota into the Red Sea and the
Persian Gulf most likely happened in the late Pleistocene-early Holocene. In the mid
Holocene, the intensified upwelling and its larger geographical extent probably caused a
barrier to tropical biota, resulting in vicariance speciation in the pockets of (sub)tropical
waters. During this time favorable habitats for temperate marine biota expanded, e.g.
luxuriant algal communities (Sheppard et al. 1992).
Dependent on the author and the investigated group of organisms, the region is said to
comprise a large number of widespread species and few endemics (Wilson 2002), whereas
others characterize the Hadramout (Yemen) and Dhofar (Oman) coasts of the Arabian
Peninsula as centers of endemism (Randall & Hoover 1995; Randall 1996). In this context,
Paulay (1999) notes that the coral communities of the Arabian Sea are isolated from reefs in
the surrounding seas by unfavourable habitats, i.e. intense upwelling toward the west and
soft bottoms and major river discharge (Indus) toward the east. This isolation is conducive to
allopatric speciation. Furthermore, the coral reefs of Oman are located at the entrance to the
ancient European Tethys, and because of their isolation could conceivably be home to relict
taxa from the ancient tethyan biota. This factor may contribute toward the occurrence of relic
endemics. Detailed taxonomic work on other Arabian Sea biota has also lead to new insights
as the extension of known distribution ranges of organisms (e.g. Kemp 1998b); the
occurrence of disjunctly distributed species (e.g. the coral and algal species from Oman that
also occur in Hawaii and Japan, respectively; Coles 1995; Wynne 2000); the discovery of
new (endemic) species (e.g. Wynne 1999a); the significant increase of the regional marine
biodiversity (e.g. the rich fauna of decapod Crustaceae, Apel 2000; the high diversity and
high degree of endemism of echinoderms for the Arabian Sea, Price 1982); and taxonomic
updates (e.g. the intensely observed, so-called “Montipora foliosa” reefs seem to represent a
new endemic species, Paulay & Meyer 2001).

10 Chapter 1
Sample sites defined: marine habitats
“Marine plant communities of upwelling areas within the Arabian Sea” implies that the
studied flora grows in marine influenced habitats. Adlittoral and intertidal habitats were
generally devoid of algal communities because of the limited splash zone during the NE
monsoon, the high evaporation rate, the solar irradiation and wind stress that limit algal
growth severely. Due to the relatively low tidal range of the area, intertidal biotopes were
largely limited to areas with a gentle slope. The few extensive intertidal habitats include the
upper zone of mudflats and certain seagrass beds, composed of macroalgal assemblages,
seagrasses and rarely mangroves. Besides these biotopes of fine sediment, sample efforts
were focused on hard substrata, i.e. rocks and coral deposits (sometimes covered by a layer
of fine sediment), as most benthic organisms (algae) grow best on these surfaces. The
subtidal habitats harbour the most luxuriant biotic life and different biotopes can readily be
discerned: coral reefs, coral communities, seagrass beds, macroalgal communities and soft
sediment biotopes. An additional semi-marine biotope includes the blue holes, i.e. terrestrial
pits that are interconnected with the sea by means of caves, characterized by a layer of fresh
water on top of the saline water mass. They contain a specialized flora (e.g. Ruppia maritima
Linnaeus), restricted to the photic top layer, which can cope with salinity fluctuations
according to the specific zonation belt. A characteristic macroalgal zonation pattern of
intertidal and exposed rocky shores of the Arabian Sea is presented in Fig. 8. Besides
intertidal pools, the intertidal of less exposed shores is relatively barren with few macroalgae
(e.g. Codium arabicum Kützing).
Socotra Archipelago
Whereas the south coast of Socotra Island is greatly affected by the upwelling phenomenon,
the northern shores are more protected, especially certain embayments near the center of the
north coast. Dunes and sandy beaches characterize the north coast, and well-developed coral
communities thrive well at certain sheltered sites. Due to their small size, the outer islands,
Abd al-Kuri and The Brothers, are less protected from the extreme upwelling conditions. F.
Leliaert (Ghent University) was the first phycologist to participate in a marine survey in the
framework of the United Nations Development Programme and Global Environment Facility
(hereafter UNDP/GEF) project entitled “Conservation and sustainable use of biodiversity of
Socotra Archipelago”. He collected 463 algal samples from 63 sites in the period from 13
January-20 February 1999 (Leliaert 2000). These specimens were very helpful to acquire an
insight in the macroalgal flora of the main island. Since complete lists of the investigated
sites and quantitative (relevé) data could not be assessed due to time restrictions, the
ecological analysis of this thesis was confined to the material collected during the two
subsequent studies. The second field trip to the Socotra Archipelago took place from 26
March-7 May 2000. A map of sample sites where detailed species inventories were recorded
is presented in Fig. 1c of chapter 7.
Masirah Island
In 1999, the Ardoukoba Association (France) organized the scientific campaign “Oman 99”
to Masirah Island. Eleven marine scientists (zoologists, botanists and biochemists)
participated in a joint effort to characterize the biocoenoses of the different ecosystems and
to search for bioactive molecules. The base camp was installed at the southern tip of the

Introduction and objectives 11
island where the upwelling coasts border the upwelling sheltered shores, being an excellent
location to sample the contrasting biotopes by small boats. The impact of the upwelling
phenomenon in the area was striking in many ways: suspension feeders were extremely
abundant, the population density of most invertebrates was very high, corals displayed
extensive bioerosion, and consequently reef construction was extremely limited (Paulay
1999). Sampling of macroalgae was undertaken between 2-30 November 1999. Fig. 1b
(chapter 7) shows a map of sample sites with detailed species inventories.
Fig. 8. A diagrammatic representation of the dominant species in the intertidal on the exposed rocky
shores of southern Oman. (a) General, steeply sloping rock of the type found at Mughsayl, Raysut and
Sadha. (b) Vertical rock face at Mughsayl. (c) Semi-exposed broken rock at Mirbat. Scale bar = approx.
1 m. After Barratt et al. (1984).

12 Chapter 1
Ecological and biogeographic units: macroalgal and seagrass species
In analyzing the biodiversity, the similarities and the biogeography of the sampling sites
from the different marine plant communities, there was a need for a basic unit. In broad
ecological studies, the commonly used entity, and arguably the only biologically meaningful
level (Sheppard et al. 1992), is the basic taxonomic unit “species”. More refined
identifications of different growth forms from a specific species (ecological or regional
variants: varieties, ecomorphs, subspecies, etc.) are only used when the continuum in
morphological variety fits into categories (e.g. Caulerpa polymorphism). These
identifications below species level can be useful as certain types of morphology are related
to the governing environmental parameters, which also shape marine biocoenoses. Although
species concepts differ between ecologists, molecular biologists and philosophers (Hull
1997), the term “species” generally refers to an exclusive combination of morphological and
anatomical traits that can be observed in the field or the laboratory. Recent molecular and
culture studies, however, have shown that the existence of cryptic diversity (molecularly
diverged but not pronounced so in anatomical or morphological traits, e.g. Stiller & Waaland
1993) and species complexes (a multitude of hitherto recognized species that are not
supported by molecular phylogenies, e.g. Zuccarello & West 2002) might be more common
than currently accepted. Consequently, biogeographic studies might indicate links with
(distant) areas based on traditional identification techniques, while the respective species in
fact have already molecularly or reproductively speciated into different taxa. By using a
multitude of traits (e.g. inclusion of the study of post-fertilization events directly linked to
the reproductive process, chapters 2-5), and focusing primarily on the Rhodophyta
(pronounced and distinct reproductive features between species in comparison to the
Phaeophyta and Chlorophyta), these problems have been partly overcome.
Macroalgae
Macroalgae or seaweeds are the common names for a polyphyletic group of photosynthetic,
eukaryotic and multicellular organisms belonging to three phyla classified by their
photosynthetic pigmentation, viz. the Rhodophyta (red algae), Phaeophyta (brown algae) and
Chlorophyta (green algae). Structurally, macroalgae have been grouped in the Thallophyta:
plants without a differentiation into roots, stem and leaves, and lacking the conducting
tissues phloem and xylem. In contrast to the omnipresent and likewise “artificial” (non-
monophyletic) group of algae (all organisms containing chlorophyll a, except the land
plants), macroalgae mainly occur in marine habitats. Macroalgae are found in all seas and in
various forms: filamentous, crustaceous, epiphytes and large macrophytes. Currently, about
7300 species of marine macroalgae or seaweeds are known (Smith 2002). Most seaweeds are
highly adapted to a specific littoral zone (adlittoral, intertidal, subtidal fringe, subtidal) and
specific environmental conditions (epilithic, epipelic, epipsammic, epiphytic, temperature,
salinity, etc.) for optimal growth or population structure. Most well-developed and luxuriant
algal communities are confined to hard substratum, i.e. rocky shores or solid anthropogenic
constructions. The subtidal fringe and the subtidal are generally the zones that harbour the
most diverse macroalgal communities (largely attributable to rhodophytes). Because of the
limited tidal range in the Arabian Sea and the fact that exposed substrata are subjected to
intense irradiation and wind stress (see Sample sites defined), this study aims at comparing
the well-developed and species-rich plant communities of subtidal habitats.

Introduction and objectives 13
Seagrasses
Besides macroalgae, a few flowering plants have readapted to a marine environment, viz.
mangroves, tidal marsh plants and seagrasses. Of these flowering plants, the seagrasses are
the sole ones that have colonized subtidal marine habitats. A few other flowering plants like
Ruppia spp., however, can also thrive in brackish waters (e.g. blue holes). Seagrasses are
Magnoliophyta that can constitute biologically important seagrass beds, intertidal or subtidal
meadows, serving as (i) a specific biotope for certain coastal biota (e.g. dugong and
seahorses), (ii) a nursing ground for various marine animals (e.g. juvenile fish and
invertebrates) and (iii) an important phorophyte for epiphytic biota. Seagrasses occur on all
continents except Antarctica, with the highest diversity in tropical seas (7 genera versus 5
genera in temperate waters, Phillips & Meñez 1988).
History of phycological research in the Arabian Sea
The first phycologist recognizing the peculiar biogeographic affinities of the Arabian Sea is
Børgesen (1934a). This compilation of species records from Karachi (Pakistan), Okha and
Dwarka (northwestern India) was based on his previous publications, new samples from
Karachi and herbarium collections from the Royal Botanical Gardens, Kew. Upon listing the
species and analyzing their distributions, Børgesen (1934a) concludes: “But I am of opinion
that the discovery of several species so far only known from such far-off regions as
Australia, Japan, Cape and even the northern Atlantic in the northern part of the Arabian Sea
is of considerable plant-geographical interest”. Upwelling occurs in this part of the northern
Arabian Sea during the NE monsoon (Fig. 4), differing in seasonality from the upwelling
areas around Socotra and Masirah. Despite the seasonal differences, characteristic elements
of the Arabian Sea flora are found throughout these upwelling locations [e.g.
Melanothamnus somalensis Bornet & Falkenberg and Nizamuddinia zanardinii (Schiffner)
P.C. Silva]. Besides the macroalgal studies on the eastern coasts (India, Iran and Pakistan) of
the Arabian Sea (Anand 1940, 1943; Børgesen 1930, 1931, 1932a, b, 1933 a, b, 1934 a, b,
1935, 1937 a, b, 1938, 1939), phycological research in the western Arabian Sea was scarce
during the mid twentieth century (Newton 1953) and renewed interest in the region arose in
the two last decades of the century. Since the 1970’s, Pakistani and Indian researchers
remained very productive in describing their macroalgal flora, its ecology and
phycochemical aspects (e.g. Nizamuddin 1964; Nizamuddin & Gessner 1970; Nizamuddin
& Begum 1973; Shameel 1978; Moazzam & Shameel 1985; Aliya & Shameel 1999; Hayee-
Memon & Shameel 1999). In the western Arabian Sea, a continuation of the three basic
taxonomic papers on Yemeni macroalgae (Banaimoon 1986, 1988; Wynne & Banaimoon
1990) resulted in the first comprehensive ecological study on intertidal macroalgal
assemblages of an upwelling area within the Arabian Sea (Hadramout coast of Yemen,
Ormond & Banaimoon 1994). The study reports on a marked seasonal pattern in algal
growth and a clear zonation from the upper to the lower intertidal. These findings have been
republished in a different format as Banaimoon (1998). At the same time an ecological
research team, headed by L. Barratt (Barratt et al. 1984, 1986), investigated the upwelling
regions of the Arabian Sea where they consulted the phycologists S. Hiscock, M.
Nizamuddin and M.J. Wynne. Especially the cooperation with Wynne proved to be fruitful
and resulted in several taxonomic publications on Omani algae (Wynne & Jupp 1998;
Wynne 1999a, b, 2000, 2001; Wynne & Leliaert 2001). The resulting plethora of new
records and the description of many new species and genera indicated that the area was

14 Chapter 1
largely understudied, and that it harbours a rich and unique flora within the Indian Ocean.
Wynne (2000) stressed the biogeographic links of the Omani flora with Japan, as proposed
by Børgesen (1934a), by recording eight disjunctly distributed taxa between both regions.
Socotra Archipelago
The first botanical explorations to the archipelago included small macroalgal collections. In
an investigation of the Natural History of Socotra, sponsored by the British Association for
the advancement of Science, Prof. I.B. Balfour led an expedition to Socotra. His team visited
the island from 11 February-30 March 1880. Many zoological, geological and botanical
collections were made and resulted in the description of over 200 species and 20 genera new
to science. Few algae were collected and these were investigated by Dickie (1888), resulting
in 16 algal species records for Socotra Island. The second published inventory of algae of the
Socotra Archipelago was compiled by Holmes (1903), resulting from a joint British Museum
and Liverpool Museum expedition to Socotra and Abd al-Kuri from 3 December 1897-23
February 1898. This expedition was jointly led by H. Forbes and W.R. Ogilvie-Grant and did
not add a significant number of new records or species to the flora of Socotra. Holmes
(1903) reported 13 macroalgae for Abd al-Kuri. After these intense research efforts at the
end of the 19th century it was over 50 years until the island was again visited by a botanist
(Miller 2002). In the meantime, occasionally enthusiast collectors on ships that frequented
Socotra sampled algae. No publications, however, on any of such sparse collections
appeared. In the late 1990’s, Kemp (1998a) is the first biologist to comment on the peculiar
aspects of the algal flora of the archipelago. Being an ichthyologist, the extensive stands of
the large fucoid Nizamuddinia zanardinii (Schiffner) P.C. Silva drew his attention. He
reported on the distribution of this alga, a monotypic genus endemic to the Arabian Sea,
within the archipelago and noticed differences in the number of productivity peaks and a
temporal shift in the growth cycles between mainland Arabia and Socotra. His research was
part of the preparatory phase of a large project funded by UNDP/GEF. Subsequently,
Leliaert (2000) was the first phycologist studying the marine benthic macroalgae of Socotra.
In the framework of the UNDP/GEF project, he visited the island in January-February 1999
and estimated a number of 260 macroalgal species for the archipelago. Furthermore, Wynne
& Leliaert (2001) reported on a striking green alga, Pedobesia simplex (Kützing) M.J.
Wynne & Leliaert, new to the Indian Ocean. The subsequent field trip from the Phycology
Research Group of Ghent University focused on ecological observations by means of
quadrat sampling, being the subject of this thesis. The preliminary results of the latter field
trip were presented in Schils (2002).
Masirah Island
As previously mentioned, a revival of phycological research in Oman during the late nineties
started with a project of the Darwin Initiative led by L. Barratt. M.J. Wynne has been the
main phycologist in charge of taxonomic issues of her team. This resulted in several
taxonomic publications on the Omani flora, including a number of new species (see History
of phycological research in the Arabian Sea). The seagrass beds off Masirah Island were
included in a study on the distribution, abundance and species composition of Omani
seagrass stands (Jupp et al. 1996). Wynne & Jupp (1998) published a general overview of
macroalgae new to Oman in respect to the Indian Ocean Catalogue of Silva et al. (1996), the
latter not incorporating a publication on the algae of the Gulf of Oman (Cordero 1993).

Introduction and objectives 15
About half (35 out of 71) of the newly recorded species in Wynne & Jupp (1998) were
collected from the vicinity of Masirah (Masirah Island and the Barr al-Hikman Peninsula)
increasing the floristic knowledge of the area substantially. The subsequent communications
on the marine flora of the area consist of two progress reports of the “Oman 99” field trip
(Schils 1999, 2001).
O
BJECTIVES
This study attempts to characterize the marine flora of various localities within the Arabian
Sea by means of species inventories and relevé data. Initially, this project started off as a
case study of the marine plant communities of the Socotra Archipelago and included an
investigation on the seasonality of the biocoenoses. The latter aspect was hampered as the
fieldwork of the UNDP/GEF project ended after the visit in 2001. Since then, SCUBA
facilities were absent and the availability of motorized transport around the archipelago was
limited. As a result, the seasonality study was aborted, but the preceding invitation of the
Ardoukoba Association (France) to participate in a field trip to Masirah Island (Oman)
compensated for this by creating an opportunity for an elaborate biogeographic study within
upwelling areas of the Arabian Sea. The sequel to this “Oman 99” mission to Masirah was
scheduled for September 2001. The goal of the “Oman 2001” field trip was to investigate the
marine biota of the fjords of the Musandam Peninsula (Oman), being a biogeographic and
biological haven for organisms dependent on hard substrata. Musandam is located in the
Strait of Hormuz and connects the Persian Gulf with the Gulf of Oman, both principally
consisting of soft sediments. Due to the unpredictable events following 11 September 2001
and the resulting safety precautions for traveling in the Middle East in the months thereafter,
the envisioned trip was cancelled and the flora of this area could not be included in the
biogeographic analyses. The observations made during both field trips, however, gave a clear
insight in the seasonal appearance of macroalgae during these periods. Communication of
these observations with colleagues was helpful in interpreting seasonal variations in species
occurrences and biomass (e.g. seasonality of the fucoid Nizamuddinia zanardinii, S.C.
Wilson pers. comm.).
Documenting survey data
Prior to the ecological fieldwork, the collection of Leliaert (2000) was studied. These
specimens were categorized and included in the recent Arabian Sea collections. Two databases
(MS Access) were developed for this purpose: “Phycobase” and “SMM relevés”. The former
contains (i) the collection information of the specimens, (ii) an assemblage of the majority of
presently known macroalgal genera and their current systematic position, (iii) tables and
queries of most of the reported macroalgal taxa for nations of the Indian Ocean. This structure
allows for the identification of new species and generic records, the execution of exhaustive
biogeographic comparisons, the generation of systematic listings of genera and species, etc.
Additionally, hyperlinks to web pages are included, in which the diagnosis of the taxon is
given and compared to literature descriptions of closely related taxa. These dynamic web pages
are continuously updated as identifications proceed. The web structure is based on current
systematics and contains links to higher and lower systematical levels, macro- and microscopic
pictures, and personal comments of taxonomists. Currently, 1603 specimens have been entered

16 Chapter 1
in Phycobase, of which 1052 are samples from the Socotra Archipelago and 551 samples from
Masirah Island.
The second database, “SMM relevés”, collates the vegetation relevé data. The forms show
for each sampling site the description, the environmental parameters and the vegetation relevés
as sub-forms. The combined view of all quadrats per station is helpful in having an overview to
make sound adaptations (refined species identifications) to the original field observations. All
data are gathered in 2 tables, facilitating simple and thorough processing by means of various
cross tables (simple statistics, extracting matrices as input for multivariate analyses, etc.).
Taxonomy of the Rhodophyta (see chapters 2-5)
Dependent on the scale, the purpose and the resources, organisms are identified up to a
certain taxonomic level in order to use these taxa as the basic entities in ecological or
biogeographic studies. Generally, “species” are chosen as the basic units for these studies
(see Ecological and biogeographic units: macroalgal and seagrass species). The
identification of species (taxonomy) is therefore an elemental part in applied biological
studies. The investigated sites of this study were all marine and focused on subtidal habitats
(limited intertidal diversity), where the rhodophytes accounted for the highest diversity of the
macroalgal phyla. Moreover, the red algae belonging to the Florideophyceae are the most
diverse macroalgal class, expressed in various distribution and biogeographic patterns on a
global and local scale.
The life cycle of the Florideophyceae is trigenetic, with complex and diverse reproductive
structures and fertilization events in comparison to the Bangio-, Phaeo- and Chlorophyceae.
Fig. 9 shows the life cycle of a Florideophyceae based on Reticulocaulis species from the
Arabian Sea and completed with the tetrasporophyte and young gametophyte stage of the
related Naccaria wiggii (Turner) Endlicher (Boillot & L’Hardy-Halos 1975). Detailed
studies of the reproductive structures and post-fertilization events showed the diagnostic
value of these traits in respect to species identification and systematics (chapters 2, 3). These
characters can also be used in an evolutionary context, serving as character states on
phylogenetic trees based on molecular data. Taxonomic studies on Arabian Sea algae hence
contribute to the knowledge of post-fertilization processes in red algae, especially the
gelatinous red algae of which the gametophytes seem to develop seasonally according to the
changes in day length and other environmental conditions.
Conservation
Historically, the number of marine reserves and the research efforts on marine conservation
lag behind the terrestrial reserves (Sloan 2002). Ecological analyses (chapters 6, 7) are
generally used to give insight into the distribution of species and their interactions on a local
scale. Species-rich and diverse communities are generally considered to be important areas
for conservation, as ecological interactions and community structure are believed to be best
preserved. The occurrence of rare, threatened and endemic species add value to the
proposition of sites for conservation. On a larger scale, the degree of endemism and the
distribution patterns of the occurring species are indicative of the uniqueness and global
importance of marine biocoenoses. Formerly, macroalgae have been rather neglected in
surveys for conservation issues (Walker & Kendrick 1998), which primarily concentrated on
(attractive) marine animals. Recently, scientific recommendations on marine protected areas

Introduction and objectives 17
Fig. 9. Hypothesized life cycle of the genus Reticulocaulis (Rhodophyta; see chapter 3), containing pictures
of the tetrasporophyte phase and a young gametophyte of Naccaria wiggii (Turner) Endlicher. The three
Naccaria figures after Boillot & L’Hardy-Halos (1975). Carpogonium (cp), carposporangium (csp)
gonimoblast initial (gi), hypogynous cell (hy), meiotic division (R!), nutritive cells (nc), tetraspores (tsp)
and trichogyne (tri) are indicated.

18 Chapter 1
try to incorporate all aspects of habitat and biotic diversity (Phillips 1998). In this respect the
present studies (chapters 6, 7) form part of larger holistic projects. During the Ardoukoba
field trip to Masirah Island eleven scientists, mainly taxonomists, visited the island and
focused on the biodiversity of the sampling sites and the different ecosystems. Local experts
and government officials also attended the expedition, hence encouraging local
environmental awareness. The Socotra fieldwork fitted in the framework of the UNDP/GEF
project for conservation and sustainable use of the archipelago. The findings of the vast
number of marine experts (SCDP 2002) have been reported in several project reports. These
included the development of monitoring and zoning plans for the most diverse and unique
biotopes to be implemented by trained locals. These systems should preserve the biodiversity
hot spots of this relatively unspoilt region. In addition, the project serves as a current status
report of the marine biocoenoses and is an excellent reference tool for further environmental
impact studies. In this context, a database has been produced to facilitate future use for the
collected survey data (Apel et al. 2000). Environmental issues threatening both islands are
global warming (extensive coral bleaching has been reported for the Socotra Archipelago
during the El Niño of 1997-1998, Wilkinson 2002), the increase of anthropogenic influence
(intensive fishing, tourism, oil pollution, increase of build up areas, etc.) and invasive species
as transport by sea in the area increases.
Commercial applications
Algae are well-known natural resources in South-East Asia (Prud’homme van Reine &
Trono Jr 2001) and certain other regions (e.g. Brittany, France). In the Middle East,
however, this resource has been practically unexploited. In a prospective study to exploit
these resources, the Oman Seaweed Project (hereafter OSP) analyzed various biochemical
aspects of locally abundant and certain endemic (to the Arabian Sea) macroalgae. The OSP
identified various macroalgae substances, the distribution of economically important species
and data on local utilization. This included an assessment of potentially useful colloid-
bearing species. These polysaccharides (agars, carrageenans and alginates) are valuable
extracts with a multitude of application purposes in the fields of biochemistry,
biotechnology, aquaculture and the food industry. The large Gelidium sp. nov. (previously
referred to as a Ptilophora sp. and Suhria sp.) is locally abundant (up to 100% cover and a
biomass from 0.4 to 0.9 kg m
-2
, with an estimated total of over 300 tonnes for the Arabian
Sea coasts) in intertidal habitats and contains commercially acceptable agar (an agar yield of
18% dry weight and a gel strength of 700-800 g cm
-2
). Furthermore, these Gelidium
populations do not seem to be affected by harvesting as they regenerate from turf-like
clumps. Besides this agarophyte, the carrageenophytes Grateloupia indica Børgesen and
Hypnea bryoides Børgesen are of commercial interest. Both species occur in subtidal
habitats and their cultivation is necessary for the profitable exploitation of these algae. The
OSP proposed the development of an integrated polyculture of macroalgae in aquaculture
farms (fish or shellfish), where the algae help to remove excess waste nutrients (ammonia-N,
P and other effluents). Studies on macroalgal beach cast, thrown up every year by
intermittent storms during post-monsoon months, showed that Nizamuddinia zanardinii has
the highest crude fiber and crude protein contents of the investigated Arabian Sea algae.
Consequently, this endemic alga has a great potential for livestock feed supplementation.
Analyses of the dominant taxa in local beach cast showed that the abundant Sargassum
species contain the highest N contents (equivalent to 13% protein content) of these algae. In
addition, the C:N ratio of Sargassum (9.61) is smaller than 10, being indicative for fast

Introduction and objectives 19
mineralization rates of the plants in composts, making beach cast a promising source for
fertilizer production (OSP 1997, 1999a, b; Jupp 1999).
Few secondary compounds of Arabian Sea algae have been screened so far. Besides the
extracts used in gross quantities (polysaccharides), many seaweeds contain smaller
concentrations of bioactive natural products, often associated with chemical defense against
competitors or herbivores. Such metabolites have antibiotic and feeding deterrent properties
(e.g. bromoform and halogenated acetones in Asparagopsis, Norris & Fenical 1982). The
search for these natural products is largely dependent on taxonomical research for sound
field identifications and the screening of related taxa. Endemic algae seem to be of particular
interest as they have certainly not been screened previously and this natural heritage can
prove to be important for export purposes. This strategy was also applied while collecting
Porifera and Tunicata during the Masirah Island field trip. The biochemical analyses and
bioassays of these animals advance well, but the taxonomical identifications lag behind due
to the limited number of taxonomic experts (Amade 2001). Similarly, a better knowledge of
the Omani marine flora, especially that of the productive upwelling areas, is beneficial for
future biochemical studies on well-defined taxa.
P
ERSONAL CONTRIBUTION TO THE THESIS
The chapters 2-7 are cited as multi-authored publications. The analyses, drawings, field
work, laboratory work, photographs and writing for the chapters 2-4 and 6-7 were, however,
carried out solely by T. Schils. The presented manuscripts were thereafter discussed,
corrected and commented on by the respective coauthors (E. Coppejans, O. De Clerck and
J.M. Huisman). In addition, H. Engledow kindly commented on the manuscripts and checked
the complete English text. Chapter 5 was a study in collaboration with J.M. Huisman during
a research stay in Murdoch University (Western Australia). Certain specimens studied in
chapter 4 were collected by F. Leliaert (Ghent University) during an expedition to Socotra
Island preceding this project (13 January-20 February 1999). These specimens were very
helpful in gaining insight into the specific marine flora. The subsequent collecting trip to
Masirah Island (2-30 November 1999) was executed by T. Schils with the support of the
Ardoukoba Association (France). Vegetation and specimen sampling on Socotra (26 March-
7 May 2000) were also performed by T. Schils, in collaboration with the Senckenberg
Research Institute (Germany) and the personnel of the project implementation unit (UNDP).
The field work comprised largely SCUBA diving, snorkeling, and intertidal collecting. The
procedure of vegetation sampling is explained in the Materials and Methods of chapter 6.
The photographs in this thesis were taken under standard light microscopes with a 35-mm
camera and two types of digital cameras (for further details, see Materials and Methods of
the respective chapters). Drawings were made with a camera-lucida on the microscopes,
upon which they were scanned with an Agfa Snapscan e50. The different dyes that were
used for staining the specimens for microscopical examination are listed in the Materials and
Methods of the chapters 2-5.
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Gelatinous red algae of the Arabian Sea 25
CHAPTER 2
Gelatinous red algae of the Arabian Sea, including Platoma heteromorphum sp. nov.
(Gigartinales, Rhodophyta)
Published as: Schils T. & Coppejans E. 2002. Gelatinous red algae of the Arabian Sea, including
Platoma heteromorphum sp. nov. (Gigartinales, Rhodophyta). Phycologia 41(3): 254-267 (and cover
photo).
ABSTRACT
This study reports on the gelatinous red algae of the Arabian Sea (Masirah Island, Oman and
Socotra Island, Yemen) belonging to the families Dumontiaceae, Nemastomataceae and
Schizymeniaceae. Dudresnaya capricornica, Gibsmithia larkumii, Predaea laciniosa, P.
weldii and Titanophora pikeana are new records for the region. The morphological and
reproductive features of these species are presented, with emphasis on post-fertilization
events. Platoma heteromorphum Schils sp. nov. is described from an upwelling region along
the eastern coast of Masirah Island. Based on similarities in morphology and post-
fertilization events, this species is closely related to P. ardreanum, P. cyclocolpum (the
generitype) and P. izunosimense. The connecting filament initiation in P. heteromorphum is
comparable to Titanophora, but the post-fertilization processes observed in P.
heteromorphum and T. pikeana clearly demarcate both genera within the Schizymeniaceae.
A first impression of the gelatinous red algae in the Arabian Sea suggests a high
biogeographical affinity with Australia, but additional records from the Indian Ocean
indicate that their distribution may be more widespread than is currently accepted.
I
NTRODUCTION
The study of the benthic marine algal flora of the Arabian Sea started with Børgesen (1934),
who stressed the peculiar composition of the algal flora relative to adjacent areas and
suggested biogeographical links with distant regions, e.g. Australia, Japan, South Africa and
the northern Atlantic. Renewed interest in the phycology of this region occurred in the
1990s, resulting in various new records and new species descriptions (Wynne & Banaimoon
1990; Kemp 1998; Wynne & Jupp 1998; Wynne 1999a, b, 2000, 2001). Despite the recent
increase in taxonomic studies in the northern Indian Ocean (Djibouti, India, Iran, Laccadive
Islands, Maldives, Oman, Pakistan, Socotra, Somalia, Yemen), information on the gelatinous
red algae of the region remains scarce (Holmes 1903; Silva et al. 1996). For each of the
families (Dumontiaceae, Nemastomataceae and Schizymeniaceae) we studied in this paper,
only a single species has previously been recorded for the northern Indian Ocean, viz.
Dudresnaya japonica Okamura (Oman: Wynne 2000), Predaea feldmannii Børgesen var.
indica M.S. Balakrishnan & Chawla (India: Balakrishnan & Chawla 1984) and Schizymenia
apoda (J. Agardh) J. Agardh (Somalia: Hauck 1889).

26 Chapter 2
MATERIAL AND METHODS
Specimens were collected by the first author during field trips to the islands of Masirah,
Oman (November 1999) and Socotra, Yemen (March–May 2000). Specimens were collected
in plastic zip-lock bags during SCUBA dives and afterwards pressed as herbarium specimens
(lodged in GENT: Ghent University Herbarium, Krijgslaan 281 (S8), 9000 Ghent, Belgium)
or preserved in a 5% formaldehyde–seawater solution or dried in silica gel.
After staining of specimens with Aniline Blue, Fast Green or Lugol’s solution, slides were
made by mounting the specimens in a 50% corn syrup-water solution (containing a few
drops of phenol). Subsequently, the samples were studied using a light microscope (Leitz
Diaplan). ImageTool 2.00 (The University of Texas Health Science Center in San Antonio,
Texas) and a digital camera (Olympus DP50) were used for microscopical measurements,
which are presented in the text as length × width.
R
ESULTS
Dudresnaya capricornica Robins & Kraft 1985, p. 23 (Dumontiaceae)
Figs 1–4
SPECIMENS EXAMINED: Yemen: Socotra, east of Bidholih (ALG-41: 12°19'19''N, 54°02'2''E),
1 May 2000, subtidal: –19.4 m, leg. T. Schils (SMM 480).
DISTRIBUTION: Australia, Norfolk Island, Papua New Guinea, Saudi Arabia, Tanzania,
Yemen [Robins & Kraft 1985; Huisman & Walker 1990; De Clerck & Coppejans 1996 (as
Dudresnaya sp. det. A. Millar, 14 August 1998); Silva et al. 1996; Huisman 1997; Phillips
1997; Millar et al. 1999; Coppejans et al. 2000; Tai et al. 2001; this paper].
Plants are bright red plant with a terete thallus (11 cm tall; Fig. 1) and grow epilithically.
Axial cells are marked by the presence of longitudinally elongated hexagonal protein crystals
(8.5–17 µm × 2–4.5 µm) which are visible using bright field optics (Fig. 2) or ultraviolet
fluorescence. Initially, the distinct primary axes produce cortical filaments in a secund
arrangement, resulting in an irregular multiple branching pattern. The outer cortical cells are
cylindrical (5.5–40 µm × 2–9 µm) and hairs are absent. Rhizoids (3.5–15 µm in diameter)
develop from the basal cells of the cortical filaments.
A single female gametophyte was collected. The reproductive filaments lack a
mucilaginous coat. The carpogonial filaments consist of 8–22 cells, with a terminally
deflexed carpogonium (4.5–9.5 µm × 5.5–8.5 µm) resulting from a single oblique division.
The trichogyne can reach a length of 0.5 mm. The auxiliary-cell filaments consist of 8–40
cells, with a subspherical to rectangular generative auxiliary cell (8.5–12 µm × 8.5–13 µm)
situated amongst large, dark-staining cells. Adventitious laterals and rhizoids develop from
carpogonial and auxiliary-cell filaments. Fusion of the connecting filament with the auxiliary
cell causes the latter to swell and form a bulge at the site of contact, resulting in a latero-
pyriform shape (18–27 µm × 22–35 µm). Three gonimoblast initials are formed. Two are
recurved (reniform) (13.5–19 µm × 7–11 µm) and the third is generally larger and reniform
to subspherical (Figs 3, 4). These gonimoblast initials give rise to an uncleft cystocarp (up to
265 µm in diameter) that completely encircles the auxiliary-cell filaments. Carposporangia
reach a diameter of 9.5–17 µm.

Gelatinous red algae of the Arabian Sea 27
REMARKS: Of the 17 currently recognized Dudresnaya P. & H. Crouan species (Robins &
Kraft 1985; Searles & Ballantine 1986; Kajimura 1993, 1994; Tabares et al. 1997; Afonso-
Carrillo et al. in press), D. hawaiiensis R.K.S. Lee is the only well documented species for
the Indian Ocean (South Africa: Norris 1992). Wynne (2000) reported on D. japonica from
the Dhofar coastline of Oman and commented on the ill-defined mucilage coat surrounding
the auxiliary-cell filament and the cystocarps being indistinctly cleft. Robins & Kraft (1985)
use the latter feature to classify Dudresnaya species into two groups. Our specimen, from
Socotra, agrees with D. japonica as described by Wynne (2000), but it should be referred to
D. capricornica owing to its irregular radial branching, the absence of a thick mucilaginous
coat around the reproductive filaments, the reniform gonimoblast initials, and cystocarps that
completely surround the auxiliary-cell filaments. Future studies should elucidate the species
diversity and the variability of the genus in the region.
Figs 1–4. Dudresnaya capricornica.
Fig. 1. Habit of a female gametophyte, SMM 480. Scale bar = 2 cm.
Fig. 2. Axial cell, showing a single longitudinally elongated hexagonal protein crystal (arrow). Slide
SMM 480f. Scale bar = 25 µm.
Figs 3, 4. Two reniform (rgi) and a third larger subspherical to reniform gonimoblast initial (sgi)
developing from a diploidized auxiliary cell (aux), with incoming and outgoing connecting filaments
(arrowheads). Slide SMM 480d. Scale bars = 25 µm.
Figs 5, 6. Gibsmithia larkumii.
Fig. 5. Habit of a female gametophyte, SMM 496. Scale bar = 2 cm.
Fig. 6. Carpogonial filament bearing two carpogonia (arrows). Slide SMM 496a. Scale bar = 10 µm.

28 Chapter 2
Gibsmithia larkumii Kraft 1986, p. 439 (Dumontiaceae)
Figs 5, 6
SPECIMENS EXAMINED: Yemen: Socotra, Qatanhin, Permanent Transect IX (ALG-23:
12°21'18''N, 53°32'40''E), 9 April 2000, subtidal: –10.5 m, leg. T. Schils (SMM 257);
Socotra, east of Bidholih (ALG-41: 12°19'19''N, 54°02'02''), 1 May 2000, subtidal: –19.4 m,
leg. T. Schils (SMM 496, SMM 497). Tanzania: Ruvula Beach (Mnazi Bay, Mtwara area),
26 July 2000, subtidal: –20 m, leg. E. Coppejans, O. Dargent & G. Bel (HEC 12898); Ruvula
Beach, in front of the lodge (Mnazi Bay, Mtwara area), 7 August 2000, subtidal: –25 m, leg.
E. Coppejans, O. Dargent & G. Bel (HEC 14197).
DISTRIBUTION: Australia, Papua New Guinea, Tanzania, Yemen (Kraft 1986; Millar et al.
1999; this paper).
Thalli are bright red, gelatinous, up to 7 cm tall and 8.5 cm broad (Fig. 5). They are attached
by a cartilaginous disc (0.5 cm in diameter), which lacks the characteristic perennial stipe of
other species of Gibsmithia Doty. The pseudodichotomous cortical filaments consist of
subrectangular cells (5–35 µm × 2.5–9 µm). Apical cortical cells are blunt, lacking terminal
hairs. Inner cortical cells give rise to medullary filaments, 2.5–8.5 µm in diameter.
The unfertilized female gametophytes contain carpogonial filaments (6–12 cells long) with
an enlarged subterminal hypogynous cell, which initiates a carpogonium by an oblique
division. The occurrence of two carpogonia on a single carpogonial filament was scarcely
ever observed (Fig. 6). Auxiliary-cell filaments are 6–13 cells long. The subrectangular
auxiliary cell is flanked by two enlarged, deeply staining cells. Adventitious laterals and
rhizoidal filaments develop to various extents on carpogonial and auxiliary-cell filaments.
Tetrasporophytes bear obovoid, cruciate tetrasporangia (16–29 µm × 11–23 µm) terminally
on the cortical filaments.
This alga was sampled from the site with the highest species diversity yet found in the
Socotra Archipelago (30 ± 2 species per 0.25 m
2
). Very strong currents were observed
around this eastern extremity of Socotra. The rocky substratum contained a high diversity of
red algae, intermixed with bare sandy patches.
REMARKS: Two other Gibsmithia species have previously been recorded for the Indian
Ocean: G. hawaiiensis Doty (Australia, Kenya, Seychelles and Tanzania: Silva et al. 1996;
Coppejans et al. 2000) and a Gibsmithia sp. from Zanzibar, Tanzania (Coppejans et al.
2000). We have recently recollected both species in Tanzania (Mnazi Bay), indicating that
the lack of Gibsmithia records for the Indian Ocean most probably results from the lack of
subtidal phycological studies in this area.
Platoma heteromorphum Schils, sp. nov. (Schizymeniaceae)
Figs 7–17
Plantae atrorubrae foliosae ad subcylindricae. Hapteron discoideum (1 mm crassum), stipite
brevi (6–9 mm longo). Cortex 4–8 cellulis externis corticalibus, numerosas intercalares
glandicellulas continentibus, cellulis internis corticalibus elongatis (includentibus cellulas
X- et V-formes) filamenta medullosa edentibus. Interdum cellulae steriles in ramis
carpogonialibus tricellularibus praesentes. Carpogonium post fecundationem
longitudinaliter dimidiatum, ambo dimidia ad contiguas cellulas auxiliares subsidiarias

Gelatinous red algae of the Arabian Sea 29
conjugentia. Una ex quibus et una cellula distalis producentes filamenta conjunctiva septata
directe. Cellulae auxiliares generativae intercalares in fasciculis corticalibus separatis,
perspicuae forma obpyriformi (16–21 µm longae et 11–13 µm crassae) et coloratae
atrocyaneae. Post conjunctionem laterale fili conjunctivi cum cellula auxiliari generativa,
illa crescens porrecto et peragrans. Cellula auxiliaris diploidea in prima cellula
gonimoblasti (6.5–9.5 µm longa et 6–10 µm crassa) transverse dividens. Duo gonimolobos
producens, maturescentes sequenter et produscentes carposporangia angulares (11.5–30 µm
diametro). Tetrasporangia et spermatangia incognita.
Deep red plants, foliose to subcylindrical in shape. Multiple blades with short stipes (6–9
mm long) arise from a single discoid holdfast (1 mm across). Cortex consists of 4–8 outer
cortical cells, containing numerous intercalary gland cells, and an inner layer of elongated
cells (including X- and V-shaped cells) giving rise to medullary filaments. Three-celled
carpogonial branches occasionally bear sterile cells. The fertilized carpogonium divides
longitudinally into two halves, fusing with adjacent subsidiary auxiliary cells. One of the
diploidized subsidiary cells and the cell distal to it initiate septate connecting filaments
directly. Generative auxiliary cells are formed in an intercalary position in separate cortical
filaments and are characterized by their obpyriform shape (16–21 µm × 11–13 µm) and a
deep aniline staining. After lateral fusion of a connecting filament with a generative auxiliary
cell, the former continues to grow and effects further diploidizations. The diploidized
generative auxiliary cell divides transversely, producing a conical gonimoblast initial (6.5–
9.5 µm × 6–10 µm). Two gonimolobes are formed, which mature sequentially and produce
angular carposporangia (11.5–30 µm in diameter). Tetrasporangia and spermatangia
unknown.
HOLOTYPE: MAS 139, upper left specimen on herbarium sheet (field picture: Fig. 7).
ETYMOLOGY: The specific epithet alludes to the combination of compressed and
subcylindrical parts of the thallus.
TYPE LOCALITY AND SPECIMENS EXAMINED: Oman: Masirah Island, close to Ra’s Zarri (site
09: 20°11'85''N, 58°42'55''E), 9 November 1999, subtidal: –9 m, leg. T. Schils (MAS 139).
Species-rich algal flora, dominant species are Spatoglossum asperum J. Agardh, Sebdenia
flabellata (J. Agardh) P.G. Parkinson, Dictyota spp. and Padina spp. Rocky platform with
grooves and rocky outcrops; Masirah Island, Close to Ra’s Zarri (site 22), 20 November
1999, subtidal: –9 m, leg. T. Schils (MAS 374) (holotype).
The plants are up to 8.5 cm tall, deep red in colour (bright red when dried) and gelatinous in
texture (Fig. 7). A distinctive feature of the species, consistent with the most recent
etymological interpretation of Platoma Schousboe ex Schmitz (‘becoming wide’:
Athanasiadis 2000), is the flattened subcylindrical thallus shape with irregular lobes (cf.
certain Nemastoma J. Agardh and Predaea De Toni spp.), which do not fuse. The thallus
occasionally has surface proliferations, but lacks marginal calluses. There is a short stipe (6–
9 mm), attached by a small discoid holdfast, 1 mm across.

30 Chapter 2
Figs 7–17. Platoma heteromorphum.
Fig. 7. Habit of female gametophytes, including the holotype (arrow), MAS 139. Scale bar = 2 cm.
Fig. 8. Large intercalary gland cell (arrow) in the inner cortex. Slide MAS 139x. Scale bar = 25 µm.
Fig. 9. A three-celled carpogonial branch consisting of an oval basal cell (bc), a subrectangular
hypogynous cell (hy) and a conical carpogonium (cp). The supporting cell (sc) bears two subsidiary
auxiliary cells (sac). Slide MAS 139x. Scale bar = 25 µm.
Fig. 10. Longitudinal division of the fertilized carpogonium and fusion of both halves (arrowheads)
with the adjacent subsidiary auxiliary cells. One diploidized subsidiary auxiliary cell (sac1) and the
cortical cell distal to it (cc) initiate septate connecting filaments (arrows) directly. Slide MAS 139af. Scale
bar = 25 µm.

Gelatinous red algae of the Arabian Sea 31
Fig. 11. Both halves of a divided carpogonium fuse (arrowheads) with the subsidiary auxiliary cells
(sac). The connecting filaments (arrows) arise from one of the subsidiary auxiliary cells and branch
profusely. Supporting cell (sc), hypogynous cell (hy) and cortical cells (cc) are indicated. Drawing from
slide MAS 139af. Scale bar = 25 µm.
Fig. 12. Undiploidized generative auxiliary cell (arrow) in an intercalary position in a cortical filament.
Slide MAS 139ae. Scale bar = 50 µm.
Fig. 13. Incoming and outgoing septate connecting filaments (arrowheads) on a fertilized generative
auxiliary cell, which protrudes distally (arrow). Slide MAS 139p. Scale bar = 25 µm.
Fig. 14. A transverse division of the diploidized generative auxiliary cell results in a conical gonimoblast
initial (arrow). Slide MAS 139p. Scale bar = 10 µm.
Fig. 15. An oblique division of the gonimoblast initial (gi) gives rise to the first gonimolobe initial
(gli1). Slide MAS 139p. Scale bar = 10 µm.
Fig. 16. Development of gonimoblast cells (arrowheads) from the first gonimolobe initial (gli1), on top
of the gonimoblast initial (gi). Slide MAS 139p. Scale bar = 10 µm.
Fig. 17. The gonimoblast initial (gi), the primary gonimolobe initial (gli1) and an inner gonimoblast cell
(arrowhead) are perceptible as large, globose cells in a maturing carposporophyte. A second
gonimolobe (arrow) develops from the secondary gonimolobe initial (gli2). Slide MAS 139f. Scale bar =
25 µm.
The moniliform outer cortex consists of discrete, dichotomous branch systems that are 4–8
cells long with blunt apices. The inner cortical cells are elongate and include X- [cf. P.
abbottianum J.N. Norris & Bucher (1977) and P. izunosimense Segawa (Kajimura 1997)]
and V-shaped cells (cf. Itonoa: Masuda & Guiry 1995); they initiate rhizoidal filaments. In
accordance with the other well studied Platoma species (Kraft & Abbott 1997), the cortical
fascicles contain intercalary and subterminal subspherical gland cells (6.5–40 µm in
diameter), which stain deeply with Aniline Blue. Certain gland cells close to the inner cortex
become very large (Fig. 8). The cell content of small gland cells is dense and that of the large
gland cells is coagulated and contains a single large spherical protein inclusion (3.5–15 µm
in diameter).
Only dioecious female gametophytes were observed. The carpogonial branches (Fig. 9)
develop at the terminal end of an inner cortical cell (an apically depressed obovate
supporting cell, 15–18 µm × 12–15.5 µm), positioned in the dichotomy of a cortical fascicle.
The three-celled carpogonial branches consist of an oval basal cell (4.5–9 µm × 9.5–12 µm),
a subrectangular hypogynous cell (3–5 µm × 8.5–10.5 µm), and a distal carpogonium
(conical in shape, 9–10.5 µm × 6–8 µm) with a straight trichogyne that is some 0.2 mm long.
Occasionally, sterile cells were noticed on the basal and hypogynous cells. The two cortical
cells on top of the supporting cell become subsidiary auxiliary cells (or epi-supporting cells,
13.5–22.5 µm in diameter; Fig. 9). Following presumed fertilization, the carpogonium
divides longitudinally and both halves fuse with the adjacent subsidiary auxiliary cells (Fig.
10). One diploidized subsidiary auxiliary cell and the cortical cell distal to it then initiate
septate connecting filaments directly; these filaments branch abundantly near their site of
origin (Fig. 11). By traversing the thallus, the connecting filaments can ultimately fuse with a
generative auxiliary cell. The latter cells are formed in an intercalary position in cortical
filaments separate from those containing supporting cells. Prior to fusion with connecting
filaments, these generative auxiliary cells (16–21 µm × 11–13 µm) differ from normal
vegetative cells by their obpyriform shape and their dark staining with Aniline Blue (Fig.
12). Most connecting filaments continue to grow from the point of contact with the
generative auxiliary cell, giving rise to a crescent-shaped lateral extension on the auxiliary
cell. Upon diploidization, the generative auxiliary cell protrudes distally (Fig. 13) and
divides transversely to form a conical gonimoblast initial (6.5–9.5 µm × 6–10 µm; Fig. 14).
A subsequent oblique division of the gonimoblast initial forms the first gonimolobe initial

32 Chapter 2
(6–9 µm × 7–9 µm; Fig. 15), which continues to divide (Fig. 16) to produce the first
gonimolobe. A second gonimolobe initial (Fig. 17) develops later and the resulting
gonimolobe matures sequentially. The gonimoblast initial, the primary gonimolobe initial
and inner gonimoblast cells are discernible as large globose cells (17–22 µm in diameter;
Fig. 17) in the mature nonostiolate cystocarp (90–210 µm in diameter). The angular
carposporangia are 11.5–30 µm in diameter. During cystocarp development, the cortical
filament cells adjacent to the generative auxiliary cell enlarge and elongate to some extent.
REMARKS: Platoma heteromorphum fits the generic definitions of female reproductive
structures and postfertilization events presented by Masuda & Guiry (1994). The presence of
gland cells and subsidiary auxiliary cells, together with various morphological features
(Norris & Bucher 1977; Kajimura 1997; Kraft & Abbott 1997) clearly demarcates the Omani
species from less studied species, such as P. abbottianum, P. australicum Womersley &
Kraft, P. fanii Dawson, P. foliosum Womersley & Kraft, P. incrassatum Schousboe ex De
Toni and P. tenue Howe & Taylor. Its morphology and especially the postfertilization events
(Table 1) differ from the well documented (Itono 1984; Kajimura 1997) Japanese species, P.
izunosimense. In that species, the fertilized carpogonium does not divide in two but fuses
with one or both subsidiary auxiliary cells or a cortical cell distal to one of the latter. A
monopodial connecting filament–initial branch then initiates the connecting filaments
indirectly. Compared to P. ardreanum Kraft & Abbott (1997), P. heteromorphum lacks the
distinctive calluses and blade ruffling and has a stipe. Some carpogonial branch cells bear
sterile cells, as in P. ardreanum. Multicellular laterals and sterile cells on the supporting or
epi-supporting cells were not observed, however, but cannot be said never to occur, because
carpogonial branches with sterile cells were scarce in the material. Like the Hawaiian
species, the fertilized carpogonium divides into two halves, which fuse with the adjacent
subsidiary auxiliary cells. Conversely, the connecting filament initiation in P.
heteromorphum is not restricted to a subsidiary auxiliary cell. Besides the morphological
differences (stipe, surface proliferations), these postfertilization events also distinguish the
new Platoma species from P. cyclocolpum (Montagne) F. Schmitz, the type of the genus. In
P. cyclocolpum, the fertilized carpogonium can fuse with one or two subsidiary auxiliary
cells (Masuda & Guiry 1994; Huisman 1999) and the connecting filaments can develop from
both fusion cells and supplementary cortical cells. Itono (1984) observed that connecting
filaments in Titanophora (J. Agardh) Feldmann also arose from the cell distal to one of the
two subsidiary auxiliary cells. In this respect, P. cyclocolpum, P. heteromorphum and P.
izunosimense illustrate close similarities in postfertilization events between Platoma and
Titanophora.
Predaea laciniosa Kraft 1984, p. 11 (Nemastomataceae)
Figs 18–27
SPECIMENS EXAMINED: Oman: Masirah Island, in between Ra’s Abu Rasas and Ra’s Zarri
(site 25), 22 November 1999, subtidal: –11 m, leg. T. Schils (MAS 530). Yemen: Darsa
Island, south coast (ALG-21: 12°06'36''N, 53°17'48''E), 8 April 2000, subtidal: –21 m, leg.
T. Schils (SMM 209). Rocky platform with large concave grooves (vertical walls and
obscured areas); abundance of soft corals.

Gelatinous red algae of the Arabian Sea 33

34 Chapter 2
DISTRIBUTION: Australia, French Polynesia, Hawaii, Oman, Papua New Guinea, Yemen
(Kraft & Abbott 1971; Kraft 1984; Huisman 1997; Abbott 1999; Millar et al. 1999; Payri et
al. 2000; this paper).
The plants are small, up to 1.8 × 2.5 cm, and grow on coralline red algae and shell debris
(Fig. 18). Four to eight oval, outer cortical filament cells (3–9 µm × 2–5 µm) originate from
elongated subcortical cells. Large spherical gland cells (12–24 µm × 10–21 µm) are
prominent, and are intercalary or terminal in cortical filaments. Rhizoidal filaments develop
from the inner cortical cells and constitute the medulla, their cells 5–280 × 2–3 µm.
Only dioecious female gametophytes were collected. Although were observed at different
stages of development, carpogonial branches were absent. The cortical filament cells (7–14
µm × 3–6 µm), attached to the auxiliary cell (21–26 µm × 9–14 µm; Fig. 19), bear
aggregations (generally 4 branching tiers, each consisting of 3–15 cells) of small
subspherical nutritive cells (2–5 µm × 2.5–7 µm). Connecting filaments fuse baso-laterally
with the auxiliary cell. The incoming connecting filament initiates a bulge (Fig. 20), which
gives rise to a gonimoblast initial (Fig. 21) opposite to the site of contact with the auxiliary
cell. The gonimoblast initial swells, becoming subspherical (reaching a size of 6.5–18 µm in
diameter) and cutting off the primary gonimolobe initial (Fig. 21). The resulting gonimoblast
cells divide profusely and initiate a large subspherical primary gonimolobe (up to 180 µm ×
220 µm). The remains of the incoming connecting filament are visible as a spine-like
protuberance on the auxiliary cell (Figs 24, 25). Secondary (Fig. 23) and tertiary
gonimolobes (Fig. 26) are initiated sequentially, lateral to the first gonimolobe. The
subspherical to isodiametric carposporangia (5–13 µm in diameter) mature asynchronously
and small clusters of secondary and tertiary carposporangia are evident at the base of the
prominent primary gonimolobe (Fig. 27).
REMARKS: The Arabian Sea specimens lacked the ruffled surface originally thought
characteristic of P. laciniosa (Kraft 1984). Predaea tokidae Kajimura differs from P.
laciniosa by having a lobed thallus without surface ruffles. Besides this difference in habit,
the vegetative structure and reproductive traits of both species are remarkably similar
(Kajimura 1987, 1995). Since P. laciniosa would have priority over P. tokidae if the two
species were combined, and since our observations of Omani and Socotran specimens are
completely consistent with the description of P. laciniosa (Kraft 1984), apart from the
ruffled surfaces, MAS 530 and SMM 209 are identified as P. laciniosa; an additional feature
in favour of this identification is the presence of three gonimolobes in the Arabian Sea
specimens. The high degree of morphological variability in these gelatinous red algae, the
disjunct distribution pattern of P. laciniosa, and the floristic affinity between the northern
Arabian Sea and the Sea of Japan (Børgesen 1934; Wynne 2000) may be indicative of a
greater distribution range of the species than currently accepted. Detailed studies on P.
tokidae and P. laciniosa should clarify the morphological and developmental differences
between both species.

Gelatinous red algae of the Arabian Sea 35
Figs 18–27. Predaea laciniosa.
Fig. 18. Habit of a female gametophyte, MAS 530. Scale bar = 1 mm.
Fig. 19. Nutritive cells (arrowheads) and an undiploidized generative auxiliary cell (arrow) in an
intercalary position in a cortical filament. Slide SMM 209b. Scale bar = 25 µm.
Fig. 20. Diploidized auxiliary cell with (laterally) an incoming connecting filament (icf), initiating a
bulge (bu) prior to gonimoblast initiation. The contiguous cortical cells (arrows) of the auxiliary cell
bear nutritive cells (arrowheads). Slide SMM 209a. Scale bar = 10 µm.
Fig. 21. The gonimoblast initial (arrowhead) and the gonimolobe initial (arrow) arise outwardly from
the connecting filament bulge. Slide SMM 209b. Scale bar = 5 µm.
Fig. 22. Development of the first gonimolobe (arrow). Slide SMM 209a. Scale bar = 10 µm.
Fig. 23. Initiation of a secondary gonimolobe (arrow) from the gonimoblast initial (arrowhead). Slide
SMM 209a. Scale bar = 25 µm.

36 Chapter 2
Fig. 24, 25. Prominent spike-like projection on the auxiliary cell (arrow), representing the remains of
the connecting filament. Slide SMM 209a. Scale bar = 10 µm.
Fig. 26. Development of a tertiary gonimolobe (arrow) on the side of the gonimoblast initial
(arrowhead). Slide SMM 209a. Scale bar = 25 µm.
Fig. 27. Sequentially maturing secondary carposporangia (arrow) at the base of the primary
gonimolobe. Slide SMM 209a. Scale bar = 50 µm.
Predaea weldii Kraft & I. A. Abbott 1971, p. 194 (Nemastomataceae)
Figs 28–35
SPECIMENS EXAMINED: Oman: Masirah Island, Coral Garden (site 01: 20°10'15''N,
58°37'80''E), 3 November 1999, subtidal: –3 m, leg. T. Schils (MAS 002); Masirah Island, 6
November 1999, subtidal, leg. A. Couté (MAS 077); Masirah Island, around the rock (site
07: 20°12'51''N, 58°36'87''E), 8 November 1999, subtidal: –8 m, leg. T. Schils (MAS 111).
Platforms with dominant Spatoglossum asperum vegetations. Many P. weldii specimens
growing on the boulders of the rocky platform.
DISTRIBUTION: Australia, Fiji, Hawaii, Oman, Papua New Guinea, Puerto Rico, South
Africa, Venezuela (Kraft 1984; Millar 1990; N’Yeurt et al. 1996; Ballantine & Aponte 1997;
Huisman 1997; Phillips 1997; Abbott 1999; Coppejans & Millar 2000; Huisman 2000; De
Clerck et al., in press; this paper).
Thalli are bright red, mucilaginous and foliaceous, with numerous blunt, tapering branchlets,
and grow up to 12 cm tall (Fig. 28). The pseudodichotomous cortical filaments consist of
12–21 rectilinear cells (11–17 µm × 3.5–5.5 µm), some producing rhizoidal filaments. Inner
cortical cells measure 20–75 µm × 5–12 µm. Gland cells are absent. Medullary filaments
vary in size from 28–205 µm × 2–5 µm.
Three-celled carpogonial branches (Fig. 29) develop from a cortical filament cell (the
supporting cell, 10.5–19 µm × 5.5–7.5 µm). The basal cell is cylindrical in shape (6.5–13.5
µm × 4–6.5 µm), the hypogynous cell subspherical (5.5–9 µm × 4.5–7 µm); the conical
carpogonium has a blunt distal end (9.5–13 µm × 3.5–5 µm) and bears a straight terminal
trichogyne. After presumed fertilization, the zygote enlarges and divides transversely (Fig.
30). The basal part then produces connecting filaments prior to the degeneration of the
trichogyne (Fig. 30). Throughout the thallus, the branched connecting filaments occasionally
develop small cells (Fig. 31) that give rise to multiple connecting filaments extending out in
all directions. The auxiliary cell develops in an intercalary position in a cortical filament and
is often uteriform in shape (16.5–22.5 µm × 9–13 µm). Small aggregations [1–4 tiers, each
consisting of 1–2(–3) cells] of large spherical nutritive cells (5.5–10 µm in diameter) are
attached to the cortical cell, subtending the auxiliary cell and the distal two cortical cells that
originate from it (Figs 30, 31). After the fusion of a connecting filament at the basal side of
an auxiliary cell, the latter protrudes terminally (Fig. 31; 24–37.5 µm × 9.5–14 µm) and
divides transversely at its terminal end, initiating a gonimoblast initial (7–10 µm in diameter;
Fig. 32). This is followed by a distal transverse division of the gonimoblast initial, giving
rise to the primary gonimolobe initial (Fig. 32). The latter divides first transversely and then
twice obliquely (perpendicular to one another) to develop the first gonimoblast cells. These
cells continue to divide along different axes and constitute the first gonimolobe. Secondary
and tertiary gonimolobes (Figs 33, 34) develop sequentially from the sides of the
gonimoblast initial, but the carposporangia (up to 12 µm in diameter) mature synchronously.

Gelatinous red algae of the Arabian Sea 37
During cystocarp development the cells bearing the nutritive cell aggregations stain deeply
with Aniline Blue and enlarge, and the pit connections towards the auxiliary cell expand.
Figs 28–31. Predaea weldii.
Fig. 28. Habit of a female gametophyte, MAS 002. Scale bar = 2 cm.
Fig. 29. In an intercalary position in a cortical filament, a supporting cell (arrow) bears a three-celled
carpogonial branch consisting of a cylindrical basal cell (bc), a subspherical hypogynous cell (hy) and a
conical carpogonium (cp) with a straight terminal trichogyne (tri). Slide MAS 002b. Scale bar = 25 µm.
Fig. 30. Upon enlargement, the fertilized carpogonium divides transversely (arrowhead) and the basal
part initiates connecting filaments (arrow). The trichogyne (tri) remains perceptible on the distal part of
the carpogonium. The cortical filament supports a carpogonial branch as well as an undiploidized
auxiliary cell (aux). The cortical cells adjacent to the auxiliary cell bear large subspherical nutritive cells
(nc). Slide MAS 111a. Scale bar = 25 µm.
Fig. 31. Small cells (arrows), in an intercalary position in connecting filaments, give rise to multiple
connecting filaments that branch throughout the thallus and diploidize auxiliary cells. The diploidized
auxiliary cells protrude distally (arrowheads) before gonimoblast initiation. Slide MAS 002b. Scale bar =
25 µm.
REMARKS: The Omani material differs from the original description of P. weldii (Kraft &
Abbott 1971) in the transverse division of the zygote prior to connecting filament initiation.
Millar & Guiry (1989) discussed this feature in P. kraftiana and noted that Lemus &

38 Chapter 2
Ganesan (1977) depicted this trait for P. weldii, without mentioning it. Previous doubts
(Kraft & Abbott 1971; Kraft 1984; Millar & Guiry 1989) concerning the conspecificity of P.
pusilla and P. weldii were clarified by Verlaque (1990), who showed that the difference in
gonimoblast initiation (lateral versus terminal) is the main diagnostic feature separating these
species. Our Omani P. weldii specimens were gathered during the same season as when the
species is abundant in eastern Australia (Kraft 1984).
Figs 32–35. Predaea weldii.
Fig. 32. A diploidized auxiliary cell (aux) with an incoming connecting filament (icf) laterally. Two
subsequent transverse divisions of the diploidized auxiliary cell originate in a gonimoblast initial (arrow)
and the first gonimolobe initial (arrowhead). Slide MAS 002b. Scale bar = 25 µm.
Figs 33, 34. Development of a secondary (gl2) and tertiary gonimolobe (gl3) from the gonimoblast
initial (arrows). Slide MAS 002a. Scale bar = 25 µm.
Fig. 35. Carposporophyte with synchronously maturing gonimolobes. Slide MAS 002a. Scale bar = 25
µm.
Titanophora pikeana (Dickie) Feldmann 1942, p. 111 (Schizymeniaceae)
Figs 36–44
SPECIMENS EXAMINED: Yemen: Socotra, west of Rhiy di-Diblih (ST-021: 12°19'31''N,
53°59'59''E), 12 March 1999, subtidal: –6 m, leg. F. Leliaert (SOC 347); Socotra, Steroh
(ST-037: 12°19'00''N, 53°52'51''E), 14 March 1999, subtidal: –15 m, leg. F. Leliaert (SOC
356); Socotra, east of Qatanhin, Quray (ALG-22: 12°18'55''N, 53°37'23''E), 9 April 2000,
subtidal: –17 m, leg. T. Schils (SMM 216); Socotra, west of Bidholih (ALG-40: 12°18'46''N,
53°58'47''E), 30 April 2000, subtidal: –20 m, leg. T. Schils (SMM 448, SMM 496, SMM

Gelatinous red algae of the Arabian Sea 39
497); South Africa: Sodwana Bay, dive site ‘Deep Sponge’, 11 February 2001, subtidal: –
30 m, leg. O. De Clerck, S. Fredericq, W. Freshwater, F. Leliaert, A. Millar, T. Schils & E.
Tronchin (KZN 2128).
DISTRIBUTION OF T. PIKEANA: Egypt, Hawaii, Madagascar, Mauritius, Réunion, South
Africa, Sri Lanka, Tanzania, Yemen (Nasr 1940; Feldmann 1942; Børgesen 1943, 1949,
1950; Mshigeni & Papenfuss 1980; Payri 1985; Bucher & Norris 1992; Norris 1992; Abbott
1999, Coppejans et al. 2000, this paper).
DISTRIBUTION OF T. WEBERAE BØRGESEN (SEE BELOW): Australia, French Polynesia,
Indonesia, Japan, Kenya, Madagascar, Tanzania (Weber-van Bosse 1921; Børgesen 1943;
Itono 1972; Farghaly 1980; Mshigeni & Papenfuss 1980; Huisman 1997; Huisman 2000;
Payri et al. 2000).
Plants are whitish pink in colour. The flat thalli (420–725 µm thick) are narrow to broad,
occasionally pertusate, with varying degrees of marginal proliferation (Fig. 36). Certain
specimens lack calcification and in others the aragonite deposits are restricted to the
medullary layer. The vegetative thallus consists of medullary filaments with large axial
filaments (Norris 1992) in the central medulla, often resulting in X- and V-shaped cells as
noted in other Nemastomataceae and Schizymeniaceae (Masuda & Guiry 1995). Cortical
filaments are composed of four or five cells; the ultimate cells are oval to elongate (3.5–10
µm × 2–5 µm) and the underlying ones are subspherical in outline (4.5–21.5 µm in
diameter). Prominent subspherical gland cells (17–65 µm in diameter) occur throughout the
outer cortex. Cylindrical to club-shaped gland cells are found in an intercalary position in the
medullary filaments. As in other Nemastomataceae and Schizymeniaceae taxa, the gland cell
contents vary widely in appearance from dense and homogeneous, through coagulated, to
granulate.
Only female gametophytes were present in our collections. A large subspherical
supporting cell (13.5–17 µm) bears a three-celled carpogonial branch distally (Fig. 37),
which is aligned in a plane parallel to the thallus surface. The oval basal cell measures 7–9.5
µm × 10.5–12.5 µm, the subrectangular hypogynous cell 4.5–7 µm × 9–16 µm, and the
carpogonium 5.5–10 × 7–9 µm. Two deeply staining cortical cells (epi-supporting cells)
flank the supporting cell, functioning as subsidiary auxiliary cells. Upon presumed
fertilization of the carpogonium, one subsidiary auxiliary cell fuses with the carpogonium
and the hypogynous cell. The diploidized subsidiary auxiliary cell initiates a connecting
filament. The second subsidiary auxiliary cell then fuses with this complex at the
hypogynous cell and initiates a connecting filament (Fig. 38). The connecting filaments
disperse throughout the cortex and diploidize distant generative auxiliary cells. In contrast to
the specimens investigated by Norris (1992), many undiploidized generative auxiliary cells
were present in the cortex of the Socotran plants (Fig. 39). The latter cells (10.5–20 µm in
diameter) are formed in an intercalary position in cortical filaments separate from those
containing supporting cells and stain darkly with Aniline Blue. Recurved and elongate
involucral cells (Figs 40–43) develop from the auxiliary cell and underlying branch systems
prior to diploidization of the latter. The involucral cells branch di- or trichotomously and
constitute involucral filaments of 3–5 cell layers. After fusion of a connecting filament with
a generative auxiliary cell, the latter divides transversely and initiates an elliptical
gonimoblast initial (7–22 µm × 13–32 µm). The gonimoblast initial generally produces two
gonimolobe initials sequentially, giving rise to gonimolobes with carposporangia of different
developmental stages. During cystocarp development, an ostiole is formed (Fig. 44);

40 Chapter 2
cystocarps are 60–200 µm in diameter. Mature carposporangia are subspherical to ellipsoidal
and measure 12–45 µm in diameter.
Figs 36–44. Titanophora pikeana.
Fig. 36. Habit of a female gametophyte, SMM 448. Scale bar = 3 cm.
Fig. 37. A large subspherical supporting cell (arrow) bears a three-celled carpogonial branch distally,
consisting of an oval basal cell (bc), a subrectangular hypogynous cell (hy) and a carpogonium (cp).
Two subsidiary auxiliary cells (sac) flank the supporting cell. Slide SMM 216d. Scale bar = 10 µm.
Fig. 38. One subsidiary auxiliary cell (sac1) fuses with the fertilized carpogonium (cp) and the
hypogynous cell (hy). Upon diploidization, the former initiates a connecting filament (cf). Subsequently,
the second subsidiary auxiliary cell (sac2) fuses with the hypogynous cell (arrow) and itself initiates a
connecting filament (cf). Slide SMM 216d. Scale bar = 10 µm.
Fig. 39. Dark-staining undiploidized generative auxiliary cell (arrowhead) with involucral filament
initiation (arrows). Slide SMM 216c. Scale bar = 25 µm.
Fig. 40. Recurved and elongated involucral cells (arrows) develop from the generative auxiliary cell
(arrowhead) and the underlying branch systems prior to diploidization. Slide SMM 216e. Scale bar = 25
µm.

Gelatinous red algae of the Arabian Sea 41
Fig. 41. The diploidized generative auxiliary cell (arrowhead), which bears involucral filament cells
(arrows) and initiates the gonimoblast initial (gi) and gonimoblast cells. Slide SOC 356a. Scale bar = 10
µm.
Fig. 42. Developing carposporophyte with the auxiliary cell (arrowhead), the gonimoblast initial
(arrow) and involucral filament cells (ifc). SMM 216b. Scale bar = 25 µm.
Fig. 43. Maturing carposporophyte with the auxiliary cell (arrowhead), the gonimoblast initial (arrow),
involucral filament cells (ifc) and carposporangia (csp). Slide SOC 356a. Scale bar = 25 µm.
Fig. 44. Surface view of the ostiole of a mature cystocarp. Slide SMM 216e. Scale bar = 25 µm.
REMARKS: Differences in habit were the main characteristics used at first to distinguish
Titanophora species (Børgesen 1943, 1949). Mshigeni & Papenfuss (1980), Bucher & Norris
(1992) and Norris (1992) reported on variability of habit and on minor differences in thallus
shape and reproductive structures among these species. Later species descriptions (Itono &
Tsuda 1980; Bucher & Norris 1992) were based predominantly on anatomical
characteristics. Conspecificity of T. pikeana and T. weberae has been proposed by various
authors (Mshigeni & Papenfuss 1980; Norris 1992; Abbott 1999), and there is a need for
developmental studies on pre- and postfertilization events in Titanophora species (Masuda &
Guiry 1994). The Socotran plants fitted both species descriptions and the specimens were
identified as T. pikeana, which is the earlier name. Additionally, the specimens agree with
the description of T. mauritiana Børgesen, which is distinguished principally by the
restriction of calcium carbonate crystals to the medullary layer. Variation in thallus shape
and calcification was observed throughout the Socotran samples, without clear differences in
reproductive or anatomical structures. Therefore, we conclude that the Socotran plants
represent one species with diverse morphotypes. In supporting Norris’ point of view (1992)
on the conspecificity of T. pikeana and T. weberae, we additionally compared the Socotran
samples with a female gametophyte from the locality he included in his study (Sodwana Bay,
South Africa). No differences in the above-described characteristics could be observed
among the Titanophora plants of Socotra and South Africa.
Owing to the low degree of calcification, the specimens were analysed by transverse
sections without an HCl treatment prior to microscopy. This might explain why the compact
cortex remained intact (versus separated filaments) and hence the difference in carpogonial
branch organization compared to the observations of Mshigeni & Papenfuss (1980).
Our account of postfertilization events in Titanophora corresponds to Itono’s (1984)
observations, viz. initiation of connecting filaments from both subsidiary auxiliary cells.
However, the connecting filaments did not develop from the cells distal to one of the
subsidiary auxiliary cells (Itono 1984; see above: Platoma heteromorphum), probably as a
consequence of the fact that the carpogonial complex we observed was in an early
postfertilization stage. In addition, the diploidization events differed for both subsidiary
auxiliary cells. The fertilized carpogonium in T. pikeana fuses entirely with a single
subsidiary auxiliary cell and the hypogynous cell. The second subsidiary auxiliary cell then
fuses with this complex at the hypogynous cell. Further studies should demonstrate if the
latter postfertilization events could be used as a diagnostic feature for the genus within the
Schizymeniaceae.

42 Chapter 2
DISCUSSION
The species we studied from the Arabian Sea suggest a great affinity with the gelatinous red
algal flora of Australia and especially of the Great Barrier Reef. However, the new records of
Dudresnaya capricornica from Saudi Arabia, Gibsmithia larkumii from Tanzania, and
Predaea weldii from South Africa show that many gelatinous red algae may have a wider
distribution range within the Indian Ocean. Hommersand (1986) states that these rather
‘primitive’ algae are widely distributed in the tropics and in regions that bordered the
original Tethyan Ocean. A report of two Reticulocaulis I.A. Abbott species from Oman and
Yemen (our unpublished observations) seems to support the latter hypothesis by their
disjunct distribution pattern in the Arabian Sea and Hawaii (Abbott 1985, 1999). The scarce
reports of gelatinous red algae in the Indian Ocean are probably a result of their seasonal
appearance and a lack of sublittoral studies. Indeed, previous claims of biogeographical links
with distant areas, such as Australia, Japan and South Africa (Børgesen 1934; Wynne 2000)
cannot be confirmed using representatives of the Dumontiaceae, Nemastomataceae and
Schizymeniaceae. The disjunct distribution of gelatinous rhodophytes of the Arabian Sea is
therefore an artefact of the research done in the Indo-Pacific, as many of the intervening
regions have been studied inadequately.
A
CKNOWLEDGEMENTS
We appreciated constructive comments from John Huisman and an anonymous reviewer.
Sincere thanks are expressed to the Senckenberg Research Institute (Michael Apel, Uwe
Zajonz and Fareed Krupp) and the Ardoukoba Association for their excellent preparations
for field work in the Socotra Archipelago and Masirah Island, respectively. Mohammed
Ismail, Ali Bin Naser Al Rasibi and André Germé are gratefully acknowledged for their
assistance with diving. The English text and the Latin description were kindly corrected by
Henry Engledow and Paul Goetghebeur, respectively. Tom Schils is indebted to the Fund for
Scientific Research Flanders (FWO, Belgium) for a research assistant grant. This research
was carried out in the framework of the FWO research projects 3G002496 and 3G013601.
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46
Platoma heteromorphum Schils: a new red algal species described from the southeast coast of Masirah Island
(see chapter 2).

Reticulocaulis in the Indian Ocean 47
CHAPTER 3
The red algal genus Reticulocaulis from the Arabian Sea, including R. obpyriformis sp.
nov., with comments on the family Naccariaceae
Published as: Schils T., De Clerck O. & Coppejans E. 2003. The red algal genus Reticulocaulis from
the Arabian Sea, including R. obpyriformis sp. nov., with comments on the family Naccariaceae.
Phycologia 42(1): in press (and cover photo).
ABSTRACT
Reticulocaulis obpyriformis Schils, sp. nov., is described from the south coast of Socotra
Island (Yemen), and a second species, R. mucosissimus, is recorded from a similar upwelling
area in the Arabian Sea (Masirah Island, Oman). These are the first published records of
Naccariaceae for the Indian Ocean and end the monospecific, Hawaiian-endemic status of
Reticulocaulis. Features distinguishing R. obpyriformis from R. mucosissimus include its
more sparsely branched thallus, obpyriform rather than cylindrical inner cortical cells, the
presence of short moniliform laterals of small spherical cells on the cortical filaments,
monoecious rather than dioecious gametophytes, and the direct development of spermatangia
from catenate mother cells. The morphology and anatomy of the gametophytes of this
heteromorphic genus are discussed in relation to those of other naccariacean genera.
INTRODUCTION
Recent phycological studies in the Arabian Sea and the northern Indian Ocean have resulted
in the description of new taxa (Wynne 1999a) and a plethora of new records (Wynne &
Banaimoon 1990; Wynne & Jupp 1998; Wynne 1999b, 2000) indicative of a unique marine
benthic flora. The south-west monsoon that results in upwelling along the south-eastern
coastline of the Arabian Peninsula (Currie et al. 1973; Ormond & Banaimoon 1994) is an
important physical phenomenon influencing these neritic ecosystems and their biotas,
particularly those of Masirah Island (Oman) and the Socotra Archipelago (Yemen), which
support a seasonally rich diversity of gelatinous red algae (Schils & Coppejans 2002).
Among the more unexpected of the algae recently discovered, there are two species of
Reticulocaulis, a hitherto monotypic genus thought to be confined to Hawaii in the central
Pacific Ocean and a member of the relatively little-known and infrequently encountered
family Naccariaceae.
Following the recommendations of Kylin (1928), Svedelius (1933) and Feldmann &
Feldmann (1942), the Naccariaceae is generally included in the order Bonnemaisoniales,
based on details of gonimoblast development and the presence of nutritive-cell clusters on
the carpogonial branch (Chihara & Yoshizaki 1972), an ordinal placement supported by
ultrastructural characters of the pit plugs (Pueschel & Cole 1982). Womersley (1996),
however, commented that the family might not be related to the Bonnemaisoniaceae,
because of some seemingly major differences in the carposporophyte, such as a diffuse

48 Chapter 3
rather than compact gonimoblast and the complete absence of a pericarp. Abbott (1999)
recently placed the Naccariaceae in the Gigartinales without specifying her reasons for the
transfer. The Naccariaceae currently comprises the genera Atractophora P. Crouan & H.
Crouan, Naccaria Endlicher and Reticulocaulis I.A. Abbott. Despite consisting of only seven
species, of which five belong to Naccaria, the family is widely distributed throughout the
Atlantic and Pacific Oceans. Although a single robust female gametophyte of Naccaria
naccarioides (J. Agardh) Womersley & I.A. Abbott is known from the Indian Ocean coast of
Western Australia (GEN-10793e, MELU: leg. G.T. Kraft & G.W. Saunders, 7.x.1995,
Pinaroo, Western Australia, 32.20°S, 115.45°E), the present paper is the first published
report of a member of the Naccariaceae from anywhere in the Indian Ocean.
M
ATERIAL AND METHODS
The east coast of Masirah Island (Oman; 20.42°N, 58.79°E; Figs 1, 2) and the south coast of
Socotra (Yemen; 12.47°N, 53.87°E; Figs 1, 3) are influenced by a seasonal coastal upwelling
from May to September, during the south-west monsoon. The specimens of this report were
found in similar habitats around Masirah and Socotra, viz. rocky platforms at 10–20 m depth
on which macroalgae were the most abundant benthic organisms, interspersed with isolated
small hard and soft coral colonies. Gelatinous red algae such as Dudresnaya P. Crouan & H.
Crouan, Gibsmithia Doty, Platoma Schousboe ex Schmitz and Predaea De Toni species
(Schils & Coppejans 2002) were particularly conspicuous during early winter and late spring
periods, other associated algae being Amphiroa J.V. Lamouroux spp., Callophycus Trevisan
sp., Caulerpa peltata J.V. Lamouroux, Euptilota fergusonii Cotton, Galaxaura marginata
(Ellis & Solander) J.V. Lamouroux, Halimeda J.V. Lamouroux spp., Lobophora variegata
(J.V. Lamouroux) Womersley ex Oliveira, Rhodymenia Greville spp., Spatoglossum
asperum J. Agardh, and Udotea indica A. Gepp & E. Gepp.
Specimens of Reticulocaulis were collected by the first author during field trips to Masirah
Island in 2–30 November 1999 and Socotra in 26 March–7 May 2000, the subtidal habitats
being accessed by means of SCUBA. Collected algae were pressed on herbarium sheets,
with portions preserved in a 5% formalin–seawater solution. Herbarium sheets, wet
specimens and microscope slides are deposited in GENT (Ghent University Herbarium,
Krijgslaan 281 / S8, 9000 Ghent, Belgium). Slides and formalin-preserved samples of
Hawaiian Reticulocaulis mucosissimus I.A. Abbott were kindly supplied by I.A. Abbott of
the Bernice Bishop Museum (BISH). Herbarium sheets of Naccaria corymbosa J. Agardh
and N. wiggii (Turner) Endlicher were borrowed from the National Herbarium of the
Netherlands (L). Material for microscopical examination was stained with Aniline Blue, Fast
Green or Lugol’s Iodine (for rhodoplasts). Material for nuclear and pit-connection studies
was stained using Wittmann’s aceto-iron-haematoxylin–chloral hydrate (Wittmann 1965),
following the procedures of Hommersand & Fredericq (1988). Anatomical and reproductive
characteristics were observed from tissue squashes (whole-mounts in a 50% corn syrup-
water solution, containing a few drops of phenol) using light microscopy (Leitz Diaplan).
Photographs were taken with a Wild MPS51 35-mm camera and on an Olympus DP50
digital camera.

Reticulocaulis in the Indian Ocean 49
Figs 1–3. Collection sites of Reticulocaulis in the Arabian Sea. Scale bars = 1000 km (Fig. 1) or 20 km (Figs
2, 3).
Fig. 1. The Arabian Peninsula showing Masirah Island and Socotra.
Fig. 2. Sample Site 9 (asterisk; 20.199°N, 58.715°E), near Ras Zarri, off Masirah Island, Oman.
Fig. 3. Sample site ALG-40 (asterisk; 12.303°N, 53.843°E), west of Bidholih, off Socotra, Yemen.
RESULTS
Reticulocaulis mucosissimus I.A. Abbott 1985, p. 555
SPECIMENS EXAMINED: Oman. Masirah Island (Figs 1, 2): Sample site 9 (20.199°N,
58.715°E), close to Ras Zarri. A rocky platform at 9 m depth with scattered rocky outcrops
in an area of strong surge (Schils, 9.xi.1999). MAS 138: female (Fig. 4) and male
gametophytes. Hawaii. Mahukona, north-west coast of Hawaii. Plants growing on dead coral
at a depth of 9 m (K. J. McDermid, 26.v.1998). Formalin sample IA 23471 (female
gametophyte) and slide KM 4481 (female gametophyte); Kawailoa, Oahu Island (W. H.
Magruder & S. Carper, 10.v.1985). Slide IA 17225: female gametophyte.
Thalli are bright red, mucilaginous, and attached by a discoid holdfast (Fig. 4). Omani plants
reach 13 cm in length and grow from dome-shaped apical cells that divide obliquely, the
immediate daughter cells being aligned in a nearly straight row (Fig. 5). The axial cells are
slender and elongate, those lying 1 mm away from the apical cells having length : width

50 Chapter 3
ratios of > 4 : 1. The first periaxial cell (the ‘superior’ periaxial) is cut off three axial cells
from the apex and superior periaxial cells on successive segments are produced in an
irregular 1/4 spiral. A second periaxial cell (the ‘inferior’ periaxial) is always positioned
proximal to the first. It is generally cut off in cells positioned 15–20 cells away from the
apex (Fig. 5) and at a 90° angle to the first periaxial cell. At the same time, several rhizoidal
outgrowths develop from both periaxial cells; these outgrowths branch. Besides differing in
the timing of their initiation, the shapes of the two periaxial cells are also dissimilar: the
superior periaxial cell becomes elongated and rectilinear, whereas the inferior one remains
spherical (Fig. 5). The inferior lateral becomes the more developed of the two laterals and
occasionally gives rise to indeterminate branches as it continues growing and initiates
periaxial cells. Infrequently, an axial cell can initiate a third periaxial cell, which develops
like the superior lateral. The derivatives of the periaxial cells (from about the 15
th
axial cell)
differentiate rapidly by branching and cell elongation into determinate filaments that
constitute the cortex. The inner cortical cells are cylindrical (Fig. 6), whereas the outer cells
remain ovoid to (sub)spherical.
Two-celled propagules, reaching 16.5 µm in diameter (Fig. 7) and developing terminally
on many of the cortical filaments, were observed in slide IA 17225 of a specimen from
Hawaii. One or two axial cells below the site where the second periaxial cell first forms, both
periaxial cells initiate rhizoidal downgrowths. The periaxial cells and the rhizoidal
downgrowths inflate into what were termed ‘jacket cells’ by Abbott (1985), viz. cells that
mutually cross-connect by lateral secondary pit connections (Fig. 8) and constitute a sheath
around the central-axial strand (Fig. 9). While maturing, the pit connections of the jacket
cells attenuate and become difficult to distinguish, which results in a seemingly
parenchymatous covering. Before the covering is complete, the jacket cells initiate secondary
cortical filaments that are either fasciculate or unbranched, as well as secondary rhizoidal
downgrowths. In older parts of the thallus, the jacket cells become densely covered by these
secondary rhizoidal filaments, which rarely branch and form uniseriate rows that cross one
another, but actually constitute a single layer.
The rhodoplasts are discoid but like erythrocytes in shape (2-4 µm in diameter), having
centres that are thinner than the margins.
Female gametophytes have carpogonial branches that are of accessory origin; they were
found throughout the thallus in various stages of development. Near the apex, carpogonial
branches arise singly from either of the periaxial cells. Further down the thallus, they also
develop from other jacket cells (rhizoidal filament cells) and the lower cortical filament
cells. Pairs of carpogonial branches on a single supporting cell are infrequently seen. The
branches consist of 7–13 equally-staining cells, which, following the terminology of
Lindstrom (1984), can be designated by numbers starting with the carpogonium (#1).
Eccentric positioning of the primary pit connections results in a zigzag arrangement of
carpogonial-branch cells when viewed dorsally or ventrally (Fig. 12). The carpogonial
branch curves sharply toward the axis bearing it and the carpogonium arises adaxially on cell
#2, the hypogynous cell (Figs 10, 11). The initially short and reflexed trichogyne can
elongate to over 500 µm (Figs 12, 13; Abbott 1985).

Reticulocaulis in the Indian Ocean 51
Figs 4–9. Reticulocaulis mucosissimus. ac = axial cell; jc = jacket cell; pc = periaxial cell. Vegetative features.
Scale bars = 2 cm (Fig. 4); 50 µm (Figs 5, 6); 10 µm (Fig. 7); 50 µm (Fig. 8, 9).
Fig. 4. Female gametophyte (pressed herbarium specimen) from Masirah Island; MAS 138.
Fig. 5. Apex of an indeterminate axis, showing the apical cell (arrow) and periaxial cells (arrowheads);
KM 4481.
Fig. 6. The transition from cylindrical inner- to spheroidal outer-cortical cells; MAS 138.
Fig. 7. Two-celled propagules on a Hawaiian specimen; IA 17225.
Fig. 8. Detail of an inflated jacket cell in a Hawaiian specimen, showing primary (arrows) and lateral
secondary pit connections (arrowheads); IA 23471.
Fig. 9. Sheath of jacket cells around the central-axial strand, showing secondary cortical filament
initiation (arrows); MAS 138.

52 Chapter 3
Figs 10–15. Reticulocaulis mucosissimus. Carpogonial and carposporophyte morphology (MAS 138). ac =
axial cell; bc = basal cell of carpogonial branch; cfc = cortical filament cells; cp = carpogonium; cs =
carposporangium; jc = jacket cell; nc = nutritive-cell cluster; sc = supporting cell of carpogonial branch; sl
= sterile lateral; tri = trichogyne. Scale bars = 10 µm.
Fig. 10. Seven-celled carpogonial branch before elongation of trichogyne from the carpogonium, with
sterile laterals growing from the lower cells.
Fig. 11. Young carpogonial branch, on which the carpogonium has produced a reflexed trichogyne and
sterile laterals have arisen from most of the proximal cells. A jacket cell has also been initiated by the
supporting cell.
Fig. 12. Dorsal view of a mature carpogonial branch, showing the zigzag arrangement of the cells and
densely clustered nutritive cells borne on the hypogynous cell (cell #2).

Reticulocaulis in the Indian Ocean 53
Figs 13, 14. Lateral views of carpogonial branches bearing nutritive-cell clusters on the hypogenous cell
and on cells #3, #4 (shaded), and lengthy sterile laterals on more proximal cells.
Fig. 15. Early carposporophyte development, showing the nutritive-cell clusters (shaded) and
carposporangium initiation. The carpogonial branch cells and the basal cells of the sterile laterals inflate
and pit connections widen. Cortical filaments arise from jacket cells.
Figs 16–20. Reticulocaulis mucosissimus. Cystocarpic and spermatangial features. (MAS 138). cfc = cortical
filament cell; cp = carpogonium; cs = carposporangium; gc = gonimoblast cell; gi = gonimoblast initial;
hy = hypogynous cell; nc = nutritive cell; sp = spermatangium; spm = spermatangial mother cell; tri =
trichogyne. Scale bars = 10 µm.
Fig. 16. Division of the (presumably fertilized) carpogonium to produce the gonimoblast initial.
Nutritive-cell filaments are borne on the hypogynous cell, and the trichogyne is still attached to the
carpogonium.
Fig. 17. Fusion of the nutritive-cell clusters to the hypogynous cell through primary pit connections
(arrowhead), in which the pit plugs progressively break down (arrows), resulting in broad open
passageways. Gonimoblast cells are larger and more angular than nutritive cells and abut the clusters
next to the remnant trychogyne.
Fig. 18. Ovoid terminal carposporangia borne on angular penultimate cells of branched gonimoblast
filaments.
Fig. 19. Spermatangia forming in dendroid clusters on one of a pair of ultimate branches of a cortical
filament, the cells of the second branch remaining sterile.
Fig. 20. Detail of a dendroid spermatangial cluster: the spermatangia are borne mostly in pairs on
subterminal mother cells.

54 Chapter 3
Cell #2 initiates a cluster of 4–6 branched filaments of tightly packed nutritive cells (Fig.
14), whereas cells #3 and #4 tend to bear a primary, slightly branched lateral, a second
slightly more branched lateral, and 1–3 small clusters of ramified nutritive cells (Fig. 13).
Primary laterals, 6–16 cells in length and branched to two orders, form adaxially on most of
the remaining carpogonial branch cells, the longest occurring on the most proximal cells
(Figs 13, 14). Any of the cells proximal to cell #4 may ultimately bear either an abaxial or an
adaxial second sterile filament.
Upon presumed fertilization, the carpogonial branch cells and the basal cells of the sterile
laterals inflate, and both the pit connections and the nuclei of these cells enlarge substantially
(Fig. 15). The gonimoblast initial develops directly from the fertilized carpogonium (Fig.
16); at the same time, the nutritive cells fuse directly with the hypogynous cell through their
pit connections, which retain their original size or expand only slightly as the pit plugs break
down (Fig. 17). The passageways that are now open between the hypogynous cell and the
nutritive cell clusters presumably become paths for direct nutrient transport to the developing
gonimoblast. The carposporophyte remains compact, does not intermingle with vegetative
tissue, and lacks a pericarp. Ovoid carposporangia (40 × 30 µm) terminate branches of the
compact gonimoblast (Fig. 18); cystocarps at various stages of development are found
scattered within the cortex and reach 330 µm in diameter.
Spermatangia are produced in terminal dendroid clusters on separate male gametophytes,
the fertile axes often being accompanied by a sterile sibling cortical filament of one or two
cells (Fig. 19). Spermatangial mother cells initiate 1–3 spermatangia (Fig. 20).
Tetrasporangial thalli were not collected in the course of this study and are unrecorded for
the genus. In line with findings for other genera of the Naccariaceae (Jones & Smith 1970;
Boillot & L’Hardy-Halos 1975), Reticulocaulis is presumed to have a heteromorphic life
history involving a diminutive system of prostrate filaments bearing terminal tetrahedral
tetrasporangia. Growth of Hawaiian R. mucosissimus in culture, reported by Abbott (1999, p.
123), resulted in a microscopic filamentous phase but no production of tetrasporangia.
Reticulocaulis obpyriformis Schils, sp. nov.
Affinis Reticulocaulis mucosissimis Abbott (1985) sed differt characteribus pluribus.
Gametophyta monoica; thallus pallido-roseolus pallidus, usque ad 15 cm altus, rami
indeterminatis laxe et irregulatim ramificantibus. Cellulae corticis obpyriformes cylindricae;
rami breves cellulis parvis sphaericis in filamento corticato, rarus evolutantes in axes
indeterminatos; interdum trichomata in cellulis terminalibus rel subterminalibus corticis
portata; cellulae axiales intra 1 mm sub apice latae ad 70(–80) µm. Spermatangia evoluta e
filamenti corticalis cellulis distalibus. Praesentia duorum ramorum carpogonialium in
cellula basali frequentior quam in R. mucosissimo. Filamenta lateralia secunda persaepe in
cellulis proximis ramorum carpogonialium.
Similar to Reticulocaulis mucosissimus Abbott (1985) but with the following distinguishing
characters: gametophytes monoecious; thalli pale pink, to 15 cm high; branching of
indeterminate axes loose and irregular. Cortical cells obpyriform and cylindrical; cortical
filaments bearing short laterals consisting of small spherical cells and potentially developing
into indeterminate axes; hairs occasional on terminal and subterminal cortical cells; axial
cells broadening to 70(–80) µm within 1 mm of the apices. Spermatangia developing directly
from catenate series of distal cortical cells. Supporting cells bearing two carpogonial

Reticulocaulis in the Indian Ocean 55
branches occur more frequently than in R. mucosissimus. Secondary laterals common on
proximal carpogonial branch cells.
HOLOTYPE: GENT, SMM 446 (Fig. 21)
TYPE LOCALITY: west of Bidholih, south coast of Socotra Island (Figs 1, 3). Sample site
ALG-40 (12.303°N, 53.843°E): a rocky platform at –19 m covered with thin layers of sand
and punctuated by deeper sand patches (Schils, 30.iv.2000).
ETYMOLOGY: obpyriformis, refers to the inverse pear shape of the cortical cells.
The thalli are terete, pale pink, and up to 15 cm in length (Fig. 21). Branching is irregularly
radial, with a sparse development of up to four orders of indeterminate laterals. The dome-
shaped apical cell divides obliquely, the immediate derivatives forming a sinusoidal pattern
before the axial cells become aligned (Fig. 23).
Within 1 mm of the apices, the axial cells broaden to attain length : width ratios of < 4 : 1
(Fig. 22). The superior periaxial cell is cut off at about the third axial cell behind the apex,
the ‘phyllotaxy’ on successive segments being alternate (Fig. 23). Inferior periaxial cells,
rhizoidal downgrowths and laterals develop from about the 40
th
axial cell downwards, at
which time the phyllotaxy of the determinate laterals tends to become an irregular 1/4 spiral,
because the inferior periaxials set in at a 90° angle to the superior periaxial cells. Derivatives
of the inferior periaxial cells become more strongly developed than those of the superior
cells and initiate the occasional indeterminate branch when the cortical filament continues
growing and initiates periaxial cells. Third-order periaxial cells are very infrequently
initiated in older parts of the thallus; they develop cortical filaments and jacket cells like the
other periaxial cells.
The lower cells of the cortical filaments are predominantly obpyriform (Figs 22, 24),
although cylindrical to barrel-shaped cells also occur (Fig. 24). The sizes and contours of the
cortical cells change rather abruptly distally, from being elongated, obpyriform or
cylindrical, and up to 90 µm long by 27 µm wide, to being small, spherical, and 4–6 µm in
diameter. Hairs occasionally develop on terminal and subterminal cortical cells (Fig. 25), but
propagules were not observed.
Certain cortical filaments bear short moniliform laterals of small spherical to ovoid cells
(Fig. 24); these laterals can bear spermatangia, less often carpogonial branches, or may
transform directly into indeterminate axes (the atypical way of indeterminate lateral
formation: Fig. 23).
Several orders of rhizoidal downgrowths develop from the periaxial cells, the cells
becoming inflated and linked by lateral secondary pit connections (Fig. 26) and forming a
sheath around the axial strand (Fig. 27), in which the pit connections attenuate and become
obscure. These jacket cells are spheroidal and may give rise to secondary cortical filaments.
In older parts of the thallus, the jacket cells become densely covered by rhizoidal filaments.
The rhizoidal filaments develop from periaxial cells and other jacket cells; they branch (Fig.
28) and some initiate secondary cortical filaments (Figs 22, 27, 28).
The rhodoplasts are discoid, have a distinctive ‘erythrocyte’ appearance (Fig. 29), and are
2–4 µm in diameter. As in R. mucosissimus, the rhizoidal and jacket cells contain fewer
rhodoplasts than the cortical cells, and older axial cells virtually lack them altogether.

56 Chapter 3
Figs 21–24. Reticulocaulis obpyriformis. Habit and vegetative features (SMM 446). ac = axial cell; cfc =
cortical filament cell; cpb = carpogonial branch; pc = periaxial cell. Scale bars = 2 cm (Fig. 21); 100 µm
(Fig. 22); 10 µm (Figs 23, 24).
Fig. 21. Holotype (a pressed monoecious specimen).
Fig. 22. Bead-like, inflated axial cells jacketed by derivatives of the periaxial cells and by rhizoids that
give rise to unbranched secondary cortical filaments (arrowheads). Primary cortical filaments of
obpyriform cells and a carpogonial branch are borne on the periaxial cells.
Fig. 23. Direct transformation of a short moniliform branch of a cortical filament into an
indeterminate lateral, as indicated by the sinusoidal development of the axis behind the apical cell
(arrow) and the alternate production of periaxial cells and cortical filaments.
Fig. 24. Obpyriform and cylindrical cortical cells bearing single or paired moniliform laterals of
restricted growth.
The gametophytes are monoecious. Spermatangia develop on terminal (Fig. 25) and
subterminal cortical cells, with up to nine fertile axial cells forming in series (Fig. 30).
Unlike in R. mucosissimus, the spermatangia tend to be borne directly on fertile axial cells,
rather than on terminal mother cells of dendroid cortical filaments. Carpogonial branches are
scattered throughout the thallus in various states of development. The carpogonial branch is
7–13 cells long, the supporting cell being one of the periaxial cells, a jacket cell (rhizoidal
filament cell), or a lower cortical filament cell. The presence of two carpogonial branches on
a single supporting cell occurs more frequently than in R. mucosissimus (Fig. 31). The
hypogynous cell produces 4–6 branched clusters of densely aggregated nutritive cells. Cells
#3 and #4 generally each bear two longer branched laterals and 1–3 small nutritive-cell
clusters. The carpogonial branch cells proximal to cell #4 bear a long primary sterile lateral
and may ultimately come to bear an ab- or adaxial second sterile lateral. As the carpogonial
branch matures, sterile laterals become progressively more branched. Upon fertilization, the
carpogonial branch cells and the basal cells of the sterile laterals inflate, both the pit
connections and nuclei of these cells enlarging substantially. The gonimoblast initial

Reticulocaulis in the Indian Ocean 57
develops directly from the fertilized carpogonium. The nutritive cells did not stain, because
their contents were rapidly emptied, and thickened strands between the nutritive cell clusters
and the hypogynous cell were not seen. Mature carposporophytes were not observed and
hence no measurements of cystocarpic structures (diameter of cystocarps and
carposporangia) could be made.
Tetrasporophytes are unknown.
Figs 25–28. Reticulocaulis obpyriformis. Habit and vegetative features (SMM 446). ac = axial cell; cfc =
cortical filament cell; jc = jacket cell; pc = periaxial cell. Scale bars = 10 µm (Fig. 25); 20 µm (Fig. 26); 100
µm (Fig. 27); 20 µm (Fig. 28).
Fig. 25. Hairs (arrows) and spermatangia (arrowheads) developing from terminal and subterminal
cortical cells.
Fig. 26. Primary pit connection (arrow) and lateral secondary pit connections (arrowheads) of an
inflated jacket cell covered by a narrow rhizoidal filament.
Fig. 27. Axial cells surrounded with a sheath of jacket cells, which develop branched (black arrow) and
unbranched secondary cortical filaments (arrowhead). Primary cortical filaments (open arrow) are borne
on the periaxial cells.
Fig. 28. Jacket cells that initiate multiple rhizoidal filaments (arrowheads), which branch (arrows), and
secondary cortical filaments.

58 Chapter 3
Figs 29–33. Reticulocaulis obpyriformis and Naccaria wiggii. bc = basal cell of carpogonial branch; cp =
carpogonium; hy = hypogynous cell; sc = supporting cell of carpogonial branch; stc = sterile cell; tri =
trichogyne. Scale bars = 10 µm (Fig. 29); 20 µm (Fig. 30); 50 µm (Figs 31, 32); 10 µm (Fig. 33).
Figs 29–31. Reticulocaulis obpyriformis, SMM 446.
Fig. 29. Discoid rhodoplasts (arrowheads) with thickened rims that give them an appearance similar to
erythrocytes; the plastids densely fill an inner cortical cell and there are also surrounding reserve
vacuoles (arrows).
Fig. 30. Spermatangia (arrowheads) developing on terminal and intercalary cortical mother cells.

Reticulocaulis in the Indian Ocean 59
Fig. 31. Two carpogonial branches borne on a single supporting cell of a cortical lateral.
Figs 32, 33. Naccaria wiggii, L 0276772.
Fig. 32. Primary pit connection (arrow) and lateral secondary pit connections (arrowheads) on a jacket
cell.
Fig. 33. A four-celled carpogonial branch, on which sterile cells arise from cells #2 and #3 but which
lacks nutritive-cell clusters.
DISCUSSION
The Arabian collections of Reticulocaulis extend the known distribution of the Naccariaceae
from the Atlantic and the Pacific to the north-western Indian Ocean. Both species occur there
in habitats similar to that occupied by R. mucosissimus in Hawaii, the Hawaiian populations
forming part of a ‘spring flora’, which consists mainly of gelatinous species of
Acrosymphyton L.G. Sjöstedt, Dudresnaya, Gibsmithia and Schmitzia P.C. Silva growing in
areas scoured by waves 4–10 metres in height (I.A. Abbott, personal communication). The
strong seasonality of members of the Naccariaceae has been documented previously (Dixon
& Irvine 1977; Womersley 1996) and we suspect that seasonal growth in the northern Indian
Ocean may be related to daylength changes and water temperature. The occurrence of R.
mucosissimus in Hawaii and Oman corresponds to previous reports of a biogeographical
affinity of certain Arabian Sea biota with distant regions in the Pacific (Coles 1995: Hawaii;
Wynne 2000: Japan; Schils & Coppejans 2002: Australia). These disjunct distributions can
be explained by (1) undersampling of subtidal habitats within the Indo-Pacific (Schils &
Coppejans 2002) and (2) being relicts of Miocene distributions, which were altered as a
result of changes in the current patterns (Hommersand 1986) that formerly connected these
regions, separating the refugia that are subject to seasonal temperate water (Schils et al.
2001). However, because of the seasonal appearance of the Naccariaceae and their generally
infrequent occurrence, few data are available and it is currently not possible to favour either
of the two hypotheses.
The Reticulocaulis species, R. mucosissimus and R. obpyriformis, are easily distinguished
by various anatomical and morphological features (Table 1). In erecting the genus, Abbott
(1985) distinguished Reticulocaulis from the closely related Naccaria by the different
developmental pattern of the ‘jacket cells’ (see below), the longer and more elaborately
branched carpogonial branches, and the compact vs diffuse carposporophyte. However,
Abbott (1985) was comparing R. mucosissimus with N. naccarioides (J. Agardh) Womersley
& I.A. Abbott (previously regarded as the type species of Neoardissonia Kylin) and
Naccaria hawaiiana I.A. Abbott, rather than with the generitype, N. wiggii (Turner)
Endlicher. This becomes an important consideration when evaluating the contrast Abbott
made between the axial sheath of Reticulocaulis and the ‘axial pseudoparenchyma’ of
Naccaria. Abbott (1985) regarded the former as resulting from the cross-connection of
enlarged periaxial- and rhizoidal-cell derivatives lying parallel to the central-axial filament in
Reticulocaulis, whereas the multilayered axial sheath in Naccaria originates from several
successive basal cells of the cortical filaments. Examination of material of N. wiggii (L
0276772: leg. P. & H. Huvé, 13.v.1963, Calanque de Sormiou, Marseilles, France; Fig. 32)
and N. corymbosa (L 0276776: leg. A. J. Bernatowicz, 16.iii.1953, Gunners Bay, east end of
St David’s Island, Bermuda) shows that both have similar secondary pit connections between
axial-strand cells and that these become attenuate and obscure while maturing, as in
Reticulocaulis. The sheath of jacket cells around the central axes of N. wiggii and N.
hawaiiana is composed of inflated periaxial, rhizoidal and inner cortical cells (Boillot &

60 Chapter 3
L’Hardy-Halos 1975: Figs 8, 13; Womersley & Abbott 1968). Millar (1990) notes that the
degree of inflation of descending-filament cells in N. naccarioides varies in the few recorded
specimens according to where in Australia they come from, thus perhaps undermining the
absolute taxonomic value of the very criterion for which Reticulocaulis was named.
Table 1. Comparison of morphological and anatomical features in Reticulocaulis mucosissimus and R.
obpyriformis.
Reticulocaulis mucosissimus Reticulocaulis obpyriformis
dark rose pale pink
thallus reaching 13 cm thallus reaching 15 cm
densely branched; thallus contour tapers
pyramidally at the apices due to the
organisation of the short laterals
sparsely branched thallus, even the small
indeterminate laterals do not branch
densely
rather straight apices sinusoidal apices
branching an irregular 1/4 spiral branching initially alternate, later (from
second periaxial cell formation onwards)
an irregular 1/4 spiral
early (15–20
th
axial cell) appearance of
second periaxial cell
late (> 40
th
axial cell) appearance of second
periaxial cell
angular to globose jacket cells spherical jacket cells
gradual acropetal transition of cortical cells
from cylindrical to spherical; short
moniliform branches of cortical filaments
absent; terminal hairs lacking
abrupt acropetal transition of cortical cells
from cylindrical or obpyriform to small
and spherical or ovoid; short moniliform
branches of cortical filaments present;
terminal or subterminal hairs occasional
dioecious monoecious
secondary laterals or rhizoidal filaments on
proximal carpogonial branch cells
relatively infrequent
secondary laterals or rhizoidal filaments on
proximal carpogonial branch cells
common
axial cells slender axial cells broadly inflated
two-celled propagules occasional on outer
cortical cells
two-celled propagules absent
Additional features separating Reticulocaulis and Naccaria include differences in which of
the periaxial cells grows out into the dominant lateral on each axial cell: supposedly it is
primarily the superior in Naccaria and the inferior in Reticulocaulis. However, this criterion
may not be reliable, because Millar (1990) argues that the dominance of either determinate
fascicle in Naccaria appears to be strongly affected by age or habitat.
Other characters, however, clearly distinguish Reticulocaulis from Naccaria (Table 2).
The carpogonial branches are longer (7–13 cells vs 2–8 cells) in Reticulocaulis and develop
from the periaxial cells, the jacket cells and the lower cells of the cortical fascicles, whereas
in Naccaria species they can arise from the periaxial cells (in N. hawaiiana: Abbott 1985,
fig. 11), from intercalary supporting cells at various levels in the cortex (in N. wiggii:
specimen L 0276772), or from rhizoids (in N. naccarioides: Womersley 1996, p. 356). The
degree to which sterile laterals arise and develop on carpogonial branch cells appears to be
variable in Naccaria species such as N. hawaiiana (Abbott 1999), N. naccarioides (Millar

Reticulocaulis in the Indian Ocean 61
1990; Womersley 1996) and N. wiggii (Hommersand & Fredericq 1990; Fig. 33), but the
sterile laterals in Naccaria never approach the degree of development seen in Reticulocaulis.
The production of nutritive-cell clusters on the hypogynous cell is more consistent in
Reticulocaulis than in Naccaria [e.g. observations of N. wiggii, L 0276772; N. corymbosa J.
Agardh, L 0276776: leg. A.J. Bernatowicz, 16.iii.1953, Gunners Bay, east end of St David’s
Island, Bermuda; and N. naccarioides, Womersley & Abbott (1968)], in which their
presence is variable even on single plants; at times they can be absent altogether (Fig. 33).
The nutritive cell clusters on the two cells (carpogonial branch cells #3 and #4) proximal to
the hypogynous cell in Reticulocaulis are lacking in Naccaria. Nutritive cell clusters are also
more numerous and more densely packed in Reticulocaulis than in Naccaria (Abbott 1985).
Perhaps the greatest difference between Naccaria and Reticulocaulis lies in the structure of
the cystocarp, which grows diffusely among cortical filaments in Naccaria (Dixon & Irvine
1977; Hommersand & Fredericq 1990; Millar 1990; Womersley 1996) but remains tightly
compact in Reticulocaulis, although post-fertilization stages, such as the fusion of the
fertilized carpogonium and hypogynous cell by widening of the pit connection, are similar in
both genera (Millar 1990; Womersley 1996). Formation in Naccaria of a fusion cell that
incorporates the fertile-axial cell (Hommersand & Fredericq 1990; Womersley 1996: Fig.
160 H), however, is not seen in Reticulocaulis and constitutes another major difference
between the two genera. The difference in the sizes of the mature cystocarp structures of R.
mucosissimus between those reported here (carposporangium and cystocarp diameter) and
those reported in Abbott (1985: p. 557, Fig. 6), is probably the result of Abbott having made
measurements on immature cystocarps. The specimens from Hawaii examined in this paper
bore cystocarp structures covering the range reported found in the Omani specimens.
Spermatangial organization appears to differ between species of Naccaria to a degree
equal to that seen between the two species of Reticulocaulis. In R. mucosissimus, the male
gametophytes bear dense terminal clusters, in which branched laterals terminate in
spermatangial mother cells (Abbott 1985, Fig. 4; our Figs 19, 20), whereas in R.
obpyriformis they develop directly on outer cortical cells, as in N. hawaiiana (Abbott 1985,
Fig. 7).
The R. obpyriformis type of spermatangial arrangement is also characteristic of the
recently described Liagorothamnion mucoides Huisman, D.L. Ballantine & M.J. Wynne
(2000), an enigmatic monotypic genus that the authors provisionally put in its own tribe (the
Liagorothamnieae) within the family Ceramiaceae. The authors state that the post-
fertilization process in Liagorothamnion is ‘difficult to observe’ and ‘open to interpretation’
but that it apparently involves fusion of the fertilized carpogonium by means of connecting
cells or short filaments to the supporting cell, which is located at the base of a whorl-
branchlet. This process is very similar to that reported for Atractophora (Millar 1990), to
which Liagorothamnion thus shows a number of striking similarities. Both genera are
mucilaginous, produce four whorl-laterals per axial cell, surround their central-axial
filaments with a jacket of uninflated cells, have three- to four-celled recurved carpogonial
branches bearing more than two sterile groups, and produce a carposporophyte that
surrounds the axial strand and intermingles with vegetative filaments. Liagorothamnion may
thus prove to have a closer alliance to the Naccariaceae than to the Ceramiaceae.

62 Chapter 3

Reticulocaulis in the Indian Ocean 63
Abbott (1985) has suggested that Reticulocaulis ‘might be looked upon as reduced from
Acrosymphyton-like forms in terms of the carpogonial branch ...’ and hence related to the
Dumontiaceae, a family then placed in the order Cryptonemiales and now a member of the
Gigartinales (Saunders & Kraft 1997). The proposed affinity between Reticulocaulis and
Acrosymphyton is not supported by recent evidence. According to a phylogenetic analysis of
the Dumontiaceae (Tai et al. 2001), Acrosymphyton (Acrosymphytaceae; Lindstrom 1987) is
sister to the Gelidiales, whereas Bonnemaisonia is basal to the included Gigartinales and
Gelidiales. Ongoing molecular research (G.W. Saunders & C.A. Maggs, personal
communication) shows that the Naccariaceae is almost certainly not monophyletic (Naccaria
groups weakly with the Bonnemaisoniaceae and may not belong in the Bonnemaisoniales,
whereas Atractophora receives solid support as a member of the Bonnemaisoniaceae), and it
clearly does not belong in either the Nemaliales or the Gigartinales. Saunders & Kraft (1997,
p. 130) suggested that DNA studies of the Naccariaceae, to establish its ordinal affinities,
should be a top priority for molecular systematists, and this recommendation still holds.
ACKNOWLEDGEMENTS
We greatly appreciate the useful comments of Gerry Kraft and Max Hommersand, which
helped improve the manuscript. We also give sincere thanks to Isabella Abbott for her help
and enthusiasm in providing Hawaiian specimens, and the Senckenberg Research Institute,
Germany (Michael Apel and Friedhelm Krupp), the UNDP Socotra Marine Team, and the
Ardoukoba Organization (France) for excellent organization and a pleasant ambience during
both field trips. A special thanks to the fellow ‘missionaries’, whose cheerful and
professional spirit kept our little commune efficiently going. Tom Schils is much indebted to
the diving partners Mohammed Ismail, Ali Bin Naser Al Rasibi and André Germé, who all
became intrigued by hunting static sea life. The Latin translation was kindly supplied by Paul
Goetghebeur. Tom Schils and Olivier De Clerck are indebted to the Fund for Scientific
Research Flanders (Belgium) for research assistant and postdoctoral research grants,
respectively. Financial support was provided by the FKFO project 3G002496.
REFERENCES
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hawaiiana sp. nov. (Rhodophyta, Naccariaceae). J. Phycol. 21: 554–561.
Abbott I.A. 1999. Marine red algae of the Hawaiian Islands. Bishop Museum Press, Honolulu,
Hawai’i. 477 pp.
Boillot A. & L’Hardy-Halos M.-T. 1975. Observations en culture d’une Rhodophycée
Bonnemaisoniale: le Naccaria wiggii (Turner) Endlicher. Bull. Soc. Bot. France 20: 30–36.
Coles S. L. 1995. Corals of Oman. CYK Publications, Muscat. 100 pp.
Chihara M. & Yoshizaki M. 1972. Bonnemaisoniaceae: their gonimoblast development, life history
and systematics. In: Contributions to the systematics of benthic marine algae of the North Pacific
(Ed. by I.A. Abbott & M. Kurogi), pp. 243–251. Japanese Society of Phycology, Kobe.
Currie R.J., Fisher A.E. & Hargreaves P.M. 1973. Arabian Sea Upwelling. In: The biology of the
Indian Ocean (Ed. by B. Zietzschel), pp. 37–52. Springer Verlag, New York.
Dixon P.S. & Irvine L.M. 1977. Seaweeds of the British Isles. Vol. 1. Rhodophyta – Part 1.
Introduction, Nemaliales, Gigartinales. British Museum (Natural History), London. 252 pp.

64 Chapter 3
Fan K.-C. 1961. Morphological studies of the Gelidiales. Univ. Calif. Publ. Bot. 32: 315–368.
Feldmann J. & Feldmann G. 1942. Recherches sur les Bonnemaisoniacées et leur alternance de
générations. Ann. Sci. Nat., Bot. 3: 75–175.
Hommersand M.H. 1986. The biogeography of the South African marine red algae: a model. Bot.
Mar. 29: 257–270.
Hommersand M.H. & Fredericq S. 1988. An investigation of cystocarp development in Gelidium
pteridifolium with a revised description of the Gelidiales (Rhodophyta). Phycologia 27: 254–
272.
Hommersand M.H. & Fredericq S. 1990. Sexual reproduction and cystocarp development. In: Biology
of the red algae (Ed. by K.M. Cole & R.G. Sheath), pp. 305–345. Cambridge University Press,
New York.
Huisman J.M., Ballantine D.L. & Wynne J.M. 2000. Liagorothamnion mucoides gen. et sp. nov.
(Ceramiaceae, Rhodophyta) from the Caribbean Sea. Phycologia 39: 507–516.
Jones W.E. & Smith R.M. 1970. The occurrence of tetraspores in the life history of Naccaria wiggii
(Turn.) Endl. Brit. Phycol. J. 5: 91–95.
Kylin H. 1928. Entwicklungsgeschichtliche Florideenstudien. Lunds Univ. Årsskr. Ny Följd, Andra
Afd. 24(4): 1–127.
Kylin H. 1956. Die Gattungen der Rhodophyceen. CWK Gleerups Förlag, Lund. 673 pp.
Lindstrom S.C. 1984. Neodilsea natashae sp. nov. (Dumontiaceae, Rhodophyta) with comments on
the family. Phycologia 23: 29–37.
Lindstrom S.C. 1987. Acrosymphytaceae, a new family in the order Gigartinales sensu lato
(Rhodophyta). Taxon 36: 50–53.
Millar A.J.K. 1990. Marine red algae of the Coffs Harbour region, northern New South Wales.
Austral. Syst. Bot. 3: 293–593.
Ormond R.F.G. & Banaimoon S.A. 1994. Ecology of intertidal macroalgal assemblages on the
Hadramout coast of southern Yemen, an area of seasonal upwelling. Mar. Ecol. Progr. Ser. 105:
105–120.
Pueschel C.M. & Cole K.M. 1982. Rhodophycean pit plugs: an ultrastructural survey with taxonomic
implications. Amer. J. Bot. 69: 703–720.
Saunders G.W. & Kraft G.T. 1997. A molecular perspective on red algal evolution: focus on the
Florideophycidae. Pl. Syst. Evol., Suppl. 11: 115–138.
Schils T. & Coppejans E. 2002. Gelatinous red algae of the Arabian Sea, including Platoma
heteromorphum sp. nov. (Gigartinales, Rhodophyta). Phycologia 41: 254–267.
Schils T., De Clerck O. & Coppejans E. 2001. Macroalgal assemblages of the Socotra Archipelago
with biogeographical notes on the Arabian Sea flora. Phycologia 40 (supplement): 50–51.
Svedelius N. 1933. On the development of Asparagopsis armata Harv. and Bonnemaisonia
asparagoides (Woodw.) Ag. A contribution to the cytology of the haplobiontic Rhodophyceae.
Nova Acta Regiae Soc. Sci. Upsal., Ser. 4: 1–61.
Tai V., Lindstrom S.C. & Saunders G.W. 2001. Phylogeny of the Dumontiaceae (Gigartinales,
Rhodophyta) and associated families based on SSU rDNA and internal transcribed spacer
sequence data. J. Phycol. 37: 184–196.
Wittmann W. 1965. Aceto-iron-haematoxylin–chloral hydrate for chromosome staining. Stain
Technol. 40: 161–164.
Womersley H.B.S. 1996. The marine benthic flora of southern Australia. Rhodophyta – Part IIIB.
Gracilariales, Rhodymeniales, Corallinales and Bonnemaisoniales. Australian Biological
Resources Study, Canberra. 392 pp.

Reticulocaulis in the Indian Ocean 65
Womersley H.B.S. & Abbott I.A. 1968. Structure and reproduction of Neoardissonea Kylin
(Rhodophyta, Naccariaceae). J. Phycol. 4: 173–177.
Wynne M.J. 1999a. Pseudogrinnellia barratiae gen. et sp. nov., a new member of the red algal family
Delesseriaceae from the Sultanate of Oman. Bot. Mar. 42: 37–42.
Wynne M.J. 1999b. New records of benthic marine algae from the Sultanate of Oman. Contr. Univ.
Michigan Herb. 22: 189–208.
Wynne M.J. 2000. Further connections between the benthic marine algal floras of the northern
Arabian Sea and Japan. Phycol. Res. 48: 211–220.
Wynne M.J. & Banaimoon S.A. 1990. The occurrence of Jolyna laminarioides (Phaeophyta) in the
Arabian Sea and the Indian Ocean and a new report of Melanothamnus somalensis
(Rhodophyta). Bot. Mar. 33: 213–218.
Wynne M.J. & Jupp B.P. 1998. The benthic marine algal flora of the Sultanate of Oman: new records.
Bot. Mar. 41: 7–14.
Zerlang O.E. 1889. Entwicklungsgeschichtliche Untersuchungen über die Florideengattungen
Wrangelia und Naccaria. Flora 72: 371–407.

66
Stoechospermum polypodioides (Lamouroux) J. Agardh: a common brown alga of the Arabian Sea, which is
frequently referred to by its synonym Stoechospermum marginatum (C. Agardh) Kützing.

Chamaebotrys erectus sp. nov. 67
CHAPTER 4
Chamaebotrys erectus sp. nov. (Rhodymeniales, Rhodophyta) from the Socotra
Archipelago, Yemen
Published as: Schils T., Huisman J.M. & Coppejans E. 2003. Chamaebotrys erectus sp. nov.
(Rhodymeniales, Rhodophyta) from the Socotra Archipelago, Yemen. Botanica Marina 46(1): in
press.
ABSTRACT
A third species of Chamaebotrys, C. erectus, is described from an upwelling region off
Socotra Island, Yemen. The new species clearly displays one of the defining features of the
genus, viz. terminal tetrasporangia in nemathecial sori. The nemathecia become diffuse when
mature and produce secondary tetrasporangia. Tetraspores can apparently germinate in situ,
resulting in compound thalli with tetrasporic and cystocarpic parts. Carpogonial branches are
four-celled and cystocarps are protuberant, both of which features illustrate the affinities of
Chamaebotrys with the closely related Coelarthrum.
I
NTRODUCTION
The genus Chamaebotrys was recently erected by Huisman (1996) for Coelarthrum
boergesenii Weber-van Bosse, the two features distinguishing it from the type species of
Coelarthrum, C. cliftonii (Harvey) Kylin, being the terminal, rather than intercalary
tetrasporangia and the nemathecial sori in which they occur (Huisman 1996). A second
species of Chamaebotrys is C. lomentariae (Tanaka et K. Nozawa in Tanaka) Huisman,
which is very imperfectly known only from the type collection. Both it and the type species
have low-growing, decumbent thalli of small stature. It was therefore of interest when
several relatively large, upright thalli referable to Chamaebotrys were collected from an
upwelling area off Socotra (Fig. 1). These specimens are herein described as the new species
C. erectus.
Fig. 1. Sampling stations around Socotra where Chamaebotrys erectus was collected: IT-059 (a); IT-103, type
locality (b); Alg-40 (c). Scale bar: 20 km.

68 Chapter 4
MATERIAL AND METHODS
Specimens were collected during two field trips to Socotra Island (Yemen; 12.47 N, 53.87 E)
from 13 January–20 February 1999 and 26 March–7 May 2000, respectively. The subtidal
habitats around the island were sampled while snorkelling or SCUBA diving. Specimens
were pressed on herbarium sheets and preserved in a 5% Formalin-seawater solution.
Herbarium sheets, liquid-preserved specimens and microscope slides are deposited in GENT.
Material for microscopical examination was stained with aniline blue. The anatomical and
reproductive characteristics were observed by studying transverse sections (made by hand or
with a freezing microtome set at 40 µm) and squashed preparations (whole-mounts in a
mixture of corn syrup and phenol, 50:1) under a standard light microscope (Leitz Diaplan,
Wetzlar, Germany). Line drawings were prepared with a camera lucida, and photographs
were taken with a digital camera (Olympus DP10, Melville, U.S.A.).
R
ESULTS
Chamaebotrys erectus Schils et Huisman, sp. nov.
Ad Chamaebotrydem boergesenii (Weber-van Bosse) Huisman similis sed characteribus
sequentibus distinguitur. Planta recta, ad 20 cm alta, sine anastomosibus inter ramos.
Tetrasporangia decussate divisa, in nematheciis irregulariter formatis portata. Tetrasporae
interdum in situ germinantes, thallum compositum facientes ex partis tetrasporicis
gametophyticis et cystocarpicis constantes. Spermatangia ignota.
Similar to Chamaebotrys boergesenii (Weber-van Bosse) Huisman but with the following
distinguishing characters: plants erect, to 20 cm tall, lacking anastomoses between branches.
Tetrasporangia decussately divided, in irregularly shaped nemathecia. Tetraspores
occasionally germinating in situ, resulting in a compound thallus comprised of tetrasporic,
gametophytic and cystocarpic parts. Spermatangia unknown.
HOLOTYPE: SOC 265 (GENT).
ETYMOLOGY: The specific epithet (L. erectus = upright) alludes to the upright habit of the
species.
TYPE LOCALITY AND SPECIMENS EXAMINED: Yemen, Socotra Island (Fig. 1): 5 February
1999, 10 km east of Rhiy di-Qatanhin (IT-059: 12.308 N, 53.658 E), shallow subtidal, leg. F.
Leliaert (SOC 028: tetrasporophyte and female gametophyte); 3 March 1999, 1 km southeast
of Ghubbah di-Net (IT-103: 12.425 N, 53.475 E; type locality), shallow subtidal, leg. F.
Leliaert (SOC 265: tetrasporophyte and female gametophyte); 30 April 2000, west of
Bidholih (ALG-40: 12.303 N, 53.843 E), subtidal: -20 m, leg. T. Schils (SMM 456: female
gametophyte).
HABIT AND VEGETATIVE STRUCTURE: Plants are upright, to 20 cm tall (Fig. 2), segmented,
and branch dichotomously or have a percurrent primary axis and verticillate laterals. Several
thalli, each with a short solid stipe (to 7 mm long and 1.5 mm wide), can arise from a single
discoid holdfast (to 3 mm diam.). Young branches and apical regions are bright red in colour
and older parts of the thallus are brownish red. Thalli are soft in texture and composed of
hollow, mucus-filled segments that are joined by narrow connections (Fig. 3). The shape of
the segments varies from subcylindrical near the apex to thick, elongate and barrel-shaped in

Chamaebotrys erectus sp. nov. 69
Figs 2-7. Chamaebotrys erectus sp. nov.
Fig. 2. Habit of holotype.
Fig. 3. Apical region showing the narrow and short connections between the segments.
Fig. 4. Section of cortex.
Fig. 5. Cortical section showing gland cells attached to a medullary cell.
Fig. 6. Surface view of cortex.

70 Chapter 4
Fig. 7. Compound thallus: cystocarpic axes (C) developing from tetrasporic segments (T).
Scale bars: Fig. 2, 1 cm; Fig. 3, 1 mm; Figs 4-6, 10 µm; Fig. 7, 1 mm.
older thallus parts. The inner medulla is composed of 1 or 2 layers of large, colourless cells
(22.5-125 µm [l] x 27-160 µm [w]; Fig. 4). Gland cells (6.5-20.5 µm in diam.) are borne
singly or in pairs on the inner surface of medullary cells (Fig. 5) or on stellate cells attached
to the medullary cells. Secondary internal filaments occasionally are initiated from the
medullary cells. The cortex is composed of 2-3 layers of subspherical pigmented cells (4.5-
18 µm in diam.), these gradually decreasing in size towards the thallus surface. Outer
cortical cells regularly bear hairs. Cortical cells in surface view are irregularly arranged (Fig.
6) and variable in diameter.
REPRODUCTIVE THALLI: The larger plants (e.g. SOC 265) are compound, composed of
tetrasporic and gametophytic/cystocarpic individuals (Fig. 7), the latter occurring distally on
the tetrasporophyte. Hence, it is suspected that the tetrasporangia germinate in situ and give
rise to gametophytic thalli. The process of tetraspore germination, singly or syntagmatically,
was not observed. Smaller, to 7 cm tall, entirely cystocarpic thalli also occur, indicating that
the tetraspores can also disperse from the mother plant and produce free-living
gametophytes.
CARPOGONIAL BRANCH AND CYSTOCARPS: Carpogonial branches are 4-celled and slightly
curved (Fig. 8). A cortical cell, attached to the supporting cell and with secondary pit
connections with adjacent cortical cells, acts as the auxiliary mother cell and initiates an
obovoid auxiliary cell (Fig. 9). Immediate post-fertilisation events have not been observed.
Upon presumed diploidisation of the auxiliary cell, the latter produces a stalked gonimoblast
(Fig. 10). Basal to the gonimoblast, nutritive cells are formed from the cells that surround the
supporting cell. Simultaneously, a protuberant pericarp surrounds the gonimoblast (Fig. 11).
SPERMATANGIA: Not observed.
TETRASPORANGIA: Tetrasporangia occur in nemathecial sori (Fig. 12). During maturation the
sori spread into irregular diffuse patches that can cover the greater part of the thallus. The
nemathecia are composed of slender filaments (Fig. 13) that arise from outer cortical cells
and cut off distal tetrasporangia. Sterile filaments occur among the tetrasporangial filaments.
After releasing the first order of tetrasporangia, secondary nemathecial filaments can be
produced which give rise to secondary tetrasporangia in more elevated sori. Tetrasporangia
develop from darkly staining elliptical initials 13.5-25 µm [l] x 6.5-14 µm [w] (Fig. 13). The
first division is transverse and oblique, with subsequent divisions splitting the two halves
longitudinally at right angles to one another, resulting in decussately divided tetrasporangia
27-41 µm x 20-25 µm.
HABITAT: Plants are epilithic on bare or sand inundated rocks. The associated subtidal
macroalgal flora is composed of Asteromenia peltata (W. R. Taylor) Huisman et Millar,
Botryocladia leptopoda (J. Agardh) Kylin, Carpopeltis maillardii (Montagne et Millardet)
Chiang, Champia indica Børgesen, Chondria armata (Kützing) Okamura, Dictyota
cervicornis Kützing, Euptilota fergusonii Cotton, Hypnea boergesenii Tanaka, Lobophora
variegata (Lamouroux) Womersley ex
Oliveira, Sarcodia montagneana (J. Hooker et
Harvey) J. Agardh, Scinaia moniliformis J. Agardh, Sebdenia flabellata (J. Agardh)
Parkinson, and Udotea indica A. Gepp et E. Gepp.

Chamaebotrys erectus sp. nov. 71
Figs 8-9. Chamaebotrys erectus sp. nov.
Fig. 8. Four-celled carpogonial branch.
Fig. 9. Initiation of a cystocarp: auxiliary
mother cell (am), auxiliary cell (aux) and
carpogonial branch remnants (arrow).
Scale bars: 10 µm.
DISCUSSION
Chamaebotrys erectus clearly displays the key characteristic of the genus, viz. terminal
tetrasporangia in nemathecial sori. The new species has morphological and anatomical
features similar to the other Chamaebotrys species and also to species of the closely related
Coelarthrum (Table 1). It can readily be distinguished from Chamaebotrys boergesenii and
C. lomentariae by its erect thallus, large size and compound thalli comprising tetrasporic,
gametophytic and cystocarpic parts (non-compound thalli also occur). In addition, C. erectus
produces occasional internal filaments, these being secondarily produced and not comparable
to longitudinal filaments of the Champiaceae (Ricker & Kraft 1979; Huisman 1995) and
Lomentariaceae (Lee 1978). Adventitious filaments have also been observed in Coelarthrum
species and not accorded taxonomic significance (Huisman 1996). The latter feature,
however, might prove to be of taxonomic importance in other Rhodymeniaceae genera, viz.
the absence of internal rhizoids in Chrysymenia and their presence in Cryptarachne
(generally lumped in Chrysymenia, e.g. Abbott & Littler 1969) might support the molecular
separation of both genera (Saunders et al. 1999, p. 38).

72 Chapter 4
Figs 10-13. Chamaebotrys erectus sp. nov.
Fig. 10. Section of cystocarp: broken-off gonimoblast (gb), pericarp (pc), nutritive tissue (nt).
Fig. 11. Protuberant cystocarp with a prominent ostiole.
Fig. 12. Surface view of irregularly contoured tetrasporangial nemathecia.
Fig. 13. Section of tetrasporial nemathecium showing medullary cells (mc), nemathecial filaments (nf)
and tetrasporangial initials (ti).
Scale bars: Fig. 10, 50 µm; Fig. 11, 0.5 mm; Fig. 12, 50 µm; Fig. 13, 20 µm.
In light of the recent molecular findings on the Rhodymeniales (Saunders et al. 1999), the
observation of a 4-celled carpogonial branch in Chamaebotrys erectus supports maintaining
the genus (which was not sequenced by Saunders et al. 1999) within the Rhodymeniaceae.
The genus is unusual in the Rhodymeniaceae, however, in producing terminal tetrasporangia
in nemathecia. This has been hypothesised as a reversion to the ancestral condition by
Saunders et al. (1999). Further molecular studies may elucidate the phylogenetic placement
of Chamaebotrys in relation to other Rhodymeniaceae.
Some tetrasporangia in C. erectus appear to be tetrahedrally divided, a result of the oblique
first division in combination with the decussate arrangement of the tetraspores. Nevertheless,
the divisions are always successive, a distinctive feature of cruciately (decussately) divided
tetrasporangia (Guiry 1978, 1990).

Chamaebotrys erectus sp. nov. 73

74 Chapter 4
In comparison to the reported sizes of the other Chamaebotrys species (Mshigeni &
Papenfuss 1981; Huisman 1996), C. erectus is markedly larger. All material was collected
from the south coast of Socotra, which is subject to upwelling of cold water. This
phenomenon is beneficial for algal growth (constant nutrient flow and stable temperature
regime), as the south coast harbours the most luxuriant and species-rich algal flora of the
Island (Schils et al. 2001). Analogous discoveries of large representatives of certain genera
from this upwelling region include Champia gigantea Wynne (1998), another member of the
Rhodymeniales. These findings suggest that the Arabian Sea harbours a distinctive and
interesting marine flora.
A
CKNOWLEDGEMENTS
We appreciated constructive comments from Gerry Kraft and an anonymous reviewer.
Sincere thanks are expressed to the Senckenberg Research Institute, Germany (Michael
Apel, Uwe Zajonz and Fareed Krupp), for the excellent field trip preparations to the Socotra
Archipelago. Frederik Leliaert is gratefully acknowledged for making his exquisite
collection of Socotran algae available. Tom Schils is indebted to the Fund for Scientific
Research Flanders (Belgium) for a research assistant grant and a travel grant to Murdoch
University (Western Australia). John Huisman thanks Associate Professor Michael
Borowitzka (Murdoch University) for hosting his research and Alex George (Four Gables,
Barclay St., Kardinya) for kindly supplying the Latin translations. Financial support was
provided by grants from the 'Australian Biological Resources Study' and the 'Western
Australian Department of Commerce and Trade'.
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J.H.), pp. 111-144. Systematics Association Special Vol. 10, Academic Press, London.
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Lee I.K. 1978. Studies on Rhodymeniales from Hokkaido. J. Fac. Sci. Hokkaido Univ., Ser. 5, Bot.
11: 1-194.
Mshigeni K.E. & Papenfuss G.F. 1981. Coelarthrum boergesenii (Rhodophycophyta,
Rhodymeniales): a new record from Tanzania. Bot. Mar. 14: 471-474.
Ricker R.W. & Kraft G.T. 1979. Morphology of the subantarctic red alga Cenacrum subsutum gen. et
sp. nov. (Rhodymeniales) from Macquarie Island. J. Phycol. 15: 434-444.
Saunders G.W., Strachan I.M. & Kraft G.T. 1999. The families of the order Rhodymeniales
(Rhodophyta): a molecular-systematic investigation with a description of Faucheaceae fam. nov.
Phycologia 38: 23-40.

Chamaebotrys erectus sp. nov. 75
Schils T., De Clerck O. & Coppejans E. 2001. Macroalgal assemblages of the Socotra Archipelago
with biogeographical notes on the Arabian Sea flora. Phycologia 40 (suppl.): 50-51.
Wynne M.J. 1998. Champia gigantea and Lomentaria strumosa (Rhodymeniales): two new red algae
from the Sultanate of Oman. Bot. Mar. 42: 571-580.
Wynne M.J. 2001. New records of benthic marine algae from the Sultanate of Oman, northern
Arabian Sea. II. Nova Hedwigia 72: 347-374.

76
Coelarthrum opuntia (Endlicher) Børgesen: a Rhodymeniales species (Rhodophyta) from the Arabian Sea,
which is closely related to the new species Chamaebotrys erectus Schils & Huisman (see chapter 4).

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 77
CHAPTER 5
A re-assessment of the genus Izziella Doty (Liagoraceae, Rhodophyta)
Published as: Huisman J.M. & Schils T. 2002. A re-assessment of the genus Izziella Doty
(Liagoraceae, Rhodophyta). Cryptogamie Algologie 23(3): 237-249.
ABSTRACT
The genus Izziella Doty is reassessed based on an examination of a specimen of Liagora
orientalis J. Agardh (the species into which Izziella abbottiae Doty has been subsumed)
from the Socotra Archipelago, Yemen. This species shows marked differences from the type
species of Liagora [L. viscida (Forsskål) C. Agardh], Ganonema [G. farinosum
(Lamouroux) Fan & Wang], and Trichogloea [T. requienii (Montagne) Kützing] and we
therefore propose that Izziella be restored as an independent genus. It is our contention that
Liagora, as presently constituted, displays considerable variation in reproductive
morphology and should probably be divided into several smaller genera.
I
NTRODUCTION
The genus Izziella, with the single species I. abbottiae, was described by Doty in 1978 for
specimens collected from Oahu, Hawaiian Islands. The genus was thought to be closely
related to Liagora but differing primarily in the cluster of sterile filaments radiating from
the infra-supporting cell proximal to the developing gonimoblast. Doty (1978) gave a
detailed description of the post-fertilization events in the new genus, which he felt were
clearly unlike those of Liagora viscida (Forsskål) C. Agardh, the type of the genus Liagora.
Subsequent to the description of Izziella, the genus was subsumed into Liagora (Abbott
1990), who regarded its type species as synonymous with L. orientalis J. Agardh. Liagora
orientalis, originally described from Sri Lanka, is a widespread species that has been
reported from numerous localities in the tropical Indian and Pacific Oceans and the
Caribbean Sea (Abbott 1990).
Several authors have recently remarked on the variety of morphology and cystocarp types
presently included in Liagora (Kraft 1989; Huisman & Kraft 1994; Huisman in press),
suggesting that the differences are too great to be accommodated within a single genus. As a
result, Huisman & Kraft (1994) resurrected the previously rejected (Abbott 1984)
Ganonema for Ganonema farinosum (Lamouroux) Fan & Wang, and subsequent authors
have made further combinations in the genus (Huisman in press).
The present paper re-assesses the genus Izziella (= Liagora orientalis) in light of these
suggestions, concluding that the genus is worthy of recognition in a taxonomic scheme in
which Liagora is more narrowly defined. The eventual further subdivision of the latter
genus is also foreshadowed. This study is based primarily on a collection made by the
second author from the Socotra Archipelago, Yemen, in addition to type and authentic
specimens of Izziella abbottiae from Oahu, Hawaiian Islands.

78 Chapter 5
MATERIAL AND METHODS
Specimens were collected while snorkeling and preserved in approximately 5%
formalin/seawater. Portions of plants for microscopical examination were decalcified in 1N
HCl under a fume hood, washed in seawater, stained in 1% aniline blue, washed again in
seawater, then mounted in a 50% Karo (CPC International) corn syrup solution and
macerated or lightly squashed to separate the filaments. Herbarium specimens and slide
preparations are held in GENT (Ghent University Herbarium, Krijgslaan 281 - S8, 9000
Ghent, Belgium).
O
BSERVATIONS
SPECIMENS EXAMINED
: (1) Liagora orientalis - East Coast of Samha Island, Socotra
Archipelago, Yemen (ALG-19: 12° 09.72 N, 35° 05.08 E), subtidal at 1.5 m depth, 7 April
2000, T. Schils (SMM 183) (Fig. 1). (2). Izziella abbottiae (isotypes) – Kahanahaiki,
Waianae District, Oahu, Hawaiian Is., on surf zone sedimentary rock bench, 23 March,
1969, M. Doty (Doty 20591; MELU A037729, A037730). (3) Izziella abbottiae -
Kahanahaiki, Waianae, Oahu, Hawaiian Is., lower littoral, 10 February 1962, M. Doty &
H.B.S. Womersley (Doty 19630; AD A26006) (Fig. 2). (4) Liagora viscida - Banyuls,
France 7 July 1937, G. Mazoyer (AD A24190). (5). Liagora perennis – Maili Beach,
Waianae District, Oahu, Hawaiian Is., on intertidal bench, 26 April 2002, J. Huisman & D.
Spafford (IA 28727). (6) Ganonema farinosum – Swanzy, Oahu, Hawaiian Is., 12 April
2002, J. Huisman & D. Spafford, (IA 28712). (7) Ganonema farinosum – Hanauma Bay,
Oahu, Hawaiian Is. (IA 13871). (8) Liagora orientalis – Nanakuli, Oahu, Hawaiian Is., on
intertidal limestone bench, 5 April 1985, M. Cannon (IA 17183). (9, 10) Trichogloea
requienii - SSW tip of Rocher du Diamant (Diamond Rock), Martinique, (14º 26.94 N, 61º
02.41 W), 14 June 1995, D.S. Littler, M.M. Littler & B.L. Brooks (Littler 30916). E side of
island on a steeply angled beach, attached to beach rock , Green Turtle Key, Bahamas,
subtidal at 1 m depth, 28 March 1994, D.S. Littler and M.M. Littler (Littler 42001). (11).
Liagora ceranoides – Swanzy, Oahu, Hawaiian Is., 12 April 2002, J. Huisman & D.
Spafford (IA 28703).
HABIT: The Yemen plant (Fig. 1) is 22 cm in height, greyish/light green (when dried),
mucilaginous, and arises from a discoid holdfast 3 mm in diam. Percurrent primary axes
bear indeterminate lateral branches of similar form, both in turn bearing a further order of
numerous short lateral branches. Primary axes and major lateral branches are 1-2.5 mm in
diam., broader at the base and tapering gradually towards the apex. Secondary and short
lateral branches are 0.5-1 mm in diam. Calcification is moderate and farinose.
VEGETATIVE STRUCTURE: The thallus structure is multiaxial, with a central medulla of
hyaline longitudinal filaments 15-50 µm in diam. Assimilatory filaments are borne on
medullary filaments and are sparsely dichotomously branched, often with lengthy
unbranched sections. The filaments are 450-600 µm long, with cells 7-16 µm in diam.,
lower cells cylindrical, upper cells ellipsoidal or obovoid. Narrow rhizoidal filaments, 6-10
µm in diam., commonly arise from the lower cells of assimilatory filaments and course
through the medulla, producing adventitious secondary assimilatory filaments that are
generally simple or rarely branched. Cells of assimilatory filaments have a prominent
central pyrenoid, 4-7 µm in diam.

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 79
Fig. 1. Specimen of Izziella orientalis (J. Agardh) Huisman & Schils, comb. nov. from Yemen (SMM 183).
Scale = 2 cm.
Fig. 2. Authentic specimen of Izziella abbottiae Doty (= I. orientalis) from Oahu, Hawaiian Is. (AD
A26006). Scale = 2 cm.
CARPOGONIAL BRANCH AND CARPOSPOROPHYTE
: Carpogonial branches are 3-4-celled
(Fig. 3) and arise on the distal half of the supporting cell, which is a lower cell of an
assimilatory filament. Following presumed fertilization the zygote (= post-fertilization
carpogonium) divides transversely (Fig. 4). Of the two cells produced, the proximal remains
undivided, while the distal cell undergoes several further transverse divisions (Fig. 5). Each
of the resultant cells produces lateral gonimoblast filaments that are whorled around the
central cells (Figs 5, 6). Gonimoblast filaments are very narrow, 2-3 µm in diam., with

80 Chapter 5
terminal carposporangia 5-7 µm long and 3-5 µm in diam. After release of carpospores, the
sporangial walls persist and remain obvious. Mature gonimoblasts are spherical, 100-220
µm in diam., and are located primarily in the short lateral branches of the thallus (Fig. 7).
Figs 3-6. Izziella orientalis (J. Agardh) Huisman & Schils
Fig. 3. Three-celled carpogonial branch borne on an assimilatory filament. (SMM 183). Scale = 20 µm.
Fig. 4. Post-fertilization division of the zygote. The first transverse division (arrowhead) is followed by
subsequent divisions of the distal cell. Sterile filaments are present on the cells distal and proximal to
the supporting cell (SMM 183). Scale = 20 µm.
Fig. 5. Later stage showing several divisions of the distal cell and initiation of lateral gonimoblast
filaments. (SMM 183). Scale = 20 µm.
Fig. 6. Young gonimoblast. The sporangial mass is shown in optical section, demonstrating the
presence of the longitudinal core arising from the cells of the divided zygote. The sterile filaments are
forming a separate cluster below the gonimoblast (SMM 183). Scale = 20 µm.
Prior to fertilization, and perhaps independent to it, sterile filaments are produced from
the cells to either side of the supporting cell (occasionally also from more distant cells) (Fig.
4). A whorl of sterile filaments arises from the distal end of the cell proximal to the
supporting cell, and occasionally some additional, less branched, filaments arise from the
mid-portion of the cell. These latter filaments are frequently reduced to only a single
globose cell. The sterile filaments (from the cells distal and proximal to the supporting cell)
grow towards each other and eventually envelop the supporting cell, producing a cluster of
filaments that appear as a second cell mass below the gonimoblast (Figs 6, 9). After
fertilization an extensive fusion cell is formed that encompasses the cells of the carpogonial
branch, the supporting cell, and the majority of cells of the assimilatory filament subtending
the supporting cell (Fig. 9). This fusion cell increases in length and girth and becomes
hyaline, eventually appearing as a 'stalk' bearing the gonimoblast (Figs 8, 9). The fused cells
of the carpogonial branch can be seen as a core within the gonimoblast. The lengthening
stalk raises the gonimoblast to the level of the outer margin of the assimilatory filaments.

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 81
Figs 7-9. Izziella orientalis (J. Agardh) Huisman & Schils
Fig. 7. Decalcified squash preparation of a short lateral branch, showing the numerous cystocarps.
(SMM 183). Scale = 200 µm.
Fig. 8. Closer view, showing gonimoblasts terminating elongate stalk cells. (SMM 183). Scale = 100
µm.
Fig. 9. Detail of mature cystocarp with distal gonimoblast mass, small cluster of sterile filaments, and
elongate stalk cell. (SMM 183). Scale = 50 µm.
Fig. 10. Liagora viscida (Forsskål) C. Agardh. Mature cystocarp with somewhat diffuse gonimoblast and
intermingled sterile filaments. (AD 24190). Scale = 20 µm.
DISCUSSION
The vegetative morphology and reproductive development observed in the present specimen
are entirely consistent with those described by Doty (1978, as Izziella abbottiae) and Abbott
(1990, 1999, as Liagora orientalis) and as observed in type and other specimens recorded
by Doty (1978) as I. abbottiae (MELU A037729, A037730; AD 26006). We have also
examined a slide preparation of a type specimen of Liagora orientalis, held in the Botany
Department, University of Hawaii, Manoa (see Abbott 1990 for details). We are therefore
confident that our material is representative of that species as it conforms to the type and
other specimens of L. orientalis examined by us and described in detail by Abbott (1990).
Based on observations of the type species of Liagora, L. viscida (Huisman, in press), we
feel that L. orientalis is incorrectly placed in Liagora and we have undertaken a
comparative morphological examination of potentially related genera. Four genera are
considered: Liagora (type species Liagora viscida), Izziella (type species I. abbottiae =
Liagora orientalis), Ganonema (type species G. farinosum), and Trichogloea (type species
T. requienii). The latter is included as the appearance of the mature cystocarp is
superficially similar to that of L. orientalis. Abbott (1995) included Trichogloea javensis
Børgesen (1951: 22-26) as one of the synonyms of L. orientalis, but an examination of the
type specimen shows it to be correctly placed in Trichogloea. Trichogloea javensis is
therefore excluded from the synonymy of L. orientalis. Characteristics of the type species of

82 Chapter 5
these four genera are given in Table 1. Figures 11-22 show examples of these characteristics
(Liagora perennis Abbott is used instead of L. viscida for illustrative purposes).

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 83
Figs 11-13. Liagora perennis Abbott (all IA 28727).
Fig. 11. Cortical filaments and spermatangia, showing much-divided filaments and apical/subapical
spermatangial branches. Scale = 20 µm.
Fig. 12. Lateral carpogonial branch. Scale = 20 µm.
Fig. 13. Mature cystocarp with somewhat diffuse gonimoblast and intermingled sterile filaments. Scale
= 50 µm.
Figs 14-16. Ganonema farinosum (Lamouroux) Fan & Wang
Fig. 14. Cortical filaments, showing undivided filaments of the outer cortex. (IA 28712). Scale = 100
µm.
Fig. 15. Spermatangial branches in dense heads. (IA 28712). Scale = 100 µm.
Fig. 16. Cystocarp with compact gonimoblast mass and sterile filaments forming an involucre. (IA
13871). Scale = 50 µm.

84 Chapter 5
Figs 17, 18. Izziella orientalis (J. Agardh) Huisman & Schils
Fig. 17. Cortical filaments, showing sparsely branched filaments of the outer cortex. (IA 17183). Scale
= 50 µm.
Fig. 18. Spermatangial branches formed on apical/subapical cells. (IA 17183). Scale = 50 µm.
Figs 19-22. Trichogloea requienii (Montagne) Kützing
Fig. 19. Cortical filaments with spermatangia borne in whorls on lower cells. (Littler 42001). Scale = 50
µm.
Fig. 20. Straight, many-celled, carpogonial branch and cortical filaments, showing undivided filaments
of the outer cortex. (Littler 30916). Scale = 50 µm.
Fig. 21. Post-fertilization division of the carpogonium and production of sterile filaments from lower
cells of the carpogonial branch. Scale = 20 µm.

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 85
Fig. 22. Mature cystocarp formed at the end of the carpogonial filament, with sterile filaments borne
on the lower cells of the carpogonial filament. (Littler 30916). Scale = 20 µm.
Fig. 23. Liagora ceranoides Lamouroux. Showing compact gonimoblast and involucral filaments. (IA
28703). Scale = 50 µm.
This comparison suggests that, based on the type species, the four taxa are clearly
separable. While several features are included in Table 1, those that we consider of primary
importance are the cortical structure, the architecture of the carpogonial branch and mature
cystocarp, and the derivation of spermatangia. Our observations indicate that L. orientalis
should no longer be maintained in Liagora. A comparison of the mature cystocarps of L.
orientalis (Fig. 9) and L. viscida (Fig. 10) shows differences in morphology sufficient to
warrant placement in separate genera. The cystocarp of Liagora viscida has a somewhat
diffuse gonimoblast in which sterile filaments are intermingled, whereas that of L. orientalis
is compact and the sterile filaments form a discrete cluster below the gonimoblast. The
presence of an elongate 'stalk cell' subtending the gonimoblast further distinguishes L.
orientalis, as fusion cells in the genus Liagora only involve the cells of the carpogonial
branch and are small in comparison.
We therefore conclude that Liagora orientalis is generically distinct from Liagora. Since
Izziella Doty (1978) was based on this taxon (as I. abbottiae), we propose that the genus
should be reinstated. We therefore make the following emendation and combination:
Izziella Doty emend. Huisman & Schils
Plants mucilaginous, moderately calcified, with percurrent primary and indeterminate lateral
branches of similar form, or irregularly branched. Structure multiaxial; assimilatory
filaments sparsely dichotomously branched, often with unbranched outer cortical filaments.
Carpogonial branches lateral on supporting cells. Mature gonimoblasts spherical, compact.
Sterile filaments arising from cells to either side of the supporting cell, growing towards
each other and enveloping the supporting cell, eventually producing a cluster of filaments
that appear as a second cell mass below the gonimoblast. Fusion cell formed encompassing
the cells of the carpogonial branch, the supporting cell, and the majority of cells of the
assimilatory filament subtending the supporting cell. Spermatangia borne on short
spermatangial branches arising on apical or subapical cortical cells.
Izziella orientalis (J. Agardh) Huisman & Schils, comb. nov.
BASIONYM: Liagora orientalis J. Agardh. Analecta algologica, p. 99 (1896).
LECTOTYPE: From Sri Lanka, W. Ferguson (LD 32252). n.v., fide Abbott, 1990: fig. 7.
SYNONYMS (fide Abbott, 1990; Abbott, 1995; Abbott, 1999; excluding Trichogloea
javensis Børgesen):
Liagora formosana Yamada, Scientific Papers of the Institute of Algological Research,
Faculty of Science, Hokkaido Imperial University 2: 32-33 (1938).
Liagora tanakai I.A. Abbott, Bulletin of the Japanese Society of Phycology 15: 33 (1967).
Liagora visakhapatnamensis Umamaheswara Rao, Hydrobiologia 33: 201 (1969).
Izziella abbottiae Doty, Phycologia 17: 34 (1978).

86 Chapter 5
As a further consequence of our observations, we feel that Liagora should be restricted to
species with much-divided cortical filaments, lateral carpogonial branches, cystocarps with
somewhat diffuse gonimoblasts wherein the sterile filaments intermingle or loosely envelop,
and spermatangia borne on terminal or subterminal spermatangial branches. Izziella, in
contrast, has cortical filaments that are often distally simple, compact gonimoblasts, and
sterile filaments that form a separate cluster below the gonimoblast. This latter feature is
superficially similar to that of Trichogloea, but the ontogeny of these structures is entirely
different. Those of Trichogloea are derived from mid-cells of the elongate carpogonial
branch, whereas the sterile filaments of Izziella arise from the cells to either side of the
supporting cell.
Although the characteristics shown in Table 1 outline the differences between the four
genera, consideration of other species of Liagora does demonstrate what could be regarded
as a continuum of character states. Species such as Liagora ceranoides Lamouroux have
close affinities with Izziella, as both display compact gonimoblasts (Fig. 22) and fusion
cells. Liagora ceranoides differs from Izziella, however, in the production of in involucre
that envelopes the gonimoblast (Huisman in press) and in lacking a large stalk cell. It is our
contention that Liagora, as presently constituted, should be subdivided into several smaller
genera. One of these segregate genera would include species with compact gonimoblasts,
such as L. ceranoides. The subdivision of Liagora was also suggested by Huisman & Kraft
(1994) and Huisman & Wynne (1999), although no generic boundaries were indicated.
Preliminary DNA sequence studies (Huisman, Saunders & Harper in prep.) indicate that
Liagora is indeed polyphyletic and support its subdivision into more precisely defined units.
Further work on a range of species, however, is required before any additional taxonomic
and nomenclatural revisions can be made.
A
CKNOWLEDGEMENTS
John Huisman acknowledges the financial support of the 'Australian Biological Resources
Study' and the 'Western Australian Department of Commerce and Trade' while at Murdoch
University, where Associate Professor Michael Borowitzka hosted his research. While at the
University of Hawaii, Manoa, JH was supported by a grant from the David and Lucile
Packard Foundation, and sincerely thanks Dr Isabella Abbott for her support. Dave Spafford
is thanked for his able diving support. Tom Schils expresses his sincere thanks to the
Senckenberg Research Institute, Germany (Michael Apel, Uwe Zajonz and Fareed Krupp),
for the excellent field trip preparations to the Socotra Archipelago, and is indebted to the
Fund for Scientific Research Flanders (Belgium) for a research assistant grant and a travel
grant to Murdoch University (Western Australia). Gerry Kraft (University of Melbourne) is
thanked for his numerous suggestions that greatly improved the manuscript, and for
information regarding the isotype specimen of Izziella abbottiae housed in MELU.
Professor Bryan Womersley and the State Herbarium of South Australia are thanked for the
loan of authentic Izziella abbottiae.

Re-assessment of Izziella (Liagoraceae, Rhodophyta) 87
R
EFERENCES
Abbott I.A. 1967. Liagora tanakai, a new species from southern Japan. Bull. Jap. Soc. Phycol. 15: 32-
37.
Abbott I.A. 1984. Two species of Liagora (Nemaliales, Rhodophyta) and notes on Liagora farinosa
Lamouroux. Amer. J. Bot. 71: 1015-1022.
Abbott I.A. 1990. A taxonomic assessment of the species of Liagora (Nemaliales, Rhodophyta)
recognized by J. Agardh, based upon studies of type specimens. Cryptog. Bot. 1: 308-322.
Abbott I.A. 1995. A new "tetrasporangial" species of Liagora (Rhodophyta, Nemaliales) from
Hawai'i. Chin. J. Limnol. Oceanogr. 13: 343-347.
Abbott I.A. 1999. Marine red algae of the Hawaiian Islands. Bishop Museum Press, Honolulu,
Hawaii. 477 pp.
Agardh J.G. 1896. Analecta algologica. Continuatio III. Lunds Univ. Årsskr., Andra Afd., Kongl.
Fysiogr. Sällsk. Lund Handl. 32: 1-140.
Børgesen F. 1951. Some marine algae from Mauritius. Additions to the parts previously published, III.
Kongel. Danske Vidensk. Selsk. Biol. Meddel. 18: 1-44.
Doty M.S. 1978. Izziella abbottae, a new genus and species among the gelatinous Rhodophyta.
Phycologia 17: 33-39.
Huisman J.M.. The type and Australian species of the red algal genera Liagora and Ganonema
(Liagoraceae, Nemaliales). Austral. Syst. Bot. (in press).
Huisman J.M. & Kraft G.T. 1994. Studies of the Liagoraceae (Rhodophyta) of Western Australia:
Gloiotrichus fractalis gen. et sp. nov. and Ganonema helminthaxis sp. nov. Eur. J. Phycol. 29:
73-85.
Huisman J.M. & Wynne M.J. 1999. Liagora tsengii sp. nov. (Liagoraceae, Rhodophyta) from Lesser
Antilles, West Indies. Bot. Mar. 42: 219-225.
Kraft G.T. 1989. Cylindraxis rotundatus gen. et sp. nov. and its generic relationship within the
Liagoraceae (Nemaliales, Rhodophyta). Phycologia 28: 275-304.
Umamaheswara Rao M. 1969. Liagora visakhapatnamensis, a new species from India. Hydrobiologia
33: 201-208.
Yamada Y. 1938. The Species of Liagora from Japan. Sci. Pap. Inst. Algol. Res. Fac. Sci. Hokkaido
Imp. Univ. 2: 1-34.

88
Sebdenia flabellata (J. Agardh) Parkinson: a red alga from the upwelling shores of Masirah Island and the
Socotra Archipelago.

Subtidal communities around Socotra 89
CHAPTER 6
Spatial variation in subtidal plant communities around the Socotra Archipelago and
their biogeographic affinities within the Indian Ocean
To be published as: Schils T. & Coppejans E. 2003. Spatial variation in subtidal plant communities
around the Socotra Archipelago and their biogeographic affinities within the Indian Ocean. Marine
Ecology Progress Series: accepted.
ABSTRACT
The subtidal plant communities of the Socotra Archipelago were studied by means of
quadrat sampling. Ordination and statistic analyses reveal six distinct entities corresponding
to the geographic location and the physico-chemical factors. The north coast of Socotra
Island is composed of common Indian Ocean algae, with an intermediate species richness
and alpha diversity for the archipelago. This entity also includes two species-poor sub-
entities: the seagrass beds and the coral-dominated communities. The transition zone is an
overlapping area between Socotra’s north and south coast, showing the highest similarity in
community structure with the upwelling flora of the south coast owing to similar
environmental conditions. In addition, this zone is subject to intense current patterns
favouring a pronounced diversity in red algae. The south coast totals the highest number of
recorded species, a lower affinity with the (sub)tropical Indian Ocean flora and is marked by
disjunctly distributed species. The plant communities of the outer islands comprise a mixture
of the previous entities due to the drastically changing seasonal environmental conditions in
a limited coastal area. The intermediate character of this entity, ongoing competition
amongst biota without reaching a climax in the vegetation succession, is reflected in the
vegetation analyses and the biogeographic comparison.
I
NTRODUCTION
The Socotra Archipelago (12.47°N, 53.87°E; Yemen) is situated in the southwestern part of
the Arabian Sea (Fig. 1) and is affected by various gyres and eddies that result in upwelling
during the SW monsoon in summer. The south coast of the main island is particularly
influenced by the upwelling phenomenon, whereas the north coast is typified by warmer
water with less temperature fluctuations. Biogeographic studies of Socotra’s marine fauna
(Kemp 1997, 1998b) show that many species are widespread throughout the Indo-Pacific and
the Red Sea. In addition, the diverse habitats of the archipelago constitute an important
refuge for closely related species from the Indian Ocean, Arabian Sea, Red Sea and Gulf of
Aden (sympatry). Many species of the surrounding seas have their outermost distribution
limits around Socotra, making it an important haven for larval stages and their dispersal
throughout the Indian Ocean, the Red Sea and the Arabian Sea. Kemp (1998b) concluded
that this southern Arabian region might be an extension of the upwelling region of Oman,
characterized by a distinct species composition and a pronounced degree of endemism
(Sheppard & Salm 1988, Randall & Hoover 1995).

90 Chapter 6
Fig. 1. Geographic position of the Socotra archipelago, with the indication of the sampling sites (black
dots) and the DCA clusters: the seagrass beds (SGB), the coral dominated communities (CDC), Socotra’s
north coast (SNC), the transition zone (TZ), Socotra’s south coast (SSC), and the outer islands (OI). Scale
bar represents 25 km.
Despite limited studies on Arabian Sea macroalgae, Børgesen (1934) had already
commented on the peculiar flora and its biogeographic affinities with distant regions. In the
1990’s renewed interest in the marine biology of the region arose, including phycological
studies. Ormond & Banaimoon (1994) studied the algal assemblages in relation to physico-
chemical characteristics along the upwelling coast of Hadramout (Yemen). During the same
period, numerous taxonomic studies on the seaweeds of upwelling areas in Oman were
initiated by Wynne (Wynne & Banaimoon 1990, Wynne & Jupp 1998, Wynne 1998, Wynne
1999a, b, Wynne 2001). The large number of new records and newly described species in
these studies illustrate the lack of knowledge of the Arabian Sea flora. Early phycological
studies on the Socotra Archipelago are limited to Dickie (1888) and Holmes (1903), who
reported 27 marine algae for Socotra Island and Abd al-Kuri. More recent studies focussed
on specific taxonomic, systematic and ecological issues of Socotra’s macroalgal flora (Kemp
1998a, Wynne & Leliaert 2001, Schils & Coppejans 2002, Schils et al. 2002). In an effort to
protect the relatively pristine marine and terrestrial natural heritage of the Socotra
Archipelago (United Nations Development Programme for the sustainable use and
conservation of the Socotra Archipelago) an interdisciplinary team of scientists studied the
vulnerable and endangered ecosystems and species around the archipelago. The resulting
taxonomic and ecological studies highlighted the diversity and the pristine nature of the
marine habitats. The present study is an ecological follow-up and aims at identifying the
main plant communities around these islands, analysing their species composition and
biogeographic affinities.
M
ATERIALS AND METHODS
Macroalgal and seagrass communities around the Socotra Archipelago were sampled in
spring 2000 (26 March – 7 May). A total of 82 vegetation quadrats from 21 sites (Fig. 1;
Appendix 1) were used to compare the different algal assemblages of the main island, Abd
al-Kuri and Samha. At each site homogeneous macroalgal assemblages on subtidal
platforms, ranging from –5 to –15 m depth, were selected, in which the quadrats (0.25 m
2
)
were randomly placed. Upon recording the species by means of Braun-Blanquet’s combined
estimation (Table 1), the quadrats were cleared and the algae were gathered in fine-meshed
plastic bags. In the field laboratory, the mesh bags were sorted by species and fresh weight
(including the rhizomes of the seagrasses) was measured with a dynamometer. Small and
crustose algae are excluded from the analyses as their biomass is hard to determine and a
meticulous investigation of the whole substratum and epiphytes is too time-consuming.

Subtidal communities around Socotra 91
Representative specimens were pressed as herbarium specimens, preserved in a 5%
formaldehyde-seawater solution or dried in silica gel for molecular purposes. The reference
collection is lodged in GENT (Ghent University Herbarium, Krijgslaan 281 - S8, 9000
Ghent, Belgium).
Table 1. Braun-Blanquet’s combined estimation and the transformed scale of Braun-Blanquet (van der
Maarel 1979, Schaminée et al. 1995).
Braun-Blanquet’s combined
estimation
van der
Maarel
No of individuals Cover Code Code
rare < 5% r 1
few < 5% + 2
many < 5% 1 3
abundant < 5% 2 4
arbitrarily 5 - 25% 2 4
arbitrarily 25 - 50% 3 5
arbitrarily 50 - 75% 4 6
arbitrarily > 75% 5 7
Ordination
The biomass data was selected as the most informative ordination input. Before ordination,
the biomass data was log transformed and rare species were downweighted. Detrended
Correspondance Analysis (DCA performed with CANOCO; ter Braak 1988) was chosen as
an indirect gradient analysis as: (i) the data clearly represent a unimodal model (maximum
gradient length: 7.615 SD; ter Braak & Šmilauer 1998) and (ii) the Correspondance Analysis
(CA) showed a pronounced arch effect.
In an attempt to determine the species-environment correlation, environmental data around
Socotra (latitude: 9.650°N – 14.383°N; longitude: 51.900°E – 57.067°E) were obtained from
the Worldwide Ocean Optics Database (http://wood.jhuapl.edu, W.O.O.D. version 4.0).
Chlorophyll a (CHL), nitrate (NO
3
), nitrite (NO
2
), oxygen (OX), phosphate (PO
4
), salinity
(SAL), silicate (SiO
4
) and temperature (TEMP) parameters showed a good sample
distribution for the area. All these parameters were sampled for the SW monsoon (Julian
days 121-304) and the NE monsoon (Julian days 305-120) and the average of a parameter
during one of both periods was calculated for 3 geographic areas around the archipelago
(zone 1: > 12.335°N; zone 2: < 12.335°N and > 53.835°E; zone 3: < 12.335°N and <
53.835°E). The water masses of these 3 areas affect the greater part of the coastal waters in
respect to their physico-chemical properties. Additional parameters were derived from the
original data, i.e. the absolute difference of a parameter between the 2 monsoon periods
(abbreviation of the environmental parameter + “_AD”) and the average between the periods
(parameter + “_AV”). Thus, this environmental data set has identical parameter values for all
sites of a specific area (corresponding with the DCA clusters). To tackle this lack of
resolution in the environmental data, a pseudo-environmental data set, composed of the
latitude (LAT_N) and longitude (LON_E) coordinates of the quadrats, was used. The idea is
that the species-GIS correlation might be indicative for environmental gradients that vary

92 Chapter 6
according to the geographic position around the archipelago. All parameters have been
standardized to zero mean and unit variance.
Less informative ordination inputs, species records in a van der Maarel scale (deduced
from the Braun-Blanquet cover data; Table 1) and species presence/absence, were tested
against the ordination results of the biomass data for each species within a quadrat.
Statistics
Subsequent analyses of the DCA clusters (plant communities) include the calculation of
species richness per quadrat, total biomass per quadrat, alpha diversity per quadrat
(BioDiversity Professional Version 2: Fisher’s log-series alpha; Fisher et al. 1943) and beta
diversity (the Jaccard Coefficient as a qualitative index: S
j
= a (a+b+c)
-1
a = # species
shared between two clusters, b = # species restricted to the first cluster, c = # species
restricted to the second cluster; and the Similarity Ratio as a quantative index: SR
ij
= S
k
y
ki
y
kj
(S
k
y
ki
2
+S
k
y
kj
2
-S
k
y
ki
y
kj
)
-1
, y
ki
= biomass of species k in cluster i, y
kj
= biomass of species k in
cluster j). The species richness was square root
-1
transformed, total biomass and Fisher’s
alpha were natural log transformed prior to variance analysis in order to achieve normality
and homogeneity of variances. Analyses of variance with the Tukey HSD test (Zar 1996) for
post hoc multiple comparisons were performed with SPSS for Windows 11.0.1 (SPSS Inc.
2001).
Biogeography
The biogeographic affinity of Socotra’s subtidal plant communities are analysed by
comparing the species composition of the DCA clusters to species inventories of Indian
Ocean countries. The latter data set is primarily based on Silva et al. (1996) and
supplemented with records from recent papers. The floristic affinity of a cluster with a
specific country is calculated as the Simpson Coefficient: a (a+ min (b, c))
-1
x 100. In which
a represents the number of shared species between a cluster and a country, b and c represent
the number of species unique to the cluster and the country, respectively. The species
inventories of the clusters are always smaller than those of the countries, so the equation
does not include the floristic richness of a country as it is irrelevant in a study restricted to
subtidal surveys, and it reduces the discrepancy of sampling efforts between the different
countries. The countries are arranged from southeast Africa, over the Arabian Sea, to
Western Australia. India was excluded from the series as its size and geographic position
cover a wide diversity of floras within the Indian Ocean.
R
ESULTS
Species account
A total of 127 plant species [3 seagrasses, Magnoliophyta; 29 Chlorophyta; 26 Phaeophyta;
69 Rhodophyta] are recorded for the 82 subtidal quadrats (Appendix 2). This corresponds
with a Cheney’s ratio [(R+C)/P] of 3.8.

Subtidal communities around Socotra 93
Fig. 2. First two ordination axes of a DCA
based on the log transformed biomass data
of the subtidal plants (black dots) in the
different quadrats (grey circles), rare species
are downweighted.
Fig. 3. First two ordination axes of the
second DCA in which the quadrats of SGB
and CDC are excluded (log transformed
biomass data and downweighting of rare
species). Cluster abbreviations as in Fig. 1.
Arrows indicate the quadrats of ANC. Black
dots represent plant species, grey circles
represent quadrats.
Ordination
The DCA of the biomass data of the 82 quadrats shows 6 distinct site groupings (Fig. 2),
which correspond well with their geographic position around the archipelago (Fig. 1). Both
axes have high eigenvalues (0.781 and 0.688) and together they represent 14.8 % of the
variation in species composition. The plot reflects the geographic position of the sample
stations within the archipelago, presumably relating to the physico-chemical characteristics
of the water mass. This is shown in the high correlation of the latitude coordinates (-0.7285)
with the first and the longitude (0.4514) with the second DCA axis. Both axes have a large
length of gradient (7.442 and 6.860), indicating the high ß-diversity between the quadrats of
the different communities. The following clusters can be discerned (Fig. 2): the seagrass
beds (SGB), the coral dominated communities (CDC), Socotra’s north coast (SNC), the
transition zone at the eastern extremity of Socotra Island (TZ), Socotra’s south coast (SSC)
and the outer islands (OI). The DCA shows a gradual change in species composition from
SNC, over TZ, to SSC. The latter is characterized by a high number of species, many
restricted to this zone for the archipelago (the aggregation of species around SSC in the
biplot; Fig. 2). OI constitutes a distinct cluster, intermediately positioned along the gradient
from SNC, over TZ to SSC. The quadrats of SGB and CDC also constitute 2 distinct clusters

94 Chapter 6
in the DCA. The plant communities of these two clusters differ substantially in species
composition, biomass and species richness from the other DCA clusters (see below),
potentially distorting the affinities of the remaining quadrats, hence their exclusion in the
subsequent DCA.
The second DCA (axes 1 and 2, respectively: eigenvalues, 0.732 and 0.469; lengths of
gradient, 5.513 and 3.876; cumulative % variance of species data, 9.6 and 15.7) revealed the
same clusters as the previous analysis (Fig. 3). Though, the quadrat clusters are less
geographically distributed in the biplot in comparison to the first DCA: high correlation of
latitude (0.743) and longitude (0.490) coordinates with the first and less (0.199 and 0.291,
respectively) with the second DCA axis. The difference between SNC, SSC and OI is
principally determined by the first DCA axis. Perspective to the first axis, TZ and a few
quadrats of the north coast of Abd al-Kuri (ANC; Fig. 3: arrows) are intermediate between
SSC and SNC. The second axis mainly discerns SNC and SSC, from OI, and TZ. The second
axis might be interpreted as the variability in current velocity and direction within a season:
velocities are very high and the direction is rather irregular at TZ, somewhat less variable at
OI, and more regular (although seasonally variable) at SSC and SNC. The low value of ANC
for the second axis corresponds with the sheltered position of the site. This diversity in
current patterns around the archipelago shapes the substratum (steep rocky shorelines with
numerous microhabitats e.g. crevices, sand deposition, etc.), which in turn determines algal
composition.
Table 2. Correlation coefficients of the environmental parameters with the first two axes of the second
DCA of biomass data. Absolute coefficient values in decreasing order for the first axis. Abbreviations of
parameters as in text.
Parameter Axis 1 Axis 2 Parameter Axis 1 Axis 2
PO4_SW -0.7650 -0.0997 NO3_AD -0.7146 -0.2765
PO4_AD -0.7648 -0.0722 CHL_AD -0.7135 -0.2784
SAL_SW 0.7628 0.1315 SAL_AD -0.6893 0.1533
TMP_SW 0.7610 0.1452 NO3_SW -0.6831 -0.3230
PO4_NE 0.7608 0.0313 CHL_NE 0.6440 0.3667
TMP_AD -0.7567 -0.0085 NO3_AV -0.5833 -0.4173
NO3_NE 0.7493 -0.0216 PO4_AV -0.5770 -0.4218
OXY_AV 0.7473 -0.0283 SAL_AV 0.5351 0.4481
OXY_AD 0.7445 -0.0373 NO2_SW -0.5046 0.3462
OXY_NE 0.7437 -0.0396 LON_E 0.4904 0.2910
LAT_N 0.7433 0.1990 SIO_AV -0.4830 -0.4748
NO2_AD 0.7357 -0.0621 TMP_AV 0.4666 0.4820
CHL_SW -0.7339 -0.2386 SAL_NE -0.3112 0.4561
NO2_NE 0.7339 -0.0666 SIO_SW -0.1278 -0.5466
NO2_AV 0.7330 -0.0688 SIO_AD -0.1193 -0.5466
TMP_NE -0.7293 0.0777 OXY_SW 0.0488 0.5438
CHL_AV -0.7203 0.0975 SIO_NE 0.0136 0.5407

Subtidal communities around Socotra 95
In Table 2 the parameters PO
4
_SW to CHL_NE show that most variables have markedly
higher (absolute) correlation values with the first DCA axis as opposed to the second axis.
Certain parameters, however, correlate best with the second axis: SiO
4
_SW (-0.547),
SiO
4
_AD (-0.547), OXY_SW (0.544), SiO
4
_NE (-0.541). Most of the averages of both
monsoon parameters (parameters with the “_AV” suffix) correlate well with both axes. The
communities of SNC are separated from SSC along the first axis, which might result from
the lower phosphate concentrations, the higher salinity and the higher temperatures of the
former cluster during the SW monsoon. On the other hand, the PO
4
concentrations during the
NE monsoon are higher at SNC than SSC. The difference between these clusters can also be
explained by the lower PO
4
, lower TMP and higher OXY fluctuations (“_AD” suffix) at
SNC in comparison to SSC and OI. The separation along the second axis, e.g. TZ from SSC
and SNC, might be caused by rather low SiO
4
and high OXY concentrations (intense current
patterns) at TZ during the SW monsoon, and high SiO
4
concentrations at TZ during the NE
monsoon. The fluctuations in SiO
4
concentrations are higher at SSC compared to TZ.
Fig. 4. First two ordination axes of a DCA
based on cover data (van der Maarel scale)
of the subtidal plants (black dots) in the
different quadrats (grey circles), rare species
are downweighted.
Fig. 5. First two ordination axes of a DCA
based on presence/absence data. Cluster
abbreviations as in Fig. 1. Black dots
represent plant species, grey circles
represent quadrats.
The DCA based on the van der Maarel data (Fig. 4), resulted in similar clusters but has
less resolution as the quadrats of TZ are partly grouped in SSC and SNC, respectively. The
first two axes of this ordination have high eigenvalues (0.743 and 0.689) and together they
represent 15.7 % of the variation in species composition. The DCA of the nominal data

96 Chapter 6
(presence/absence) also shows a similar cluster pattern (Fig. 5), but the distinction between
SNC, TZ, SSC and OI is less clear (intermingled quadrats) and the latter grouping of clusters
constitutes a more homogeneous group in relation to CDC and SGB. The first two axes of
the latter DCA have high eigenvalues (0.707 and 0.589) and together they represent 12.4 %
of the variation in species composition.
Figs 6-8. Box plots of the variables
(species richness, biomass and alpha
diversity) showing the median, quartiles,
and extreme values for each of the DCA
clusters. Cluster abbreviations as in Fig.
1. Counts for categories: SGB (6), CDC
(12), SNC (24), TZ (10), SSC (17), OI
(13). ANOVA, Tukey HSD: NS, not
significant; *, p < 0.05; **, p < 0.01; ***,
p < 0.001.
Fig. 6. Species richness of the
quadrats (untransformed) from the
different DCA clusters. Inset:
ANOVA, Tukey HSD, of square root
-1
transformed data.
Fig. 7. Total biomass (fresh weight) of
the quadrats (untransformed) from the
different DCA clusters. Inset:
ANOVA, Tukey HSD, of natural log
transformed data.
Fig. 8. Fisher’s alpha of the quadrats
(untransformed) from the different
DCA clusters. Inset: ANOVA, Tukey
HSD, of natural log transformed data.

Subtidal communities around Socotra 97
Species richness and biomass
The ANOVA of the transformed species richness per quadrat shows 2 groups of DCA
clusters (Fig. 6). SGB and CDC are characterized by a low floristic species richness. The
second group incorporates the remaining clusters. The range of the species richness per
quadrat within this group varies highly, but the species richness of these clusters does not
differ significantly. The highest number of species (31) per quadrat are reported for TZ.
The analysis of variance of the biomass data shows one group of clusters (SNC, TZ, SSC)
with comparable biomasses (Fig. 7). Again, the interquartile range of TZ covers the widest
range, encompassing those of SNC and SSC. The quadrats of the latter clusters have
intermediate biomasses between those of SGB, expressing the highest biomass per quadrat,
and those of CDC, characterized by a low biomass. OI differs significantly from the first
group of clusters, but the quadrats of OI are also characterized by biomass values
intermediate between, and differing substantially from, those of SGB and CDC.
Alpha and beta diversity
The log-series variable alpha, composite index of species richness and abundance, shows the
highest species diversity per quadrat for the most species rich clusters with moderate
biomass (high evenness), i.e. TZ and SSC (Fig. 8). A second group, consisting of CDC and
OI, shows a significantly lower alpha diversity than the TZ-SSC-group. SNC has an
intermediate alpha diversity between both groups, as it does not differ significantly from any
of the four clusters. SGB is characterized by the lowest alpha diversity values.
The Jaccard coefficient, as a qualitative measurement for ß-diversity (Table 3), shows that
SSC and TZ are the most similar DCA clusters (lowest degree of species turn-over). Both are
somewhat less similar to the communities of SNC and OI. The quantitative similarity ratio is
less resolving (Table 4). In addition to the high similarity in absolute species composition,
the species occurring at TZ have a comparable biomass to those in SSC and SNC. The latter,
however, show a low quantitative similarity to each other, illustrating the intermediate nature
of TZ.
Table 3. The Jaccard coefficient (%) as a qualitative measurement for ß-diversity among the DCA
clusters. Similarities higher than 10 are marked in bold.
SGB CDC SNC TZ SSC
CDC 0.00
SNC 3.57 3.45
TZ 1.82 1.75
24.71
SSC 1.16 2.30
28.04 40.63
OI 0.00
10.26 13.75 21.92 26.32

98 Chapter 6
Table 4. The similarity ratio as a quantative measurement for ß-diversity among the DCA clusters. The
high similarity values of TZ with SSC and SNC, respectively, are marked in bold.
SGB CDC SNC TZ SSC
CDC 0.00
SNC 0.04 3.97
TZ 0.01 0.01
64.81
SSC 0.00 0.00 1.62
80.76
OI 0.00 0.00 0.45 0.02 3.13
Biogeography
The graphs of the biogeographic affinity of the DCA clusters within the Indian Ocean show
three general trends (Figs 7, 8), corresponding with the following coastal areas: (i) South
Africa – Kenya (East African Coast); (ii) Kenya – Iran (Arabian Sea); and (iii) Iran -
Western Australia (eastern Indian Ocean). CDC showed an additional trend for the eastern
Indian Ocean, an increase in affinity for the region Pakistan – Sri Lanka and a plateau for Sri
Lanka - Western Australia. For each of these coastal blocks the regression lines were
calculated in order to compare the general trends of the different clusters (Schils et al. 2001).
SGB and CDC are composed of common Indian Ocean taxa, visualized by an increasing
affinity for the East African flora from South Africa to a peak in Kenya. Thereafter, the
affinity decreases for the Arabian Sea, the result of a few unrecorded common Indian Ocean
taxa for this area. These species [e.g. Dictyosphaeria cavernosa (Forsskål) Børgesen] are
probably ubiquitous throughout the Arabian Sea as they already have been reported for the
Arabian Gulf (De Clerck & Coppejans 1996). Similar patterns were obtained for SNC, TZ
and SSC, however, with a decreasing overall affinity in this order (Fig. 9). OI behaved like a
combination of the other clusters: having a relatively high affinity with the East African
Coast (common Indian Ocean taxa) similar to SNC, a decreasing affinity with the Arabian
Sea flora (an artefact of undersampling in the Arabian Sea) like CDC and a relatively low
affinity with the Eastern Indian Ocean comparable to SSC (Fig. 10).
D
ISCUSSION
The Cheney ratio, the sum of the Rhodophyceae and Chlorophyceae divided by the number
of Phaeophyceae, has been used to correlate macroalgal floras with seawater temperature
(Cheney 1977, Bolton 1986). The overall ratio for the archipelago is 3.8, which is indicative
for a warm temperate flora (Kapraun 1980). The Cheney ratios of the major quadrat clusters
(SNC, TZ, SSC and OI) are comparable, due to similar proportions of Chloro-, Phaeo- and
Rhodophyceae in these communities (Fig. 11).
The clusters obtained from the DCA can be grouped geographically, which is shown by
the high correlation of the GIS coordinates to the first two DCA axes. The 6 clusters include
distinct entities (SGB, CDC, SNC and SSC) and intermediate ones (TZ, OI). The
characteristics of each of the subtidal plant communities are discussed below.

Subtidal communities around Socotra 99
Figs 9, 10.
Regression lines of the
biogeographic affinities (y axis: Simpson
Coefficient in %) between the DCA clusters
of Socotra and check lists of Indian Ocean
nations. The countries (x axis) are presented
from the southwestern Indian Ocean, over
the Arabian Sea, to the southeastern Indian
Ocean (indicated by the vertical lines in the
plot): South Africa (SAf), Mozambique
(Moz), Madagascar (Mad), Réunion (Réu),
Mauritius (Mau), Tanzania (Tan), Seychelles
(Sey), Kenya (Ken), Somalia (Som), Yemen
(Yem), Oman (Oma), Iran (Ira), Pakistan
(Pak), Laccadive (Lac), Maldives (Mald), Sri
Lanka (Sri), Bangladesh (Ban), Andaman
(And), Malaysia (Mala), Indonesia (Ind),
Australia (Aus).
Fig. 9. Biogeographic affinity of SNC
(filled squares), TZ (open circles) and
SSC (filled triangles).
Fig. 10. Biogeographic affinity of CDC
(asterisks), SNC (filled squares) and SSC
(filled triangles) in relation to that of OI
(thick grey line). Similarities between the
former clusters and OI, for a specific
region (East Africa, Arabian Sea, western
Indian Ocean), are indicated with a
thickened line.
Fig. 11. Percentage of Rhodophyta
(dotted), Phaeophyta (hatched),
Chlorophyta (vertically striped) and
seagrasses (grey shaded) in the DCA
cluster. Cluster abbreviations as in Fig. 1.
Seagrass beds (SGB) and coral dominated communities (CDC)
SGB and CDC are characterized by a low floristic richness. Both clusters, however, can be
regarded as sub-entities of Socotra’s north coast as they occur in specialized habitats within
SNC. The communities of these two biotopes differ substantially in species composition,
biomass and species richness from the other DCA clusters and were excluded from the
second DCA, in which the environmental variables were tested. Extensive seagrass beds are

100 Chapter 6
rather rare around the archipelago: patches of Halodule uninervis (Forsskål) Ascherson are
scattered around the north coast (sandy substrate), well-developed Thalassodendron ciliatum
(Forsskål) den Hartog beds occur in Mahfirhin Bay (Fig. 1: close to site 42; no quadrats
available) and extensive seagrass beds, composed of Halodule uninervis, Halophila ovalis
(R. Brown) Hooker and Thalassia hemprichii (Ehrenberg) Ascherson are found in
Qalansiyah lagoon (Fig. 1: site 29). Owing to the exclusion of small epiphytes in this study,
SGB is species-poor but shows the greatest standing stock of all community types. With
respect to other seagrass communities, generally consisting of one or two seagrass species
(Duarte 2000), Qalansiyah lagoon, however, contains plant communities with a moderate
seagrass richness (three species).
CDC is typified by a predominant coral cover (> 90%), complemented with some common
Indian Ocean algae characteristic for this habitat [e.g. Chlorodesmis fastigiata (C. Agardh)
Ducker and Dictyota friabilis Setchell]. Coral reef development is restricted to small patches
around the archipelago. As a rule, coral reef formation is rare within the Arabian Sea and the
phenomenon of large monotypic reefs (e.g. the Montipora reefs at Masirah Island, Oman)
shows that the environmental conditions are generally too harsh and unfavourable for many
corals species (Coles 1995, Paulay 1999, Wilson 2001). Recent field studies have, however,
demonstrated that the area hosts more coral species and endemics than previously thought
(Paulay & Meyer 2001).
Socotra’s north coast (SNC)
The north coast of Socotra is typified by a mixture of well-developed coral assemblages (e.g.
CDC at Hawlaf; Fig. 1: site 5) and algal communities (e.g. Diham; Fig. 1: site 4). The marine
macroflora of this area consists mainly of common East African/Indian Ocean taxa (Fig. 9),
reflected in the high general affinity with the Indian Ocean flora. The environmental
correlations show that this cluster is characterized by the highest water temperatures and
salinities of the archipelago during the SW monsoon. SNC has the highest values of the low
phosphate concentrations during the NE monsoon. During the SW monsoon, the phosphate
concentrations are higher with the lowest values for SNC. Consequently, this entity is
characterized by the smallest changes in phosphate concentrations and temperature, the
lowest average chlorophyll a concentrations, and the highest average oxygen concentrations.
A total of 43 species were collected in the subtidal quadrats of this area. The species richness
per quadrat does not differ from SSC, TZ and OI, and the alpha diversity is intermediate of
all communities around the archipelago. The biomass of the quadrats equals those of TZ and
SSC. The communities of SNC have a high similarity in structural composition (quantitative
ß-diversity) with TZ (64.81), and show a high qualitative similarity with SSC (28.04) and TZ
(24.71). SNC and SSC thus share a relatively high number of species, partly due to the high
number of recorded species for SSC, but these occur throughout both clusters in low
abundances.
Socotra’s south coast (SSC)
During the SW monsoon, the Great Whirl, extending northwards along the Somali Coast,
spins off towards Socotra’s south coast (http://www.nioz.nl/en/facilities/dmg/niop/themes/
theme-c/thmchydr). This cold and nutrient rich surface water (~ 22°C) shapes the southern
coast of Socotra. The impact of upwelling hampers coral development (e.g. bioerosion;

Subtidal communities around Socotra 101
Paulay 1999) and promotes macroalgal growth in an ongoing competition with the coral
communities due to the favouring environmental parameters during the SW monsoon (e.g.
high phosphate concentrations and low temperature). Consequently, the SSC vegetation is
relatively high in biomass and rich in species, resulting in high alpha diversity values. In
addition, SSC contains the largest number of species per cluster (64). The flora comprises a
large number of red algal species that generally contribute little to the total biomass in
understory layers (e.g. Zellera tawallina G. Martens), and more to the primary layer [e.g.
large plants of Botryocladia leptopoda (J. Agardh) Kylin]. In addition, a remarkable number
of gelatinous red algae (Schils & Coppejans 2002) has been reported for this area. Despite
the relatively high number of species recorded for the quadrats, the biogeographic affinity
within the Indian Ocean is low. This is the result of a number of disjunctly distributed and
endemic species (Schils et al. 2002; Schils & Huisman 2003), reflecting biogeographic
affinities with distant areas (Australia, Hawaii, Japan and South Africa). Børgesen (1934)
and Wynne (2000) noted similar distribution patterns for certain species within the Pakistani
and Omani flora, respectively. The disjunct distribution pattern of these algae could result
from: (i) the upwelling phenomenon and the resulting peculiar environmental conditions; (ii)
refugia where algae could persist subtidally over a long time (e.g. Reticulocaulis; Schils et
al. 2002; Millar and Kraft 1984); or (iii) the lack of subtidal studies in the Indian Ocean.
Similar disjunct distribution patterns have also been reported for coral species from the
Arabian Sea (Coles 1995).
Transition zone (TZ)
The algal communities at the eastern extremity of Socotra Island are characterized by high
biomass stands, being rich in species (species richness of the quadrats). This results in the
highest alpha diversity values of all surveyed sites around the archipelago. The total amount
of recorded species in this cluster (39) is somewhat lower than those of SSC and SNC, most
probably a result of the low number of quadrats (10) included in TZ. The communities are
composed of a mixture of primarily south coast species (highest qualitative and quantative
similarities) and north coast species. The macroalgal stand (biomass) is similar to those of
SNC and SSC. We can conclude that the transition zone, hence its name, is a gradual
overlapping zone between the communities of Socotra’s north and south coast. This cluster
is, however, also characterized by certain algae (e.g. Gibsmithia larkumii Kraft and
Sympodothamnion sp.; Schils & Coppejans 2002; pers. obs.), displaying a disjunct
distribution pattern within the Indo-Pacific. This is reflected in the biogeographic graph (Fig.
9), in which TZ, compared to SNC, shows a decline in the general affinity with Indian Ocean
taxa. The floristic peculiarity of this cluster is most probably related to the prevailing
environmental conditions. The eastern tip of Socotra Island is subject to upwelling and in
addition there seems to be a pronounced effect of the Socotra Eddy evolving east from the
island, contiguous with the other anticyclonic circulation the “Great Whirl”
(http://www.ssc.erc.msstate.edu/Altimetry/north_indian_ocean.html). Complex and intense
current patterns were noted in this area, and local fisherman cannot access this area during
the greater part of the SW monsoon (pers. obs.). Presumably, these intense currents favour
the luxuriant and particular red algal flora due to the constant flow of nutrients and the
temperature regulation of these subtidal habitats (corresponding to its position along the first
DCA axis, in between SSC and SNC). Unfortunately, data of current patterns and velocities
were not available for inclusion in the analysis.

102 Chapter 6
Outer islands (OI)
The outer islands of this study include Abd al-Kuri and Samha Island. There were no quadrat
data from Darsa Island available, but based on its geographic position the communities are
likely to be similar to those of OI. Certain quadrats of the north coast of Abd al-Kuri (ANC)
group with SNC in the first DCA, but less pronounced so in the second (arrows in Fig. 3).
This supports the hypothesis for a drive towards the development of macroalgal communities
comparable to those of the main island (SNC and SSC), but this climax stage is not reached
due to the drastically changing chemical characteristics and water dynamics around a small
coastal area (area effect). Support for these speculations can be found in the second DCA,
where OI is positioned close to the origin of the first axis, which is highly negatively
correlated with the fluxes in phosphate concentrations and temperature. This is backed by the
statement of van Bennekom J., de Bruin T., Nieuwenhuis J. (http://www.nioz.nl/en/facilities/
dmg/niop/themes/theme-c/thmchydr) that the region between Socotra and Ras Fartak shows
alternating patches of relatively warm and cold surface water. Likewise, van Ooijen J.C., van
Weerlee E (http://www.nioz.nl/en/facilities/dmg/niop/themes/theme-c/thmchydr) note that
between Cap Guardafui and Socotra the entire water column is seasonally renewed to a
depth of 1100 m. The importance of the high environmental dynamics at OI has major
ecological implications: Turner (http://www.cordio.org/Repstatus10) observed that the
islands Samha and Darsa were barely affected by the coral bleaching that hit main Socotra
severely in 1998. The mixed species composition is also reflected in the biogeographic trend,
being composed of different biogeographic affinities characteristic for the other
communities. Accordingly, OI is characterized by the high abundances and diversity in
coastal fish, soft corals and scleractinian corals, counting for a large proportion of the
archipelago’s total diversity (DeVantier 2000, Reinicke et al. 2000, Zajonz et al. 2000).
C
ONCLUSIONS
The DCA of the van der Maarel data, a less time consuming method, reveals similar results
to the biomass DCA. Using this methodology, it is still needed to clear the quadrats in order
to note the smaller and uncommon species that prove to be important in the analyses [e.g.
Chauviniella coriifolia (Harvey) Papenfuss and Claudea elegans Lamouroux]. The
presence/absence data, on the other hand, obscure the patterns in community structure and
more elaborate data sets (checklists of larger areas, more samples, more zonation belts) are
required to discriminate among the community types.
The relationship of the SiO
4
concentration and the second DCA axis seems to be odd, as
this indicator for upwelling does not differentiate between SNC and SSC. There are several
possibilities to explain this anomaly: (i) upwelling is a coastal phenomenon but the included
environmental data are averages of a broader area and the cycle in which the parameter
varies from highs to lows might happen considerably more frequent than the two periods for
which the data were averaged, so the resolution of the data set might be too low; (ii) the SiO
4
concentrations vary likewise in the different coastal waters and correspond to a lesser extent
with the vegetation differences around the archipelago; (iii) a synergy of environmental
variables might be important in shaping the macroalgal assemblages, obscuring the
importance of SiO
4
as an indicator for upwelling. Altogether, the oceanic data around the
archipelago correspond well to the seasonal changes in environmental parameters reported
for the southern Arabian shores and the resulting influence on its biotic communities (e.g.

Subtidal communities around Socotra 103
Ormond & Banaimoon 1994). Besides these abiotic factors, biotic interactions or complex
cascade effects are suspected to be important in shaping the subtidal communities, especially
so for the species-rich outer islands with a limited coastal area.
Although the Socotra archipelago harbours a diversity of well-characterized subtidal
communities, showing high affinities with a common Indian Ocean flora, its similarity with
other communities within the upwelling-influenced Arabian Sea remains unclear as
ecological macroalgal studies in this area are lacking. Another question that remains is the
quantification of the relationship between the upwelling flora (disjunct species of SSC, TZ
and OI) with distant regions as Australia, Hawaii, Japan and South Africa.
A
CKNOWLEDGEMENTS
Thanks are expressed to the Senckenberg Research Institute (M. Apel and F. Krupp) for the
excellent field trip preparations to the Socotra Archipelago. We are grateful to Frederik
Leliaert and Olivier De Clerck for their help in identifying Cladophorales and Dictyota
specimens, respectively. Henry Engledow is gratefully acknowledged for his constructive
comments on the manuscript. Tom Schils is indebted to the Fund for Scientific Research
Flanders (FWO, Belgium) for his research assistant grant. The four anonymous referees are
thanked for their constructive criticism.
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Arabian Sea and the Indian Ocean and a new report of Melanothamnus somalensis
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662 pp.

106 Chapter 6
APPENDICES
Appendix 1. Coordinates of the 21 sample sites around the Socotra Archipelago.
site 4: 12.630°N, 53.869°E
site 5: 12.681°N, 54.077°E
site 6: 12.693°N, 54.085°E
site 8: 12.664°N, 54.045°E
site 9: 12.204°N, 52.259°E
site 10: 12.204°N, 52.273°E
site 11: 12.226°N, 52.073°E
site 13: 12.173°N, 52.226°E
site 20: 12.157°N, 52.985°E
site 22: 12.315°N, 53.623°E
site 23: 12.355°N, 53.544°E
site 25: 12.528°N, 54.540°E
site 29: 12.701°N, 53.500°E
site 31: 12.700°N, 53.654°E
site 36: 12.321°N, 53.919°E
site 39: 12.639°N, 53.944°E
site 40: 12.303°N, 53.843°E
site 41: 12.322°N, 54.034°E
site 42: 12.403°N, 54.243°E
site 43: 12.535°N, 54.513°E
site 44: 12.532°N, 54.520°E
Appendix 2. Species recorded in the quadrats, with mention of their cluster occurrence. Cluster
abbreviations as in Fig. 1.
RHODOPHYCEAE - FLORIDEOPHYCIDAE
BONNEMAISONIALES
BONNEMAISONIACEAE
Asparagopsis taxiformis (Delile) Trevisan - SSC
CERAMIALES
CERAMIACEAE
Balliella repens Huisman & Kraft - TZ - SSC
Centroceras clavulatum (C. Agardh) Montagne - SNC
Euptilota fergusonii Cotton - SSC
Haloplegma duperreyi Montagne - SSC
DASYACEAE
Dictyurus purpurascens Bory de Saint-Vincent - SSC
DELESSERIACEAE
Chauviniella coriifolia (Harvey) Papenfuss - SSC
Claudea elegans Lamouroux - SSC
Duckerella ferlusii (Hariot) Wynne - SSC
Martensia elegans Hering - SSC
RHODOMELACEAE
Acanthophora dendroides Harvey - SNC - TZ - SSC
Acanthophora spicifera (Vahl) Børgesen - SNC
Amansia rhodantha (Harvey) J. Agardh - OI
Chondria armata (Kützing) Okamura - TZ - SSC
Chondrophycus papillosus (C. Agardh) Garbary &
Harper - SNC
Chondrophycus parvipapillatus (C.K.Tseng) Garbary &
Harper - TZ
Herposiphonia nuda Hollenberg - SNC - SSC
Laurencia majuscula (Harvey) Lucas - SNC - SSC
Laurencia pedicularioides Børgesen - TZ - SSC - OI
Leveillea jungermannioides (Hering & G. Martens)
Harvey - OI
Osmundaria melvillii (J. Agardh) R. Norris - TZ - SSC
CORALLINALES
CORALLINACEAE
Amphiroa anceps (Lamarck) Decaisne - TZ - SSC
Amphiroa fragilissima (Linnaeus) Lamouroux - SNC
Amphiroa rigida Lamouroux - SNC - TZ - SSC - OI
GELIDIALES
GELIDIACEAE
Pterocladiella caerulescens (Kützing) Santelices &
Hommersand - SNC - SSC – OI
Pterocladia cf. caloglossoides (Howe) Dawson - SNC
GELIDIELLACEAE
Gelidiella pannosa (Feldmann) Feldmann & Hamel -
CDC – SNC
GIGARTINALES
HYPNEACEAE
Hypnea charoides Lamouroux / valentiae (Turner)
Montagne complex - SGB - SNC - TZ
Hypnea musciformis (Wulfen) Lamouroux - SNC - TZ
Hypnea pannosa J. Agardh - TZ - OI
Hypnea spinella (C. Agardh) Kützing - SNC - TZ - SSC
RHIZOPHYLLIDACEAE
Portieria hornemannii (Lyngbye) P. Silva - SNC - SSC
- OI
SARCODIACEAE
Sarcodia montagneana (J. Hooker & Harvey) J. Agardh
- SSC
SCHIZYMENIACEAE
Titanophora pikeana (Dickie) J. Feldmann - SSC

Subtidal communities around Socotra 107
SOLIERIACEAE
Sarconema filiforme (Sonder) Kylin - SNC
Solieria robusta (Greville) Kylin - TZ - SSC
GRACILARIALES
GRACILARIACEAE
Gracilaria debilis (Forsskål) Børgesen - SNC
Gracilaria millardetii (Montagne) J. Agardh - SNC -
SSC - OI
HALYMENIALES
HALYMENIACEAE
Carpopeltis maillardii (Montagne & Millardet) Chiang
- SSC - OI
NEMALIALES
GALAXAURACEAE
Galaxaura marginata (Ellis & Solander) Lamouroux -
SSC - OI
Scinaia moniliformis J. Agardh - TZ - SSC
Scinaia tsinglanensis Tseng - SNC
Tricleocarpa fragilis (Linnaeus) Huisman & Townsend
- SSC
RHODYMENIALES
CHAMPIACEAE
Champia compressa Harvey - TZ - SSC - OI
Champia indica Børgesen - TZ
Champia parvula (C. Agardh) Harvey - SNC
LOMENTARIACEAE
Gelidiopsis variabilis J. Agardh (Schmitz) - SNC - TZ -
SSC
RHODYMENIACEAE
Botryocladia leptopoda (J. Agardh) Kylin - TZ - SSC -
OI
Botryocladia skottsbergii (Børgesen) Levring - TZ -
SSC - OI
PHAEOPHYCEAE
DICTYOTALES
DICTYOTACEAE
Dictyopteris delicatula Lamouroux - TZ - SSC - OI
Dictyopteris macrocarpa (Areschoug) O. Schmidt -
SSC - OI
Dictyopteris polypodioides (De Candolle) Lamouroux -
SNC - SSC
Dictyota bartayresiana Lamouroux - SNC
Dictyota cervicornis Kützing - SNC - TZ - SSC - OI
Dictyota ceylanica Kützing - SSC
Dictyota crispata Lamouroux - TZ - SSC
Dictyota friabilis Setchell - CDC - OI
Dictyota grossedentata De Clerck & Coppejans - TZ -
SSC
Dictyota stolonifera Dawson - OI
Lobophora variegata (Lamouroux) Womersley ex
Oliveira - SNC - TZ - SSC - OI
Padina australis Hauck - SNC - TZ
Padina boergesenii Allender & Kraft - SNC - SSC
Padina elegans Koh ex Womersley - SSC
Spatoglossum asperum J. Agardh - SNC - TZ - SSC
Stoechospermum polypodioides (Lamouroux) J. Agardh
- SNC
FUCALES
SARGASSACEAE
Nizamuddinia zanardinii (Schiffner) P. Silva - SNC
Sargassum angustifolium C. Agardh - SNC - SSC
Sargassum decurrens (R. Brown ex Turner) C. Agardh
- OI
Sargassum latifolium (Turner) C. Agardh - TZ - SSC
Sargassum cf. linearifolium (Turner) C. Agardh - SNC -
OI
Turbinaria ornata (Turner) J. Agardh - OI
SCYTOSIPHONALES
SCYTOSIPHONACEAE
Colpomenia sinuosa (Mertens ex Roth) Derbès & Solier
- SNC - TZ
Rosenvingea intricata (J. Agardh) Børgesen - SSC
CHLOROPHYCEAE
BRYOPSIDALES
CAULERPACEAE
Caulerpa brachypus Harvey - TZ - OI
Caulerpa lanuginosa J. Agardh - SNC - TZ - SSC
Caulerpa mexicana Sonder ex Kützing - SNC - TZ -
SSC
Caulerpa peltata Lamouroux - OI
Caulerpa racemosa (Forsskål) J. Agardh - TZ - SSC
Caulerpa scalpelliformis (R. Brown ex Turner) C.
Agardh - SSC
CODIACEAE
Codium dwarkense Børgesen - SNC - SSC - OI
UDOTEACEAE
Avrainvillea lacerata Harvey ex J. Agardh - SSC

108 Chapter 6
Chlorodesmis fastigiata (C. Agardh) Ducker - CDC -
OI
Halimeda copiosa Goreau & Graham / minima (W.R.
Taylor) Colinvaux - TZ - SSC - OI
Halimeda cuneata Hering - SNC - SSC
Halimeda discoidea Decaisne - SNC - SSC
Halimeda tuna (Ellis & Solander) Lamouroux - SNC -
TZ - SSC
Udotea indica A. Gepp & E. Gepp - SNC - TZ - SSC
CLADOPHORALES
CLADOPHORACEAE
Cladophora coelothrix Kützing - TZ - SSC
Cladophora prolifera (Roth) Kützing - SNC
Cladophora vagabunda (Linnaeus) van den Hoek -
SNC - SSC
SIPHONOCLADACEAE
Boergesenia forbesii (Harvey) J. Feldmann - SSC - OI
Chamaedoris auriculata Børgesen - TZ - SSC
Dictyosphaeria cavernosa (Forsskål) Børgesen - CDC
Siphonocladus tropicus (P. Crouan & H. Crouan) J.
Agardh - TZ
Struveopsis siamensis (Egerod) P. Silva - SSC
Ventricaria ventricosa (J. Agardh) Olsen & J. West - OI
DASYCLADALES
DASYCLADACEAE
Neomeris van-bosseae Howe - TZ - SSC
MAGNOLIOPHYTA - LILIOPSIDA
ALISMATALES
CYMODOCEACEAE
Halodule uninervis (Forsskål) Ascherson - SGB - SNC
HYDROCHARITACEAE
Halophila ovalis (R. Brown) Hooker - SGB
Thalassia hemprichii (Ehrenberg) Ascherson - SGB

Phytogeography in the Arabian Sea 109
CHAPTER 7
Phytogeography of upwelling areas in the Arabian Sea
Submitted as: Schils T. & Coppejans E. Phytogeography of upwelling areas in the Arabian Sea.
ABSTRACT
Aim Comparing the marine plant communities of two islands, with a similar diversity in
biotopes, in two different upwelling areas of the Arabian Sea.
Location Arabian Sea: (1) the Socotra Archipelago (Yemen; 12.47°N, 53.87°E) in the
Somali upwelling area, (2) Masirah Island (Oman; 20.42°N, 58.79°E) in the upwelling area
of the southern Arabian Peninsula.
Methods The marine flora of different biotopes around both islands were examined by
means of qualitative assessments. Ordination analysis (DCA) was used to identify the
different plant communities and to correlate these with environmental parameters. The
species composition of the identified communities were compared (tripartite similarity
index) and their biogeographic affinity with nations bordering the Indian Ocean was
determined. Indicator species analyses were performed to identify the characteristic species
of the different plant communities and their biotopes.
Results The DCA analysis shows a clustering of sites (plant communities) corresponding
with their geographic position, linked in turn to the prevailing environmental conditions of
the different coastal areas. The combined interpretation of the ordination, similarity and
biogeographic analyses results in the aggregation of similar plant communities of both
upwelling areas into four biotopes.
Main Conclusions The north coast communities of Socotra and the west coast communities
of Masirah can be grouped into 3 biotopes related to the degree of exposure and
sedimentation. These biotopes are typified by indicator species, characteristic for specific
substrata, and have a high biogeographic affinity with the East African coast. The plant
communities of Socotra’s south coast and Masirah’s east coast constitute a fourth biotope,
being diverse and species rich, typified by a large proportion of red macroalgae including the
characteristic species of the unique Arabian Sea flora. This biotope has a pronounced
biogeographic affinity with distant regions (disjunctly distributed taxa). Within the different
biotopes, the communities of Masirah are more divergent from an East African flora in
comparison to Socotra, the latter being a stepping stone between the East African and
Arabian Sea flora.

110 Chapter 7
INTRODUCTION
The Arabian Sea is regarded as a biogeographic sub-region of the Indian Ocean (Sheppard et
al. 1992). Seasonal upwelling, maximal in strength during the southwest monsoon (summer),
influences the greater part of the Arabian Sea coasts and is considered as the main regulating
phenomenon for a biogeographic barrier in the area (Wilson 2000).
Case studies on the macroalgae of confined areas within the Arabian Sea (Wynne &
Banaimoon 1990; Ormond & Banaimoon 1994; Wynne & Jupp 1998; Schils 1999; Wynne
1999a, b, 2000, 2001; Leliaert 2000; Wynne & Leliaert 2001; Schils 2002; Schils &
Coppejans 2002; Schils et al. 2003a, b) indicate that the region harbours a species rich and
diverse marine flora. The upwelling area along the Hadramout (Yemen) and Dhofar (Oman)
coasts on the southern Arabian Peninsula is a centre of high endemism within the Arabian
Sea (Sheppard & Salm 1988; Randall & Hoover 1995). Within this area, Masirah Island has
been comparatively well investigated as the island harbours a wide diversity of biotopes
(from upwelling affected shores to large monotypic reefs) within a limited geographic area
(de Vaugelas 2001). The Socotra Archipelago, located within the Somali upwelling area, is
likewise identified as the “Galapagos of the Indian Ocean” (Wilson & Klaus 2000) due to its
diversity in biota and biotopes. The archipelago recently received scientific interest owing to
the comparatively pristine state of its natural environment. The marine ecosystems of
Socotra also vary from coral dominated communities to upwelling influenced shores, with
clearly defined subtidal plant communities (T. Schils & E. Coppejans submitted). The
Socotra Archipelago is located at the boundary of many species distributions (sympatry of
sister taxa; Kemp 1998b) and it serves as a stepping stone for genetic exchange, by means of
larval and spore dispersal, between the Indian Ocean, the Red Sea (Gulf of Aden) and the
Arabian Sea. Besides being located on the crossroads of these biogeographic regions, the
Arabian Sea flora shows pronounced biogeographic affinities with distant marine floras
(Børgesen 1934; Wynne 2000; Schils & Coppejans 2002; Schils et al. 2003a). Despite these
anecdotic observations, no quantitative research has been performed in order to characterize
the different plant communities of the Arabian Sea and to determine their similarity,
diversity and biogeography. This study attempts to provide insight into the diversity and
unicity of the region by comparing detailed species inventories of different sampling sites
within the Somali and southern Arabian upwelling areas. Biomass analyses of vegetation
quadrats around the Socotra Archipelago (T. Schils & E. Coppejans submitted) showed that
a qualitative comparison (presence/absence of taxon data) returns reliable results if the sites
are intensively sampled in a relatively wide vertical (different zones) and horizontal range
(large sample area).
M
ATERIAL AND METHODS
The field trips to Masirah Island and the Socotra Archipelago were conducted by the first
author in the period between two successive SW monsoons, from 2 to 30 November 1999
and from 26 March to 7 May 2000, respectively. During the qualitative surveys, samples
were collected from intertidal and subtidal habitats to 20 m depth. Plants were gathered in
fine-meshed plastic bags and sorted in a field laboratory. Small and crustose algae were
excluded from the dataset as they can easily be overlooked from one survey to another and a
meticulous investigation of the whole substratum and epiphytes is very time-consuming.
Reference specimens were selected and pressed as herbarium specimens, preserved in a 5%

Phytogeography in the Arabian Sea 111
formaldehyde-seawater solution or dried in silica gel for molecular purposes. This collection
is housed in GENT (Ghent University Herbarium, Krijgslaan 281 - S8, 9000 Ghent,
Belgium).
Figure 1. Map of the Arabian Sea (a) with Masirah Island (b) and the Socotra Archipelago (c) as insets.
The sample sites are indicated according to their clustering in the DCA plot: east coast of Masirah (MAS
EC, open circles), seagrass beds of Masirah (MAS SG, open boxes), west coast of Masirah (MAS WC,
open triangles), north coast of Socotra and two sheltered sites in Mahfirhin Bay (SOC NC, stars), north
coast of Socotra and outer islands (S&O NC, filled triangles), seagrass beds of Socotra (SOC SG, filled
box) and south coast of Socotra and outer islands (S&O SC, filled circles). The scale bar represents 1000
km (a), 25 km (b) and 50 km (c), respectively.
Ordination
The 48 sample sites
(Fig. 1) of which complete species inventories were recorded (1048
species records) served as the ordination input. Detrended Correspondance Analysis (DCA
performed with CANOCO; ter Braak 1988) was chosen as an indirect gradient analysis as
the data clearly represent a unimodal model (maximum gradient length: 5.227 SD; ter Braak
& Šmilauer 1998).
In an attempt to determine the species-environment correlation, environmental data around
Socotra (latitude: 9.650°N – 14.383°N; longitude: 51.900°E – 57.067°E) and Masirah
(latitude: 18.080°N – 22.500°N; longitude: 57.850°E – 61.950°E) were obtained from the
Worldwide Ocean Optics Database (http://wood.jhuapl.edu, W.O.O.D version 4.0).
Chlorophyll a (CHL), salinity (SAL) and temperature (TEMP) parameters (i) showed a good
sample distribution and (ii) were sampled during the SW monsoon (Julian days 121-304;
abbreviated as “parameter” + “_SW”) and the NE monsoon (Julian days 305-120;
“parameter” + “_NE”) for both islands. The average of these parameters during one of the

112 Chapter 7
monsoons was calculated for 2 geographic areas (water masses) around the islands: (i)
Socotra’s north coast, > 12.550°N; (ii) Socotra’s south coast, < 12.550°N; (iii) Masirah’s
west coast, < 58.637°E; (iv) Masirah’s east coast, > 58.637°E. The south coast of Socotra
and the east coast of Masirah are the main upwelling areas of the islands. Socotra’s north
coast and Masirah’s west coast are on the lee side of the major current patterns and less
influenced by the upwelling phenomenon. Whereas SAL and TEMP are directly related to
upwelling and are influential for algal growth, CHL represents the overall productivity of the
phytoplankton, linked to the changes in dissolved nutrients and hence is indirectly related to
upwelling. Additional parameters were derived from the original data, i.e. the absolute
difference of a parameter between the 2 monsoon periods (abbreviation of the environmental
parameter + “_AD”) and the average of both monsoon periods (parameter + “_AV”). The
complete environmental data set had identical parameter values for all sites of a specific
area.
Indicator analysis
Indicator species analysis was used to examine the characteristic species, showing significant
indicator values (IV), for each of the marine plant communities (DCA clusters) and biotopes
(grouping of similar communities of Socotra and Masirah). The indicator analyses were
conducted with PC-ORD (McCune & Mefford 1999), using 1000 Monte Carlo random
permutations to test the statistical significance of the indicator values.
Species richness and similarity
Subsequent analyses of the plant communities included the calculation of species richness
(specified per Phylum/Class) for each DCA cluster, and the tripartite similarity index
(Tulloss 1997) as a qualitative index of beta diversity.
Biogeography
The biogeographic affinity of the plant communities are analysed by comparing the species
composition of the DCA clusters to species inventories of Indian Ocean nations. The latter
data set is primarily based on Silva et al. (1996) and supplemented with records from
omitted and recent sources: Dickie (1888), Holmes (1903), Nizamuddin & Campbell (1995),
De Clerck & Coppejans (1996; 1999), Critchley et al. (1997), Kemp (1998a), Wynne & Jupp
(1998), cd-rom “Mangroves and seagrasses of the Indian Ocean” (R. Phillips and M.
Spalding; Indian Ocean Guides, Department of Biological Sciences, University of Warwick,
1998), De Clerck (1999), Wynne (1999a, b, 2000, 2001), Coppejans et al. (2000), Huisman
(2000), Wynne & Leliaert (2001), De Clerck et al. (2002). The floristic affinity of a cluster
with a specific country is calculated as the Simpson Coefficient: a (a+ min (b, c))
-1
x 100. In
which a represents the number of shared species between a cluster and a country, b and c
represent the number of species unique to the cluster and the country, respectively. The
species inventories of the clusters are always smaller than those of the countries, so the
equation does not include the floristic richness of a country which reduces the discrepancy of
sampling efforts between the different countries. The countries are arranged from
southeastern Africa, over the Arabian Sea, to Western Australia. India was excluded from

Phytogeography in the Arabian Sea 113
the series as its size and geographic position cover a wide diversity of floras within the
Indian Ocean. In order to visualize the main biogeographic trends of the site clusters, based
on both species and generic inventories, the plots are best represented as polynomial trend
lines of a fourth order.
R
ESULTS
Species account
A total of 236 plant species were recorded for the 48 sites (Appendix 1): 6 seagrasses
(Magnoliophyta), 53 Chlorophyta, 43 Phaeophyta and 134 Rhodophyta. Certain species of
the same genus with a similar ecology could not be discerned in the field, therefore the 236
taxa are lumped into 204 species abbreviations (Appendix 1), which are used in the
subsequent analyses. The number of recorded genera totals 128: 5 seagrasses
(Magnoliophyta), 26 Chlorophyta, 17 Phaeophyta and 80 Rhodophyta.
Ordination
A DCA of the species data of the 48 sites showed 6 site groupings (Fig. 2), corresponding
with coastal areas around both islands. Both axes have high eigenvalues (0.525 and 0.406)
and high lengths of gradient (5.226 and 3.531), indicating a high beta diversity within the
samples. The 6 DCA clusters are identified as (Fig. 2, counter clock-wise starting from the
left): (i) the seagrass beds of Socotra (SOC SG) and Masirah (MAS SG); (ii) a distinct entity
of Socotra’s north coast sites (SOC NC); (iii) the south coast sites of Socotra and the outer
islands (Abd al-Kuri, Samha, Darsa; S&O SC); (iv) the east coast of Masirah (MAS EC); (v)
the west coast sites of Masirah (MAS WC); and (vi) the north coast sites of Socotra and the
outer islands (S&O NC). Fig. 3 shows the proportion of seagrasses, Rhodophyta, Phaeophyta
and Chlorophyta in the total number of species and genera recorded for each cluster. The
DCA plot of the first two axes shows an overlap in sites belonging to S&O NC and MAS
WC; and a partial overlap between S&O SC and MAS EC.
Figure 2. First two ordination axes of a
DCA based on the qualitative site data
(species records, represented as small dots).
The six DCA clusters indicative for the
different plant communities are encircled.
Sample site symbols as in Fig. 1.

114 Chapter 7
Figure 3. Percentage of Rhodophyta
(dotted), Phaeophyta (hatched), Chloro-
phyta (vertical stripes) and seagrasses (grey
shaded) in the total account of genera and
species for each DCA cluster. Cluster
abbreviations as in Fig. 1. (a) Number of
species per cluster. (b) Number of genera
per cluster.
Table 1 lists the correlation coefficients of the environmental parameters with the first two
DCA axes. The salinity parameters SAL_AD, SAL_AV and SAL_NE have high correlation
values with the first DCA axis (the latter two being negatively correlated) and lower ones
with the second axis (all negatively correlated). SAL_SW has very low correlation
coefficients with both axes. The average temperature and the chlorophyll a concentrations
show relatively high correlations with both DCA axes. Since these parameters are positively
correlated with both axes, they represent the difference in environmental variables between
the Socotra clusters and the Masirah clusters, which are plotted in the upper right-hand
corner of the DCA, following the resultant of both axes. High chlorophyll a concentrations
are indicative of upwelling, the effect of this phenomenon thus being stronger at Masirah in
comparison to Socotra. The average chlorophyll a concentration at Masirah (1.55 µg l
-1
) is
almost 4 times as high compared to that of the Socotra clusters (0.40 µg l
-1
). Similarly,
TMP_AV differs between Socotra and Masirah. The average yearly temperature turns out to
be higher around Masirah Island (24.9°C) in comparison to the Socotra Archipelago
(24.5°C) due to the higher winter temperatures of the upwelling sheltered sites (26.1°C vs
24.9°C). The remaining temperature parameters (TMP_NE, TMP_AD, TMP_SW) and
SAL_SW have low correlation coefficients with both axes, pointing out the slight differences
of the seasonal temperature between both islands, the small differences in temperature
changes between both monsoon periods, and the similar salinities for both islands during the
SW monsoon.

Phytogeography in the Arabian Sea 115
Table 1. Correlation coefficients of the environmental parameters in decreasing order (absolute values)
with the first two axes of the DCA, respectively. Abbreviations of parameters as in text.
Parameter Axis 1 Axis 2 Parameter Axis 1 Axis 2
SAL_AD 0.689 -0.239 CHL_SW 0.402 0.428
SAL_AV -0.588 -0.284 CHL_AV 0.397 0.427
SAL_NE -0.470 -0.277 CHL_NE 0.384 0.420
TMP_AV 0.453 0.306 CHL_AD 0.397 0.402
CHL_SW 0.402 0.428 TMP_AV 0.453 0.306
CHL_AD 0.397 0.402 SAL_AV -0.588 -0.284
CHL_AV 0.397 0.427 SAL_NE -0.470 -0.277
CHL_NE 0.384 0.420 SAL_AD 0.689 -0.239
TMP_NE 0.241 0.042 TMP_SW 0.076 0.226
TMP_AD 0.118 -0.072 TMP_AD 0.118 -0.072
TMP_SW 0.076 0.226 TMP_NE 0.241 0.042
SAL_SW 0.066 0.030 SAL_SW 0.066 0.030
Tripartite similarity
The tripartite similarity indices are shown in Table 2, in which the sites are ordered so that
the highest indices adjoin the diagonal. This results in a linear representation of sites that are
most similar to one another. MAS WC and MAS EC have the highest similarity index with
one another (0.51), but the former also has a high similarity index with S&O NC (0.48) and
the latter with S&O SC (0.47). S&O SC has equal similarity indices for MAS EC and SOC
NC. MAS SG has the highest index with SOC NC (0.47). All similarity indices with SOC
SG are very low due to the low species richness of this cluster. SOC SG has its highest
similarity index with MAS SG (0.08).
Table 2. Tripartite similarity indices of DCA cluster couples. Clusters are ordered in a way that their
highest similarities adjoin the diagonal position. Similarities > 0.40 are marked in bold. Cluster
abbreviations as in Fig. 1.
S&O NC MAS WC MAS EC S&O SC SOC NC MAS SG SOC SG
S&O NC -
0.48
0.40 0.34 0.38 0.36 0.03
MAS WC
0.48
-
0.51
0.31 0.28 0.34 0.02
MAS EC 0.40
0.51
-
0.47
0.35 0.17 0.02
S&O SC 0.34 0.31
0.47
-
0.47
0.20 0.02
SOC NC 0.38 0.28 0.35
0.47
- 0.39 0.04
MAS SG 0.36 0.34 0.17 0.20 0.39 - 0.08
SOC SG 0.03 0.02 0.02 0.02 0.04 0.08 -
Biogeography
SOC SG was omitted from the analysis, as this site only contained 5 species. The dominant
factors that determine species occurrence at SOC SG are the harsh and variable ecological
conditions characteristic of lagoons, as opposed to the biogeographic distribution patterns of
species.
The biogeographic trends of the DCA clusters based on the species inventories (Fig. 4a)
shows a decreasing affinity with the Indian Ocean from the seagrass beds to the upwelling

116 Chapter 7
zones: MAS SG (47.8%) > S&O NC (46.5%) > MAS WC (42.6%) > SOC NC (40.2%) >
S&O SC (33.6%), MAS EC (33.5%). In general, the biogeographic affinities increase from
South Africa to Kenya, decrease from Somalia to Malaysia and increase again towards
Indonesia and Western Australia.
In addition to the biogeographic comparison based on species lists, affinities at a generic
level were also calculated (Fig. 4b) as certain Indian Ocean taxa have been identified by a
plethora of names (to some extent corrected for in the analyses) dependent on the author or
the phycological school. The identifications at genus level, however, are more rigid. The
generic affinities of the clusters with the Indian Ocean nations are markedly higher than
those based on the species lists. The decreasing order of general affinity with the Indian
Ocean are similar to the results of the species analysis: highest affinity for MAS SG (77.4%);
high affinities for SOC NC (74.7%), S&O NC (73.3%) and MAS WC (71.4%); and lower
affinities for MAS EC (58.3%) and S&O SC (57.4%).
All clusters have high affinities with both ends of the graphs (Figs 4a, b), corresponding
with South Africa and Western Australia, respectively. Parts of these nations are subjected to
temperate waters and other parts to (sub)tropical waters, resulting in high affinities with all
plant communities of the Arabian Sea defined here. The overall biogeographic affinities are
highest with the East African coast and surprisingly lower with the Arabian Sea. The
affinities of the SOC (S&O) and MAS communities with Yemen and Oman respectively, are
by definition 100%. This result is, however, not obtained from the analysis because the
species lists of the Indian Ocean nations are based on literature reports. Consequently, many
of the species reported here are new records for Yemen and Oman.
Figure 4. Biogeographic affinities (Simpson
Coefficient in %, y-axis) between the
species lists of the DCA clusters and those
of the Indian Ocean nations. The countries
are ordered on the x-axis from the
southwestern Indian Ocean, over the
Arabian Sea, to the southeastern Indian
Ocean: South Africa (1), Mozambique (2),
Madagascar (3), Réunion (4), Mauritius (5),
Tanzania (6), Seychelles (7), Kenya (8),
Somalia (9), Yemen (10), Oman (11), Iran
(12), Pakistan (13), Laccadive (14), Maldives
(15), Sri Lanka (16), Bangladesh (17),
Andaman (18), Malaysia (19), Indonesia
(20), Australia (21). DCA cluster symbols as
in Fig. 1: MAS WC (open triangles), MAS
SG (open boxes), MAS EC (open circles),
S&O NC (filled triangles), SOC NC (stars),
and S&O SC (filled circles). (a) Quartic
polynomial trend lines of the biogeographic
affinity of the DCA clusters based on the
species records. (b) Quartic polynomial
trend lines of the biogeographic affinity of
the DCA clusters based on the generic
records. The biogeographic affinities of Sri
Lanka behave as outliers for all polynomial
trend lines, hence their separate
representation in both graphs.

Phytogeography in the Arabian Sea 117
In both biogeographic analyses, Sri Lanka is an outlier (Figs 4a, b). To date, no other
reports of strong affinities between the marine communities of the Arabian Sea and Sri
Lanka are known. Being on the crossroads of the Arabian Sea, the Bay of Bengal and the
Indian Ocean, the high similarities can be attributed to common Indian Ocean taxa that also
occur in the tropical regions of the East African Coast (e.g. Kenya and Tanzania).
Calculations support this statement: out of the 83 species that the Arabian Sea (ordination
data) and Sri Lanka share, 76 and 73 species have also been reported for Kenya and
Tanzania, respectively. Of the 85 genera found in the Arabian Sea and Sri Lanka, 80 and 83
genera are also known for Kenya and Tanzania, respectively.
Indicator species
The species, with a significant indicator value (P < 0.05), listed in Table 3 prove to be
characteristic for the identified DCA clusters. S&O NC contains only three indicator species,
being common Indian Ocean taxa. The indicator species of MAS WC are predominantly
composed of Phaeophyta (6/9). The indicator species Nizamuddinia zanardinii and
Lomentaria strumosa are endemic for the Arabian Sea and ecologically associated to the
upwelling phenomenon (Kemp, 1998a). The other large Phaeophyta (Dictyota
bartayresiana, Sargassum spp., Stoechospermum polypodioides, Turbinaria ornata) are
generally linked to increased nutrient levels in (sub)tropical seas (Schaffelke & Klumpp,
1998). MAS EC is typified by indicator species predominantly belonging to the Rhodophyta.
Many of these species are indicative of colder water, e.g. Calliblepharis fimbriata,
Kallymenia crassiuscula, Plocamium telfairiae and Rhodymenia spp., and show a disjunct
distribution pattern within the Indo-Pacific. Similar observations to those of MAS EC apply
for the indicator species of S&O SC. Despite the high number of species records for SOC
NC, the majority of species found in this cluster also occur in other clusters. This results in
only three species with significant indicator values, being common Indian Ocean species.
The species-rich seagrass beds of MAS WC are characterized by plants typically associated
with these habitats. SOC SG was excluded from the analysis because of its extremely low
species richness.
In a second analysis, the plant communities of both islands (DCA clusters) are united in
biotopes, based on similarities in species composition and biogeographic trends. This results
in 3 clusters that are composed of Socotra and Masirah sites, and a single Socotra cluster.
S&O NC and MAS WC are united in a cluster composed of upwelling sheltered sites, S&M
SS. S&O SC and MAS EC are combined in a cluster composed of upwelling affected sites,
S&M US. SOC SG and MAS SG are joined in the cluster of seagrass communities, S&M
SG. SOC NC shows the highest similarity in species composition with S&O SC though its
biogeographic affinity more closely resembles that of S&O NC. Because of its mixed
behaviour, SOC NC was retained from aggregation with other clusters. The sites of these
cluster groupings correspond with the areas of both islands that are subject to similar
seasonal environmental conditions. A subsequent species indicator analysis revealed the
species that are characteristic for each of the four biotopes in the Arabian Sea (Table 4).

118 Chapter 7
Table 3. Species with significant probabilities (P < 0.05) and indicator values (IV, % perfect indication)
for each of the plant communities (DCA clusters). High indicator values are marked in bold and grouped
according to cluster preference. Probabilities are based on 1000 Monte Carlo permutations. Cluster
abbreviations as in Fig. 1. The species abbreviations correspond to the species listed in appendix 1.
Species S&O NC MAS W
C
MAS EC S&O SC SOC NC MAS SG P
Sar_lin
38
0 0 0 0 0 0.027
Dic_fri
37
0 1 1 0 0 0.008
Gel_pan
25
0 0 0 0 0 0.039
Niz_zan 2
64
0 0 0 0 0.002
Sar_sp1 0
56
0 0 0 6 0.002
Sto_pol 3
52
5 0 1 3 0.004
Lom_stru 0
50
0 0 0 0 0.010
Bry_spe 1
49
1 2 0 0 0.003
Pte_cae
15 38
2 4 2 2 0.017
Tur_orn 2
35
0 1 0 0 0.030
Dic_bar 0
35
1 0 2 0 0.035
Sar_pil 0
33
0 0 0 8 0.039
Plo_tel 0
21 41
0 0 0 0.018
Rho_sp2 0 0
70
0 0 0 0.001
Rho_sp1 0 7
52
0 0 0 0.001
Dic_cri 0 6
44
2 0 0 0.006
Kal_spe 0 0
43
1 0 0 0.011
Cal_fim 0 0
40
0 0 0 0.007
Sci_tsi 0 0
37
7 1 0 0.035
Gra_tex 0 0
33
1 0 0 0.022
Amp_anc 0 4
32 22
0 0 0.020
Hal_com 0 0 0
67
0 0 0.001
Bot_lep 0 0 0
50
0 0 0.012
Hal_dup 0 0 0
50
0 0 0.005
Zel_spe 0 0 0
42
0 0 0.007
Cry_spe 0 0 0
33
2 0 0.012
Cha_ind 0 0 0
33
0 0 0.049
Ast_pel 3 0 0
32
0 0 0.021
Cau_lan 0 0 0 3
64
0 0.002
Gra_deb 0 0 2 0
47
0 0.006
Amp_fra 5 0 0 8
44
0 0.010
Hal_uni 0 0 0 0 1
90
0.001
Hal_ova 0 0 0 0 0
75
0.001
Cho_pap 0 0 0 0 1
65
0.004
Gra_sal 0 0 0 0 0
50
0.014
Sar_fil 0 0 0 0 2
41
0.023
Boe_for 0 0 0 4 0
38
0.008
Cau_len 0 0 0 1 2
36
0.032
Cau_sca 0 0 0 1 2
36
0.028
Nizamuddinia zanardinii and Sargassum linearifolium are indicator species of S&M SS
that make up the largest biomass stands of the studied macroalgal communities (excl. the
seagrass communities; T. Schils pers. obs.). Besides N. zanardinii, the indicator species of
S&M SS have a wide (sub)tropical distribution within the Indian Ocean. As a consequence
of uniting S&O SC and MAS EC, the indicator species of S&M US are predominantly
Rhodophyta, composing very diverse algal communities. Again, species indicative for colder
water characterize this biotope, e.g. Kallymenia crassiuscula and Rhodymenia sp. 2. More
indicator species were found for SOC NC in the second analysis, this however, being

Phytogeography in the Arabian Sea 119
characteristic for similar habitats as those examined in the first analysis. The indicator
species of S&M SG are also identical to those of MAS SG in the previous species indicator
analysis.
Table 4. Species with significant probabilities (P < 0.05) and indicator values (IV, % perfect indication)
for each of the biotopes (groups of DCA clusters). Biotope 1, upwelling sheltered areas (S&M SS): MAS
WC, S&O NC; biotope 2, upwelling exposed area (S&M US): MAS EC, S&O SC; biotope 3, distinct
north coast entity of Socotra: SOC NC; biotope 4, seagrass beds (S&M SG): MAS SG, SOC SG. High
indicator values are marked in bold and grouped according to biotope preference. Probabilities are based
on 1000 Monte Carlo permutations. The species abbreviations correspond to the species listed in
appendix 1.
Species S&M SS S&M US SOC NC S&M SG P
Pte_cae
39
5 3 3 0.018
Niz_zan
33
0 0 0 0.009
Val_pac
29
1 0 0 0.018
Dic_fri
26
2 0 0 0.032
Sar_lin
25
0 0 0 0.047
Amp_anc 1
56
0 0 0.001
Lau_ped 1
40
2 0 0.016
Car_mai 4
38
0 0 0.018
Gal_mar 0
36
0 0 0.024
Hal_com 0
36
0 0 0.019
Seb_fla 0
36
0 0 0.028
Dic_cri 1
34
0 0 0.037
Rho_sp2 0
32
0 0 0.030
Sci_tsi 0
32
2 0 0.049
Sch_spe 2
30
0 0 0.047
Bot_lep 0
27
0 0 0.027
Hal_dup 0
27
0 0 0.035
Hyp_spe 0
27
0 0 0.032
Kal_spe 0
27
0 0 0.029
Hal_dct 0
23 38
8 0.045
Cau_lan 0 1
70
0 0.001
Amp_fra 2 3
54
0 0.002
Gra_deb 0 0
51
0 0.004
Pad_aus 0 1
29
0 0.048
Cho_sp2 0 0
22
0 0.040
Cla_lon 0 0
22
0 0.040
Hlp_spe 0 0
22
0 0.040
Hal_uni 0 0 1
90
0.001
Hal_ova 0 0 0
80
0.001
Cho_pap 0 0 2
51
0.002
Gra_sal 0 0 0
40
0.008
Boe_for 0 2 0
33
0.015
Sar_fil 0 0 2
31
0.030

120 Chapter 7
DISCUSSION
The plant communities defined in this study cover a larger geographic area compared to
those derived from a biomass analysis of quadrat data around the Socotra archipelago (T.
Schils & E. Coppejans submitted). The transition zone between Socotra’s south and north
coast, and the outer island communities (both with a pronounced south coast affinity) are in
the present study included in S&O SC. The analysis of species inventories hence results in a
substantial loss of resolution because the species structure (biomass data) of the different
communities is excluded from the information input. However, in a comparison between the
plant communities of different geographic locations (both islands), analogies among the
communities of both islands can satisfactorily be assessed by a holistic approach
incorporating analyses of site data (ordination), species data (similarity indices) and
biogeographic distribution patterns. The environmental parameters show two types of
correlation with respect to the plant communities. The first one includes the parameters with
high correlations for the first DCA axis. SAL_AV and SAL_NE are negatively correlated
with the first axis, corresponding with the high salinity concentrations recorded for the
seagrass communities (MAS SG and SOC SG), SOC NC and S&O NC. The absolute
difference in salinity values, however, is the largest for the upwelling areas (MAS EC and
S&O SC) where the changes in salinity between both monsoons are greatest. The second
type of correlation is related to the differences between the Socotra and Masirah clusters,
following the resultant of both DCA axes. All chlorophyll a parameters have relatively high
(positive) correlations with both axes, showing overall higher chlorophyll a concentrations
for Masirah. The latter environmental variable is indicative of primary production, dependent
on increased nutrient levels and thus related to the intensity of upwelling. Table 1 shows that
the resultant of both axes has the highest positive correlation with CHL_SW, which
corresponds to the chlorophyll a concentrations for Masirah during the SW monsoon, being
the highest observed values (2.20 µg l
-1
). The chlorophyll a concentrations thus show that the
effect of upwelling is more pronounced at Masirah Island.
Plant communities and biotopes
Upwelling sheltered sites (S&M SS): S&O NC and MAS WC
S&O NC has the highest similarity (0.48) in species composition with MAS WC. The
ordination also shows an overlap between the sites of these clusters. MAS WC, on the other
hand, has the highest tripartite similarity values with MAS EC (0.51), but the biogeographic
affinities within the Indian Ocean are quite different between both. The biogeographic
affinity of S&O NC, on a species level, is higher for the East African coast and the Arabian
Sea compared to that of MAS WC. Based on the generic records, S&O NC and MAS WC
also have similar Indian Ocean affinities, however, MAS WC again has a lower affinity for
the East African coast. This shows that the Socotra community has a higher transient
character from the Western Indian Ocean to the Arabian Sea, and the Masirah community
comprises a higher proportion of typical Arabian Sea taxa. The biotope of upwelling
sheltered sites has 85 species records in total. The indicator species of the plant communities,
and the biotope in general, reflect the seasonally high biomass stands for this area. These
communities have a macroalgal cover up to 100% and their species are indicative of
seasonally high nutrient levels. Besides common Indian Ocean taxa, the endemic
Nizamuddinia zanardinii grows abundantly at these partly sheltered sites.

Phytogeography in the Arabian Sea 121
Upwelling affected sites (S&M US): S&O SC and MAS EC
The ordination plot (Fig. 2) shows a gradual spread of the S&O SC sites towards MAS EC.
The tripartite similarity (Table 2) of the complete species list is high between both clusters
(0.47), although both clusters have a comparably high similarity with other biotopes from
their islands, i.e. MAS EC-MAS WC (0.51) and S&M SC-SOC NC (0.47). This is a result of
the high number of species recorded for the S&M US clusters (80 spp. and 131 spp.) and the
inclusion of transition sites between the sheltered and upwelling biotopes. In fact, a detailed
analysis of vegetation quadrats of the Socotra archipelago revealed that the southeastern tip
of Socotra is a diverse, intermediate cluster between the north and south communities (T.
Schils & E. Coppejans submitted). This low scale resolution has not been detected in the
analyses of the species inventories, which is reflected in the high number of species recorded
for S&M US: 158 species. The indicator species of this biotope are largely Rhodophyta.
These red algae are common elements of species rich communities, often associated with a
well-developed understory flora.
Distinct entity of Socotra’s north coast (SOC NC)
This cluster was retained from grouping, it is characterized by a high species richness (76
spp.) and its affinities with other clusters differ between the analyses. In the DCA, the sites
of SOC NC are plotted in between those of S&M SG and S&O SC. Its tripartite similarity is
highest with S&O SC (0.47), the cluster with the highest species richness. As discussed
under S&M US, S&O SC comprises transition zones between Socotra’s north and south
coast, increasing the affinity between SOC NC and S&O SC. The biogeographic analyses of
SOC NC, however, shows a similar trend as the communities of S&M SS, most pronounced
in the generic analysis. The indicator species analysis provides an insight into the
characteristic species of this cluster: these species are common Indian Ocean algae growing
in sheltered environments, often associated with fine sediment (sandy patches or hard
substratum covered by a fine sand layer). Although typified by different habitat specific
species, this biotope is regarded as a sub-entity of the upwelling sheltered shores (S&M SS).
The macroalgal stands of the SOC NC sites are governed by high physical stress (bioerosion
due to sand scouring) and, hence, characterized by a much lower biomass and substratum
cover in comparison to S&M SS sites.
Seagrass communities (S&M SG): MAS SG and SOC SG
In the DCA plot, the sites of both islands cluster together. SOC SG has the greatest similarity
with MAS SG, the tripartite similarity between the seagrass communities of both islands
being low, however. This results from the species-poor (5 spp.) seagrass beds at Qalansiyah
lagoon (Socotra), predominantly comprised of the seagrasses Halodule uninervis, Halophila
ovalis and Thalassia hemprichii. The indicator species of this biotope as a whole are well
known to occur in seagrass beds. Analogous to the discussion of SOC NC, this entity can be
regarded as a sub-entity of S&M SS, constituting a specific biotope within the sheltered
coasts of both islands. This is reflected in the rather high similarity values of the species rich
seagrass communities of MAS SG with SOC NC, S&O NC and MAS WC.

122 Chapter 7
CONCLUSIONS
The analysis of two upwelling areas within the Arabian Sea presented here shows (i) the
identification of similar plant communities (upwelling affected areas, upwelling sheltered
areas, seagrass communities) at both islands, based on their taxon (species and genera)
composition, and (ii) an increased divergence of the East African flora from Socotra towards
Masirah. In this respect the Socotra Archipelago is a stepping stone between marine plant
communities of the East African coast and the Arabian Sea. The plant communities of the
upwelling sheltered sites can be grouped in 3 distinct biotopes depending on the degree of
exposure (reflected in the degree of sedimentation): (i) the seagrass beds in the protected
embayments (MAS SG and SOC SG), (ii) a floristic entity related to a sand covered
substratum (SOC NC, including a few seagrass communities of protected sites on Socotra’s
south coast), and (iii) the macroalgal communities of more exposed sites (often associated
with well-developed coral communities; S&O NC and MAS WC). The peculiar marine
floristics that characterize the uniqueness of the Arabian Sea predominantly occur at the
upwelling affected shores. The plant communities of these areas show a marked
biogeographic affinity with distant areas (South Africa and Western Australia; Figs 4a, b)
due to the disjunct distribution pattern of certain taxa (Wynne 2000; Schils & Coppejans
2002; Schils et al. 2003a). The species richness of the upwelling affected communities is the
highest, with a large proportion of red algae (comprising most of the indicator species of this
biotope) in the total species composition (Figs 3a, b). This biotope also includes species-rich
overlap communities towards the upwelling sheltered sites being, however, clearly
characterized as upwelling communities.
In comparison to faunistic studies of the area (Apel 2000), it is important to note that the
characteristic plant communities of the Arabian Sea are situated at opposing biotopes where
faunistic (e.g. corals, decapods, etc.) diversity, species richness and endemism thrive. The
evolution towards distinct biogeographic entities (e.g. centre of endemism along the southern
Arabian Peninsula) at these favourable biotopes within the Indian Ocean is most likely the
result of vicariation events. The environmental barriers (warmer and less nutrient-enriched
waters) isolating the macroalgal communities are the favourable biotopes of the faunistic
communities, and vice versa. The occurrence of these opposing biotopes in a restricted
geographic area, make both islands a haven for both the characteristic floristic and faunistic
communities of the Arabian Sea. Consequently, these islands can be reasonably well
managed from a logistical and financial point of view, serving as ideal subjects of intended
conservation efforts (e.g. Socotra Biodiversity Project, GEF/Ned/UNDP) to preserve the
unique biotic communities of the Arabian Sea.
A
CKNOWLEDGEMENTS
Thanks are expressed to the Senckenberg Research Institute (Michael Apel and Fareed
Krupp; Germany) and the Ardoukoba Organization (France) for the excellent field trip
preparations to the Socotra Archipelago and Masirah Island, respectively. We are grateful to
Frederik Leliaert and Olivier De Clerck for their help in identifying Cladophorales and
Dictyota specimens. The English text was kindly checked by Enrico Tronchin. Tom Schils is
indebted to the Fund for Scientific Research Flanders (FWO, Belgium) for his research
assistant grant.

Phytogeography in the Arabian Sea 123
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126 Chapter 7
APPENDIX
Appendix 1. Species recorded for Masirah Island and the Socotra Archipelago, including the
abbreviations used in the analyses and the cluster occurrences of each species. Cluster abbreviations as in
Fig. 1.
RHODOPHYTA
AHNFELTIALES
AHNFELTIACEAE
Schottera sp. (Sch_spe) - MAS EC - MAS WC -
S&O SC
BONNEMAISONIALES
BONNEMAISONIACEAE
Asparagopsis taxiformis (Delile) Trevisan (Asp_tax) -
MAS EC - MAS WC - S&O SC
NACCARIACEAE
Reticulocaulis mucosissimus I.A. Abbott (Ret_muc) -
MAS EC
Reticulocaulis obpyriformis Schils, De Clerck &
Coppejans (Ret_obp) - S&O SC
CERAMIALES
CERAMIACEAE
Antithamnion sp. (Ant_spe) - MAS EC - SOC NC -
S&O SC
Balliella repens Huisman & Kraft (Bal_spe) - S&O
NC - S&O SC
Balliella subcorticata (Itono) Itono & Tanaka
(Bal_spe) - S&O SC
Balliella sp. (Bal_spe) - MAS EC - MAS WC
Centroceras clavulatum (C. Agardh) Montagne
(Cen_cla) - SOC NC - S&O NC
Centroceras sp. (Cen_cla) - MAS SG
Ceramium sp. (Cer_spe) - MAS EC - MAS WC -
SOC NC - S&O SC
Euptilota fergusonii Cotton (Eup_fer) - MAS EC -
MAS WC - S&O SC
Griffithsia sp. (Gri_spe) - SOC NC - S&O SC
Haloplegma duperreyi Montagne (Hal_dup) - S&O
SC
Spyridia hypnoides (Bory de Saint-Vincent)
Papenfuss (Spy_spe) - SOC NC - S&O NC
Spyridia sp. (Spy_spe) - MAS EC - SOC NC - S&O
SC
Sympodothamnion leptophyllum (Tanaka) Itono
(Sym_lep) - S&O SC
DASYACEAE
Amphisbetema indica (J. Agardh) Weber-van Bosse
(Amp_ind) - S&O SC
Dasya flagellifera Børgesen (Das_spe) - S&O SC
Dasya sp. (Das_spe) - MAS EC - SOC NC - S&O SC
Dictyurus purpurascens Bory de Saint-Vincent
(Dic_pur) - S&O SC
Heterosiphonia sp. (Het_spe) - S&O SC
DELESSERIACEAE
Acrosorium venulosum (Zanardini) Kylin (Acr_spe) -
MAS EC
Acrosorium sp. (Acr_spe) - MAS EC - S&O NC -
S&O SC
Chauviniella coriifolia (Harvey) Papenfuss (Cha_cor)
- S&O SC
Chauviniella jadinii (Børgesen) Papenfuss (Cha_jad)
- MAS EC
Claudea elegans Lamouroux (Cla_ele) - MAS EC -
S&O SC
Cryptopleura sp. (Crp_spe) - MAS EC
Duckerella ferlusii (Hariot) Wynne (Duc_fer) - S&O
SC
Hypoglossum heterocystideum (J. Agardh) J. Agardh
(Hyp_spe) - MAS EC
Hypoglossum sp. (Hyp_spe) - MAS EC - S&O SC
Martensia elegans Hering (Mar_ele) - S&O SC
Zellera sp. (Zel_spe) - S&O SC
RHODOMELACEAE
Acanthophora dendroides Harvey (Aca_den) - MAS
SG - SOC NC - S&O SC
Acanthophora spicifera (Vahl) Børgesen (Aca_spi) -
SOC NC
Amansia rhodantha (Harvey) J. Agardh (Ama_rho) -
S&O SC
Chondria armata (Kützing) Okamura (Cho_arm) -
S&O SC
Chondria dangeardii Dawson (Cho_dan) - MAS EC -
S&O SC
Chondria sp. 1 (Cho_sp1) - MAS EC - SOC NC -
S&O NC - S&O SC
Chondria sp. 2 (Cho_sp2) - SOC NC
Chondrophycus papillosus (C. Agardh) Garbary &
Harper (Cho_pap) - MAS SG - SOC NC
Digenea simplex (Wulfen) C. Agardh (Dig_sim) -
MAS SG
Herposiphonia nuda Hollenberg (Her_spe) - SOC NC
- S&O SC
Herposiphonia parca Setchell (Her_spe) - SOC NC
Herposiphonia sp. (Her_spe) - SOC NC - S&O SC
Laurencia columellaris Børgesen (Lau_col) - SOC
NC - S&O SC
Laurencia majuscula (Harvey) Lucas (Lau_maj) -
MAS SG - SOC NC - S&O NC - S&O SC
Laurencia parvipapillata Tseng (Lau_par) - S&O SC
Laurencia pedicularioides Børgesen (Lau_ped) -
MAS EC - SOC NC - S&O NC - S&O SC
Laurencia perforata (Bory de Saint-Vincent)
Montagne (Lau_per) - MAS WC - S&O SC -
SOC SG

Phytogeography in the Arabian Sea 127
Leveillea jungermannioides (Hering & G. Martens)
Harvey (Lev_jun) - MAS WC - MAS SG - S&O
NC
Lophocladia sp. (Lop_spe) - S&O SC
Melanamansia sp. (Mel_spe) - MAS EC - SOC NC
Melanothamnus somalensis Bornet & Falkenberg
(Mel_som) - MAS WC
Osmundaria melvillii (J. Agardh) R. Norris
(Osm_mel) - SOC NC - S&O SC
Polysiphonia sp. (Pol_spe) - MAS WC - S&O SC
Tolypiocladia glomerulata (C. Agardh) Schmitz
(Tol_glo) - MAS WC
CORALLINALES
CORALLINACEAE
Amphiroa anceps (Lamarck) Decaisne (Amp_anc) -
MAS EC - MAS WC - S&O SC
Amphiroa beauvoisii Lamouroux (Amp_bea) - MAS
EC - MAS WC - S&O NC - S&O SC
Amphiroa fragilissima (Linnaeus) Lamouroux
(Amp_fra) - SOC NC - S&O NC - S&O SC
Amphiroa misakiensis Yendo (Amp_bea) - MAS EC -
S&O NC
Amphiroa rigida Lamouroux (Amp_fra) - SOC NC -
S&O NC - S&O SC
Amphiroa sp. (Amp_bea) - MAS SG
Haliptilon sp. (Hlp_spe) - SOC NC
Jania sp. (Jan_spe) - MAS WC - MAS SG - SOC NC
- S&O NC - S&O SC
SPOROLITHACEAE
Sporolithon sp. (Spo_spe) - MAS SG - S&O NC
GELIDIALES
GELIDIACEAE
Pterocladia cf. caloglossoides (Howe) Dawson
(Pte_cfe) - MAS EC - MAS WC - S&O NC -
S&O SC
Pterocladiella caerulescens (Kützing) Santelices &
Hommersand (Pte_cae) - MAS EC - MAS WC -
MAS SG - SOC NC - S&O NC - S&O SC
GELIDIELLACEAE
Gelidiella acerosa (Forsskål) J. Feldmann & G.
Hamel (Gel_ace) - MAS WC - MAS SG - S&O
NC
Gelidiella pannosa (Feldmann) Feldmann & Hamel
(Gel_pan) - S&O NC
GIGARTINALES
CYSTOCLONIACEAE
Calliblepharis fimbriata (Greville) Kützing (Cal_fim)
- MAS EC
DUMONTIACEAE
Dudresnaya capricornica Robins & Kraft (Dud_cap)
- S&O SC
Gibsmithia larkumii Kraft (Gib_lar) - S&O SC
HYPNEACEAE
Hypnea charoides Lamouroux / valentiae (Turner)
Montagne complex (Hyp_cha) - MAS SG - SOC
NC - S&O NC - S&O SC - SOC SG
Hypnea musciformis (Wulfen) Lamouroux
(Hyp_mus) - MAS EC - S&O NC - S&O SC
Hypnea pannosa J. Agardh (Hyp_pan) - MAS WC -
S&O NC - S&O SC
Hypnea spinella (C. Agardh) Kützing (Hyp_cha) -
MAS EC - MAS SG - SOC NC - S&O NC -
S&O SC - SOC SG
KALLYMENIACEAE
Kallymenia crassiuscula Okamura 1934 (Kal_spe) -
MAS EC
Kallymenia sp. (Kal_spe) - MAS EC - S&O SC
NEMASTOMATACEAE
Predaea laciniosa Kraft (Pre_lac) - MAS EC - S&O
SC
Predaea weldii Kraft & I.A. Abbott (Pre_wel) - MAS
EC - MAS WC
RHIZOPHYLLIDACEAE
Portieria hornemannii (Lyngbye) P. Silva (Por_hor) -
MAS EC - MAS WC - SOC NC - S&O NC -
S&O SC
SARCODIACEAE
Sarcodia montagneana (J. Hooker & Harvey) J.
Agardh (Sar_mon) - MAS EC - MAS WC - S&O
SC
SCHIZYMENIACEAE
Platoma heteromorphum Schils (Pla_het) - MAS EC
Titanophora pikeana (Dickie) J. Feldmann (Tit_pik) -
S&O SC
SOLIERIACEAE
Callophycus serratus (Harvey ex Kützing) P.C. Silva
(Cal_ser) - S&O SC
Sarconema filiforme (Sonder) Kylin (Sar_fil) - MAS
SG - SOC NC
Sarconema sp. (Sar_fil) - SOC NC
Solieria robusta (Greville) Kylin (Sol_rob) - MAS
EC - S&O SC
GRACILARIALES
GRACILARIACEAE
Gracilaria corticata (J. Agardh) J. Agardh (Gra_mil)
- MAS WC - MAS SG - SOC NC - S&O SC
Gracilaria debilis (Forsskål) Børgesen (Gra_deb) -
MAS EC - SOC NC
Gracilaria millardetii (Montagne) J. Agardh
(Gra_mil) - MAS EC - SOC NC - S&O NC -
S&O SC
Gracilaria salicornia (C. Agardh) Dawson (Gra_sal)
- MAS SG
Gracilaria textorii (Suringar) De Toni (Gra_tex) -
MAS EC - S&O SC
HALYMENIALES
HALYMENIACEAE
Carpopeltis maillardii (Montagne & Millardet)
Chiang (Car_mai) - MAS EC - MAS WC - S&O
NC - S&O SC
Carpopeltis sp. (Car_mai) - MAS EC
Cryptonemia sp. (Cry_spe) - SOC NC - S&O SC

128 Chapter 7
Halymenia durvillei Bory de Saint-Vincent (Hal_por)
- SOC NC - S&O SC
Halymenia porphyraeformis Parkinson (Hal_por) -
MAS EC - MAS WC
PEYSSONNELIACEAE
Peyssonnelia sp. (Pey_spe) - MAS EC - MAS WC -
SOC NC - S&O NC - S&O SC
SEBDENIACEAE
Sebdenia flabellata (J. Agardh) Parkinson (Seb_fla) -
MAS EC - S&O SC
NEMALIALES
GALAXAURACEAE
Galaxaura marginata (Ellis & Solander) Lamouroux
(Gal_mar) - MAS EC - S&O SC
Galaxaura obtusata (Ellis & Solander) Lamouroux
(Gal_obt) - MAS EC - S&O SC
Galaxaura rugosa (Ellis & Solander) Lamouroux
(Gal_rug) - S&O SC
Scinaia complanata (Collins) Cotton (Sci_com) -
MAS EC
Scinaia hormoides Setchell (Sci_mon) - MAS EC
Scinaia moniliformis J. Agardh (Sci_mon) - S&O SC
Scinaia tsinglanensis Tseng (Sci_tsi) - MAS EC -
SOC NC - S&O SC
Tricleocarpa cylindrica (Ellis & Solander) Huisman
& Borowitzka (Tri_cyl) - SOC NC - S&O SC
Tricleocarpa fragilis (Linnaeus) Huisman &
Townsend (Tri_fra) - S&O SC
LIAGORACEAE
Liagora ceranoides Lamouroux (Lia_spe) - SOC NC
Liagora sp. (Lia_spe) - MAS WC - SOC NC
PLOCAMIALES
PLOCAMIACEAE
Plocamium fimbriatum Wynne (Plo_fim) - MAS EC -
MAS WC
Plocamium microcladioides South & N.M. Adams
(Plo_mic) - MAS EC - MAS WC
Plocamium telfairiae (J. D. Hooker et Harvey)
Harvey ex Kützing (Plo_tel) - MAS EC - MAS
WC
Plocamium telfairiae (J. D. Hooker et Harvey)
Harvey ex Kützing var. uncinatum (Plo_tel) -
MAS EC - MAS WC
RHODYMENIALES
CHAMPIACEAE
Champia compressa Harvey (Cha_com) - MAS EC -
MAS WC - SOC NC - S&O SC
Champia indica Børgesen (Cha_ind) - S&O SC
Champia parvula (C. Agardh) Harvey (Cha_com) -
MAS SG - SOC NC - S&O NC - S&O SC
FAUCHEACEAE
Fauchea sp. (Fau_spe) - MAS EC
Gloiocladia sp. (Glo_spe) - S&O SC
LOMENTARIACEAE
Gelidiopsis sp. (Gel_var) - MAS EC - SOC NC -
S&O NC - S&O SC
Gelidiopsis variabilis J. Agardh (Schmitz) (Gel_var) -
MAS EC - SOC NC - S&O SC
Lomentaria strumosa Wynne (Lom_stru) - MAS WC
RHODYMENIACEAE
Asteromenia peltata (W.R. Taylor) Huisman & Millar
(Ast_pel) - S&O NC - S&O SC
Botryocladia leptopoda (J. Agardh) Kylin (Bot_lep) -
S&O SC
Botryocladia skottsbergii (Børgesen) Levring
(Bot_sko) - S&O SC
Chamaebotrys sp. (Chm_spe) - S&O SC
Chrysymenia grandis Okamura (Chr_gra) - MAS EC
- S&O SC
Chrysymenia sp. (Chr_spe) - MAS EC - S&O SC
Coelarthrum opuntia (Endlicher) Børgesen
(Coe_opu) - SOC NC - S&O SC
Erythrocolon podagricum J. Agardh (Ery_pod) -
S&O SC
Rhodymenia sp. 1 (Rho_sp1) - MAS EC - MAS WC
Rhodymenia sp. 2 (Rho_sp2) - MAS EC
PHAEOPHYTA
DICTYOTALES
DICTYOTACEAE
Dictyopteris delicatula Lamouroux (Dic_del) - S&O
SC
Dictyopteris macrocarpa (Areschoug) O. Schmidt
(Dic_mac) - MAS EC - S&O SC
Dictyopteris membranacea (Stackhouse) Batters
(Dic_pol) - SOC NC
Dictyopteris polypodioides (De Candolle) Lamouroux
(Dic_pol) - SOC NC - S&O NC - S&O SC
Dictyota bartayresiana Lamouroux (Dic_bar) - MAS
EC - MAS WC - SOC NC
Dictyota cervicornis Kützing (Dic_cer) - MAS SG -
SOC NC - S&O NC - S&O SC
Dictyota ceylanica Kützing (Dic_cey) - MAS EC -
MAS WC - SOC NC - S&O NC - S&O SC
Dictyota ciliolata Kützing (Dic_cil) - MAS EC -
MAS WC
Dictyota crispata Lamouroux (Dic_cri) - MAS EC -
MAS WC - S&O SC
Dictyota dichotoma (Hudson) Lamouroux var.
intricata (C. Agardh) Greville (Dic_cer) - S&O
SC
Dictyota friabilis Setchell (Dic_fri) - MAS EC - S&O
NC - S&O SC
Dictyota grossedentata De Clerck & Coppejans
(Dic_gro) - S&O SC
Dictyota stolonifera Dawson (Dic_sto) - S&O SC
Lobophora variegata (Lamouroux) Womersley ex
Oliveira (Lob_var) - MAS EC - MAS WC -
MAS SG - S&O NC - S&O SC
Padina antillarum (Kützing) Piccone (Pad_ant) -
MAS EC

Phytogeography in the Arabian Sea 129
Padina australis Hauck (Pad_aus) - SOC NC - S&O
SC
Padina boergesenii Allender & Kraft (Pad_boe) -
MAS SG - SOC NC - S&O NC - S&O SC
Padina dubia Hauck (Pad_gym) - MAS EC - MAS
WC
Padina elegans Koh ex Womersley (Pad_ele) - MAS
EC - S&O SC
Padina glabra Gaillard (Pad_gym) - MAS EC - MAS
WC
Padina gymnospora (Kützing) Sonder (Pad_gym) -
SOC NC - S&O NC
Padina minor Yamada (Pad_min) - MAS SG
Spatoglossum asperum J. Agardh (Spa_asp) - MAS
EC - MAS WC - SOC NC - S&O NC - S&O SC
Stoechospermum polypodioides (Lamouroux) J.
Agardh (Sto_pol) - MAS EC - MAS WC - MAS
SG - SOC NC - S&O NC
Stypopodium sp. (Sty_spe) - SOC NC - S&O SC
ECTOCARPALES
ECTOCARPACEAE
Ectocarpus sp. (Ect_spe) - SOC NC - S&O SC
FUCALES
CYSTOSEIRACEAE
Cystoseira indica (Thivy & Doshi) Mairh (Cys_ind) -
MAS SG
Cystoseira myrica (S. Gmelin) C. Agardh (Cys_myr)
- MAS SG
Hormophysa cuneiformis (J. Gmelin) P. Silva
(Hor_cun) - SOC NC
SARGASSACEAE
Nizamuddinia zanardinii (Schiffner) P. Silva
(Niz_zan) - MAS WC - S&O NC
Sargassum angustifolium C. Agardh (Sar_ang) - SOC
NC - S&O SC
Sargassum decurrens (R. Brown ex Turner) C.
Agardh (Sar_dec) - MAS WC - S&O SC
Sargassum latifolium (Turner) C. Agardh (Sar_lat) -
MAS EC - MAS WC - S&O SC
Sargassum linearifolium (Turner) C. Agardh
(Sar_lin) - S&O NC
Sargassum oligocystum Montagne (Sar_oli) - MAS
WC - MAS SG
Sargassum piluliferum (Turner) C. Agardh (Sar_pil) -
MAS WC - MAS SG
Sargassum sp. (Sar_sp1) - MAS WC - MAS SG
Turbinaria ornata (Turner) J. Agardh (Tur_orn) -
MAS WC - S&O NC - S&O SC
SCYTOSIPHONALES
CHNOOSPORACEAE
Chnoospora implexa J. Agardh (Chn_imp) - S&O NC
SCYTOSIPHONACEAE
Colpomenia sinuosa (Mertens ex Roth) Derbès &
Solier (Col_sin) - SOC NC - S&O SC
Hydroclathrus clathratus (C. Agardh) Howe
(Hyd_cla) - SOC NC
Rosenvingea intricata (J. Agardh) Børgesen (Ros_int)
- S&O NC - S&O SC
CHLOROPHYTA
BRYOPSIDALES
BRYOPSIDACEAE
Bryopsis hypnoides Lamouroux (Bry_spe) - S&O SC
Bryopsis indica A. Gepp & E. Gepp (Bry_spe) - MAS
EC - MAS WC - S&O SC
Bryopsis pennata Lamouroux (Bry_spe) - MAS WC
Bryopsis sp. (Bry_spe) - S&O NC
Pseudobryopsis hainanensis Tseng (Pse_spe) - MAS
EC - MAS SG
CAULERPACEAE
Caulerpa brachypus Harvey (Cau_bra) - S&O SC
Caulerpa cupressoides (Vahl) C. Agardh (Cau_cup) -
SOC NC
Caulerpa lanuginosa J. Agardh (Cau_lan) - SOC NC
- S&O SC
Caulerpa lentillifera J. Agardh (Cau_len) - MAS SG
- SOC NC - S&O SC
Caulerpa mexicana Sonder ex Kützing (Cau_mex) -
MAS EC - MAS SG - SOC NC - S&O SC
Caulerpa peltata Lamouroux (Cau_pel) - MAS EC -
MAS WC - S&O NC - S&O SC
Caulerpa racemosa (Forsskål) J. Agardh (Cau_rac) -
MAS EC - MAS WC - MAS SG - S&O SC
Caulerpa scalpelliformis (R. Brown ex Turner) C.
Agardh (Cau_sca) - MAS SG - SOC NC - S&O
SC
Caulerpa serrulata (Forsskål) J. Agardh (Cau_ser) -
MAS WC - MAS SG
Caulerpa sertularioides (S. Gmelin) Howe (Cau_set)
- MAS SG - SOC NC - S&O SC
CODIACEAE
Codium arabicum Kützing (Cod_ara) - MAS WC -
MAS SG - SOC NC
Codium dwarkense Børgesen (Cod_dwa) - MAS EC -
MAS WC - SOC NC - S&O NC - S&O SC
Codium ovale Zanardini (Cod_ova) - MAS EC
Codium tenue (Kützing) Kützing (Cod_ten) - MAS
EC
DERBESIACEAE
Pedobesia simplex (Kützing) M.J. Wynne & Leliaert
(Ped_sim) - S&O SC
UDOTEACEAE
Avrainvillea lacerata Harvey ex J. Agardh (Avr_lac)
- SOC NC - S&O SC
Chlorodesmis fastigiata (C. Agardh) Ducker
(Chl_fas) - S&O NC
Chlorodesmis sp. (Chl_fas) - MAS EC - MAS SG
Halimeda copiosa Goreau & Graham / minima (W.R.
Taylor) Colinvaux (Hal_com) - S&O SC
Halimeda cuneata Hering (Hal_dct) - SOC NC -
S&O SC
Halimeda discoidea Decaisne (Hal_dct) - MAS SG -
SOC NC - S&O SC

130 Chapter 7
Halimeda stuposa W.R. Taylor (Hal_stu) - SOC NC -
S&O SC
Halimeda tuna (Ellis & Solander) Lamouroux
(Hal_dct) - MAS EC - MAS WC - MAS SG -
SOC NC - S&O SC
Udotea indica A. Gepp & E. Gepp (Udo_ind) - MAS
SG - SOC NC - S&O SC
CLADOPHORALES
ANADYOMENACEAE
Microdictyon sp. (Mic_spe) - S&O SC
CLADOPHORACEAE
Chaetomorpha sp. (Cht_spe) - MAS SG - SOC NC -
S&O SC
Cladophora catenata (Linnaeus) Kützing (Cla_cat) -
MAS EC
Cladophora coelothrix Kützing (Cla_coe) - MAS SG
- SOC NC - S&O SC
Cladophora prolifera (Roth) Kützing (Cla_pro) -
SOC NC
Cladophora sericea (Hudson) Kützing (Cla_ser) -
MAS WC
Cladophora vagabunda (Linnaeus) van den Hoek
(Cla_vag) - MAS EC - MAS WC - SOC NC -
S&O NC - S&O SC
Cladophora sp., section Longi-articulatae (Cla_lon) -
SOC NC
SIPHONOCLADACEAE
Boergesenia forbesii (Harvey) J. Feldmann (Boe_for)
- MAS SG - S&O SC
Boodlea composita (Harvey) Brand (Boo_com) -
SOC NC
Chamaedoris auriculata Børgesen (Cha_aur) - SOC
NC - S&O SC
Chamaedoris delphinii (Hariot) J. Feldmann &
Børgesen (Cha_del) - S&O NC
Cladophoropsis herpestica (Montagne) Howe
(Cla_her) - MAS WC - MAS SG
Cladophoropsis sundanensis Reinbold (Cla_sun) -
MAS SG
Dictyosphaeria cavernosa (Forsskål) Børgesen
(Dic_cav) - S&O NC
Phyllodictyon anastomosans (Harvey) Kraft & M.J.
Wynne (Phy_spe) - S&O NC - S&O SC
Siphonocladus tropicus (P. Crouan & H. Crouan) J.
Agardh (Sip_tro) - SOC NC - S&O SC
Struveopsis siamensis (Egerod) P. Silva (Str_sia) -
S&O SC
Ventricaria ventricosa (J. Agardh) Olsen & J. West
(Ven_ven) - S&O NC
VALONIACEAE
Valoniopsis pachynema (G. Martens) Børgesen
(Val_pac) - MAS EC - MAS WC - S&O NC
DASYCLADALES
DASYCLADACEAE
Neomeris van-bosseae Howe (Neo_van) - SOC NC -
S&O SC
POLYPHYSACEAE
Acetabularia sp. (Ace_spe) - SOC NC - S&O NC -
S&O SC
ULVALES
ULVACEAE
Enteromorpha sp. (Ent_spe) - MAS SG - SOC NC
Ulva sp. (Ulv_spe) - MAS WC - MAS SG - SOC NC
- S&O NC - S&O SC
MAGNOLIOPHYTA
ALISMATALES
CYMODOCEACEAE
Halodule uninervis (Forsskål) Ascherson (Hal_uni) -
MAS SG - SOC NC - SOC SG
Syringodium isoetifolium (Ascherson) Dandy
(Syr_iso) - MAS SG
Thalassodendron ciliatum (Forsskål) den Hartog
(Tha_cil) - MAS SG - SOC NC - S&O NC
HYDROCHARITACEAE
Halophila decipiens Ostenfeld (Hal_dec) - S&O SC
Halophila ovalis (R. Brown) Hooker (Hal_ova) -
MAS SG - SOC SG
Thalassia hemprichii (Ehrenberg) Ascherson
(Tha_hem) - SOC SG

Synthesis and perspectives 131
CHAPTER 8
S
YNTHESIS AND PERSPECTIVES
The present study investigates the marine plant communities of the Arabian Sea, largely
composed of macroalgae. The Arabian Sea is situated in the northern Indian Ocean,
bordering the Gulf of Aden and the African continent to the west, and the Gulf of Oman and
the Indian sub-continent to the east. The ecology and oceanography of the Arabian Sea are
governed by the seasonal monsoon winds, which initiate coastal upwelling in particular
areas. The marine biocoenoses of these upwelling shores are relatively understudied and
seem to represent a distinct entity within the Indian Ocean. The Socotra Archipelago
(Yemen) and Masirah Island (Oman) are situated in two geographically differing upwelling
areas within the Arabian Sea, and both contain a wide diversity of habitats in a restricted
area. The uniqueness of the plant communities of these islands is expressed in their floristic,
biogeographic and ecological aspects. The taxonomic issues are discussed first, followed by
the community analyses.
Species inventories
The inventories of marine macroalgae and seagrasses from the study area, which are used in
the ecological analyses, contain several new species records for the region. The number of
new records from the investigated areas are as follows, where the first number represents the
marine plants identified to species level and the second those only identified to generic level
(the first records of these genera, or species differing from those previously reported):
Masirah Island, 90 and 19 species; Oman, 48 and 12 species; Socotra Archipelago, 130 and
28 species; Yemen, 92 and 20 species. Further taxonomic studies on macroalgae from the
Arabian Sea will result in more new records, especially as complex species groups (e.g.
Laurencia), epiphytes and crustose algae have largely been omitted or lumped into groups in
the pilot studies.
Taxonomy and biogeography at species level
The species records form the basic input data for the analyses, hence the taxonomic studies
on Arabian Sea algae in the first chapters (2-5). Chapters 2 and 3 report on the gelatinous red
algae belonging to the Dumontiaceae, Nemastomataceae, Schizymeniaceae and
Naccariaceae. In addition to the morphological and anatomical observations, the study of
reproductive structures and post-fertilization events in these algae show their importance for
reliable species identifications. Based on these detailed examinations, Platoma
heteromorphum and Reticulocaulis obpyriformis are newly described species from Masirah
Island and the Socotra Archipelago, respectively. Many gametophytes of the gelatinous reds
are seasonally present, reflecting cyclic changes in environmental conditions resulting from
physical phenomena (e.g. upwelling) or other temporal variables (e.g. day length). The study
of the Dumontiaceae, Nemastomataceae and Schizymeniaceae of the Arabian Sea (chapter
2) and their occurrence throughout the Indo-Pacific, shows that their distribution is at present
insufficiently known. Unpublished data of Indian Ocean records (Ghent University
Herbarium) indicate that these species are more wide-spread and cover a larger area than
currently known, making them useless in traditional biogeographic analyses based on species

132 Chapter 8
distributions. In contrast, both Reticulocaulis species (chapter 3) show links with distant
regions, where their absence in the intervening areas is unlikely to be a result from of
undersampling. The Naccariaceae is a small family with a specific life cycle and particular
reproductive traits. No representatives of this family have been recorded for the Indian
Ocean, apart from an unpublished collection of Naccaria naccarioides from Western
Australia (G.T. Kraft & G.W. Saunders pers. comm.). The studied gelatinous red algae thus
show contrasting geographic distributions within the Indo-Pacific: disjunct (Naccariaceae)
versus continuous (Dumontiaceae, Nemastomataceae and Schizymeniaceae). These algae
can therefore be useful in investigating specific biogeographic questions using a combined
molecular and anatomical approach. The degree of genetic divergence of ubiquitous species
(e.g. Predaea weldii) could serve as a measure of biogeographic relatedness throughout the
whole Indo-Pacific. The families Nemastomataceae and Schizymeniaceae have recently been
separated based on distinct post-fertilization events. Additional molecular studies on other
genera of these families could shed light on the phylogeny. Moreover, the validity of today’s
morphospecies could be verified by genetic analyses e.g. species diversity within the
enigmatic genus Titanophora, as representatives of these families have been
underrepresented in molecular studies. In order to establish the importance of vicariance
events versus the long-distance dispersal of disjunctly distributed Arabian Sea taxa,
molecular analyses of the two Reticulocaulis species from Arabia and R. mucosissimus from
Hawaii could illustrate such phylogeographic relationships. Additional sequencing of the two
other Naccariaceae genera, Naccaria and Atractophora, and the presumably related genus
Liagorothamnion would clarify the ordinal classification of these genera and the suggested
subdivision into different families (see chapter 3). In conclusion, a holistic approach of
molecular, biogeographic and anatomic studies on these gelatinous red algae could lead to a
sound species concept based on various biological aspects. Ideally, such a baseline study on
Arabian Sea taxa could serve as a model within the above red algal families.
Chapter 4 discusses a new species, Chamaebotrys erectus, from the Socotra Archipelago
belonging to the Rhodymeniales. Chamaebotrys has recently been erected by Huisman
(1996) based on characters of reproductive structures, viz. terminal tetrasporangia in
nemathecial sori. The remarkable features that readily discern C. erectus from both other
Chamaebotrys species are its large, upright thallus and the in situ (remaining fixed on the
tetrasporophyte) germination of the tetraspores into gametophytes. In addition to the
compound thalli with tetrasporic and cystocarpic parts, free-living gametophytes also occur.
The unusually large size, with respect to both other representatives of the genus, is most
probably linked to the upwelling of cold and nutrient-rich water, as the species was only
collected from Socotra’s south coast. Champia gigantea, another Rhodymeniales species, is
similarly endemic to the Arabian Sea and characterized by an exceptionally large thallus.
The description of C. erectus includes the first observation of a carpogonial branch within
the genus, supporting its affinity with Coelarthrum and its classification within the
Rhodymeniaceae.
The last taxonomic chapter (5) focuses on Izziella orientalis. The species is widely
distributed throughout the (sub)tropical Indo-Pacific. The reassessment of the genus Izziella
is based on Liagora orientalis. Abbott (1990) treated Izziella abbottiae, a species dedicated
to her, as a synonym of L. orientalis. While analyzing the Liagoraceae (Nemaliales), the
combined observations of the carpogonial branch, the cystocarp and the large subtending
stalk (fused cells) clearly discerned L. orientalis from other Liagoraceae genera, justifying
the reinstatement of Izziella. Upon the resurrection of Ganonema (Huisman & Kraft 1994),

Synthesis and perspectives 133
the reinstatement of the genus Izziella forms a second step in subdividing Liagora into
several genera as the genus currently accommodates numerous taxa with a wide variety in
morphology and cystocarp types (Kraft 1989; Huisman & Kraft 1994).
These taxonomic studies on Rhodophyceae of the Arabian Sea support previous anecdotal
observations (Børgesen 1934; Wynne 2000) on the biogeographic affinities with distant
areas (Australia, Hawaii, Japan, South Africa). The study on the macroalgae of the Socotra
Archipelago considerably broadens the area for which these disjunctly distributed species
were reported. Personal observations (T. Schils) during the course of this study supplement
these findings, e.g. the Delesseriaceae. The provisional count totals 15 Delesseriaceae
species for Yemen and Oman, which form a sympatric flora composed of typical East
African algae (Duckerella ferlusii); certain South-East Asian and Pacific algae (Zellera
tawallina); and general Indo-Pacific algae, including some rarely recorded Indian Ocean
species (Chauviniella coriifolia and C. jadinii). Similar to Chamaebotrys erectus,
exeptionally large endemic Delesseriaceae, Cryptopleura robusta M.J. Wynne and
Pseudogrinnellia barrattiae M.J. Wynne, have been described for Oman (Wynne 1999a, b).
The diverse distribution patterns of the Delesseriaceae flora, and their generally striking,
“pretty” appearance (easily observed in the field), make them good subjects for establishing
complete species lists for this group and thus improving biogeographic analyses within the
Indo-Pacific. Sympodothamnion, another remarkable genus of the Ceramiales, has been
collected from the Socotra Archipelago. This monospecific genus has only been known from
southern Japan. Besides the biogeographic aspects, the species identity and its familial
classification are of particular research interest. The genus has been classified in the
Dasyaceae (Itono 1977) but the present consensus is in the Ceramiaceae (Athanasiadis 1996;
de Jong et al. 1997). Our observations, however, strongly indicate a classification in the
Rhodomelaceae. Other Rhodomelaceae taxa that are nowadays of biogeographic interest are
the Amansieae (Masuda & Abe 2002; N’Yeurt 2002). Our Arabian Sea collections contain
four species belonging to this tribe. Cornilly (2002) studied these specimens plus an obscure
endemic from Yemen, Amansia arabica J. Agardh ex Newton nom. inval. The observed
phytogeographic separation of Amansia and Melanamansia (Norris 1995) in the Indo-Pacific
(excluding South Africa) cannot be supported for the Arabian Sea. This is consistent with
recent findings of co-occurring Amansia and Melanamansia species in other areas of the
Indo-Pacific (South & Skelton 1999; Masuda et al. 2000). Again, this group contains both
widely distributed species [Amansia rhodantha (Harvey) J. Agardh and Osmundaria melvillii
(J. Agardh) R.E. Norris] and species with disjunct distribution patterns [Neurymenia
nigricans T. Tanaka & Itono: Natal (South Africa), Socotra (Yemen) and southern Japan;
Melanamansia daemelii (Sonder) R.E. Norris: Hawaii, Masirah (Oman), Queensland
(Australia) and Socotra (Yemen)]. The endemic Amansia arabica, again characterized by a
large thallus size, most probably needs to be transferred to the genus Melanamansia. The
above mentioned representatives of the Ceramiales may prove to be useful in DNA marker
and molecular clock analyses in the future, which could reveal an insight in the
phylogeographic patterns (genetic history and gene flow) and important vicariant events
(divergence rates) of Arabian Sea macroalgae. Recent cryptic introductions that could
obscure these patterns are suspected to be minimal as (i) the number of harbours in the
Arabian Sea is limited, (ii) the examined subtidal rhodophytes are unlikely candidates for
anthropogenic dispersal and (iii) the latter are rather ineffective in subsequent settling. The
first molecular clock (Zuccarello & West 2002) and phylogeographic studies (Zuccarello et
al. 2002) on Ceramiales have already revealed interesting and unexpected results.

134 Chapter 8
Ecology and biogeography at community level
The analysis of the subtidal relevé data from the Socotra Archipelago identified distinct plant
communities corresponding to their geographic location within the archipelago (chapter 6).
In contrast to the particular distribution pattern of a specific taxon (see Biogeography at
species level), we here analyse the biogeographic affinity of all the species in a community.
The two contrasting algal communities of the main island are those of the upwelling affected
south coast and the upwelling protected north coast. Both communities comprise well-
developed macroalgal stands (no significant difference in species richness, biomass and
alpha diversity of the quadrats), but differ substantially in species composition (beta diversity
indices). The biogeographic affinities, expressed by the Simpson coefficient, of both
communities also vary (chapter 6). Socotra’s south coast shows a lower general affinity with
the Indian Ocean flora than the north coast. In general, the biogeographic affinities of the
Socotran communities within the Indian Ocean increase from a minimum in southern Africa
to a maximum along the tropical East African coast of Kenya and Tanzania. The affinities
then decrease within the Arabian Sea towards a low in Iran and Pakistan (a result of
undersampling). Thereafter the affinities within the eastern Indian Ocean remain rather
constant and low. Besides the north and south coast, four additional plant communities were
identified. The eastern tip of Socotra Island harbours a community with elements of both
previous entities, however, with a markedly higher affinity for the south coast flora. The
mixed community of this transition zone includes the most species-rich and most diverse
quadrats of the archipelago, largely attributable to the particular red algal flora. The intense
and complex current patterns, regulating temperature and supplying a constant nutrient flow,
around the eastern tip are suspected to be beneficial for algal growth. The biogeographic
affinities of the transition zone are intermediate between those of the north and the south
coast. The algal assemblages of the outer islands are subject to large fluctuations in
phosphate concentration and temperature, resulting from the limited coastal area and the
drastic changes in the surrounding current patterns. The species composition of this
community is most similar to that of Socotra’s south coast and its biogeographic affinities
run parallel to those of different communities for each of the three main Indian Ocean
regions (East African coast, Arabian Sea and eastern Indian Ocean). The remaining two
communities, the seagrass beds of Qalansiyah Lagoon and the coral dominated communities
of the north coast, differ substantially in species richness, diversity and biomass from the
previous communities. The species composition of these plant communities, however,
demonstrates links with the north coast. Both communities are regarded as sub-entities of the
north coast, being habitats that are governed by peculiar environmental conditions (e.g. high
salinities, high temperature and substantial sand cover) and biotic competition (especially
with corals). This results in an impoverished floristic species richness and a low floristic
diversity. The biomass stands (fresh weight per vegetation quadrat) of these two sub-entities
vary from the lowest (coral dominated communities) to the highest (seagrass beds) observed
values of the archipelago. From a phycological point of view, Socotra’s south coast, the
transition zone and the outer islands are the areas with a unique subtidal flora within the
Indian Ocean, which are characterized by high species-richnesses and high diversity values.
The development of these communities is closely linked with the phenomenon of coastal
upwelling, shaping the unique Arabian Sea biocoenoses. Zoning and development plans of
the Socotra Archipelago should designate part of these exclusive marine communities as
conservation and monitoring areas. Socotra’s north coast, including the coral dominated
communities and the seagrass beds, is composed of common Indian Ocean macroalgae, but

Synthesis and perspectives 135
conversely it comprises unique faunistic communities for the Indian Ocean and regionally
important nursing grounds. The marine organisms that show a high degree of endemism and
allopatry are essentially different for the contrasting coasts. The faunistic composition of the
northern communities is unique for the region, while the southern communities are
characterized by a particular flora. The phenomenon of upwelling in this northern part of the
Indian Ocean is the dispersal barrier for the warm- (northern coasts) as well as the cold-water
biota (southern coasts).
Fig. 1. Principal Component Analysis of the Indian Ocean distribution of the macroalgal species in the
site inventories. The Indian Ocean distribution for each species of a particular site is documented, after
which the species records per country are counted for each site. The species lists of the different sites are
then treated as the sample input and the Indian Ocean nations are used as the species input. The included
nations are: South Africa (SAf), Mozambique (Moz), Madagascar (Mad), Réunion (Réu), Mauritius (Mau),
Rodrigues (Rod), Tanzania (Tan), Seychelles (Sey), Kenya (Ken), Somalia (Som), Iran (Ira), Pakistan (Pak),
Laccadive islands (Lac), Maldives (Mald), Sri Lanka (Sri), Bangladesh (Ban), Andaman islands (And),
Malaysia (Mala), Indonesia (Ind), Western Australia (Aus). Three site groupings have been discerned: the
clusters A, B and C. The eigenvalues of the first two axes are 0.827 and 0.042, respectively.
In a second ecological approach (chapter 7), the subtidal plant assemblages of the Socotra
Archipelago and Masirah Island are analyzed by means of complete species inventories for
the different sample sites. The resulting ordinations from species lists have a somewhat
lower resolution than those from quadrat data for Socotra, i.e. certain communities
(transition zone and outer islands) are grouped into larger ones (Socotra’s north and south
coast). The ordination reveals six communities. Similar communities of Socotra and Masirah
are grouped into larger entities (four biotopes) based on the ordination results, the tripartite
similarity index and the congruous biogeographic affinities within the Indian Ocean
(founded on specific as well as generic records). The environmental conditions and the
indicator species that characterize these communities and biotopes are discussed. The
combined interpretation of the ordination including environmental parameters (especially
chlorophyll a) and the biogeographic analyses show a stronger effect of upwelling for
Masirah, resulting in macroalgal communities that are more divergent from the East African
flora in comparison to those of Socotra. All investigated communities, however, have a
strong phytogeographic affinity with the East African coast. A synopsis is represented in the
Principal Component Analysis (hereafter PCA) of the macroalgal distributions (Indian
Ocean nations) from the species inventories of the Socotra and Masirah sites (Fig. 1). The
very high eigenvalue of the first axis (0.827) shows that the separation of countries according
to this axis is by far the most important component of the analysis. The species inventories of
Masirah and Socotra (dots in Fig. 1) have high affinities with the (sub)tropical countries of

136 Chapter 8
East Africa, Western Australia, Sri Lanka and the east coast of South Africa. The
biogeographic affinities with other countries and islands of the eastern and central part of the
Indian Ocean are markedly lower. The PCA shows three distinct site groupings (Fig. 1).
Cluster A includes sites with a high biogeographic affinity for East Africa, which belong to
the following communities (for abbreviations see chapter 7): MAS WC, S&O NC, SOC NC
and SOC SG. Cluster B groups sheltered sites, also harbouring communities (part of MAS
SG and S&O SC) with high affinities for the East African flora. Cluster C (MAS EC and
S&O SC) is separated from clusters A and B by the second axis. The low eigenvalue of this
axis, adding only 4.2 % of the variation in species composition, indicates that, besides the
high East African affinity, a limited number of its species have marked affinities with local
(e.g. Pakistan and Somalia) and distant (e.g. South Africa and Western Australia) cold-
temperate floras.
Sheppard et al. (1992) suspected that most of the biotic distributions in the Arabian Seas
(comprising the Red Sea, Gulf of Aden, Arabian Sea, Gulf of Oman and Persian Gulf) are no
more than chance distributions and that the area as a whole constitutes a single
biogeographic sub-region. Besides the odd exception (e.g. high local endemism of
butterflyfish), Sheppard et al. (1992) believe that biogeographic patterns result from
insufficient time for complete dispersal after the start of the Holocene and inadequate
“mixing” of fauna throughout the various suitable habitats in the Indian Ocean. These
authors remarked that a designation on a smaller biogeographic scale might be possible for
some fish, yet for other groups, notably the plants, there is no justification for any sub-
provincial division. Various analysis techniques (chapters 6, 7), however, detect distinct
subtidal plant communities and biotopes according to differences in the governing
environmental parameters. Of these, the upwelling affected plant communities typify a
peculiar Arabian Sea flora. Certain species of these communities show disjunct distribution
patterns throughout the Indo-Pacific and are also suspected to be of biogeographic
importance within the larger Arabian region. Combined with the discovery of an increasing
number of endemic algae, this leaves us to conclude that the Arabian Sea constitutes a
phytogeographic (sub)province within the Indo-Pacific and the larger Arabian region.
Prospective fieldwork in the northern Arabian Sea (Al Qad, Oman) would extend the
investigated area considerably, being excellent to test biogeographic (dis)continuities
towards the border of the Arabian Sea and the Gulf of Oman. Questions of interest include:
(i) the degree of divergence from the East African flora, (ii) the impact of upwelling on these
communities, (iii) the use of this location in a geographic gradient, from the Arabian Sea
over the Gulf of Oman towards the Persian Gulf, in order to test the macroalgal turnover
according to the decrease in substratum availability (sedimentary coasts as a biogeographic
barrier). Recently, the first temperature loggers have been installed at Masirah Island
(Wilson 1999) in an attempt to achieve accurate coastal data on a detailed temporal and
spatial scale. These precise coastal data are needed for understanding the relationship
between the environmental conditions and the biotic interactions (e.g. competition between
algae and corals).
Seasonality
Nizamuddinia zanardinii is a large, endemic fucoid of the upwelling regions within the
Arabian Sea. In reporting N. zanardinii for the Socotra Archipelago, Kemp (1998) noticed
differences in seasonal growth between the Socotran populations and those of the southern

Synthesis and perspectives 137
Arabian shores. Two explanatory hypotheses were proposed: (i) a temporal shift of up to six
months in the growth cycle of N. zanardinii for Socotra in comparison to the mainland
populations, or (ii) two (re)productive peaks of this alga at Socotra, whereas one for the
southern Arabian plants. Although initially planned, due to practical complications (see
chapter 1), extended observations on macroalgal seasonality were not feasible during the
course of this study. The observations during the three field trips, however, can shed some
light on the seasonal growth of this keystone species. The temporal co-occurrence
(November 1999) of mature, fertile N. zanardinii specimens in intertidal rock pools at
Masirah and the undeveloped small rosettes at Barr al-Hikman, seem to indicate that periods
of reproductivity and growth can fluctuate within a specific geographic area dependent on its
habitat and/or zonation of occurrence. Similar differences were observed for the Socotra
Archipelago: whereas Kemp (1998) reports on reproductive spikes in February-March 1996
and Leliaert (2000) collected fertile axes in January-February 1999, only small plants were
noticed during the field trip in March-May 2000. This suggests the existence of two
reproductive periods (cf. Hadramout coast of Yemen, Ormond & Banaimoon 1994) related
to both upwelling periods, with temporal (annual) and local fluctuations. In addition, it is
suspected that the (re)productive response of the Nizamuddinia populations from Yemen and
Oman is greater during the southwest monsoon as opposed to the northeast monsoon.
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Abbott I.A. 1990. A taxonomic assessment of the species of Liagora (Nemaliales, Rhodophyta)
recognized by J. Agardh, based upon studies of type specimens. Cryptog. Bot. 1: 308-322.
Athanasiadis A. 1996. Morphology and classification of the Ceramioideae (Rhodophyta) based on
phylogenetic principles. Opera Bot. 128: 1-216.
Børgesen F. 1934. Some marine algae from the northern part of the Arabian Sea with remarks on their
geographical distribution. Kongel. Danske Vidensk. Selsk. Biol. Meddel. 11: 1-72.
Cornilly W. 2002. Taxonomie en biogeografie van de Amansieae (Rhodophyta, Rhodomelaceae) in de
Arabische Zee. Licentiate thesis, Ghent University. 122 pp.
de Jong Y.S.D.M., Prud’homme van Reine W.F. & Lokhorst G.M. 1997. Studies on Dasyaceae. II. A
revision of the genera Eupogodon and Dipterocladia gen. nov. (Ceramiales, Rhodophyta). Bot.
Mar. 40: 421-450.
Huisman J.M. 1996. The red algal genus Coelarthrum Børgesen (Rhodymeniaceae, Rhodymeniales)
in Australian seas, including the description of Chamaebotrys gen. nov. Phycologia 35: 95-112.
Huisman J.M. & Kraft G.T. 1994. Studies of the Liagoraceae (Rhodophyta) of Western Australia:
Gloiotrichus fractalis gen. et sp. nov. and Ganonema helminthaxis sp. nov. Eur. J. Phycol. 29:
73-85.
Itono H. 1977. Studies on the Ceramiaceous algae (Rhodophyta). Biblioth. Phycol. 35: 1-499.
Kemp J.M. 1998. The occurence of Nizamuddinia zanardinii (Schiffner) P.C. Silva (Phaeophyta:
Fucales) at the Socotra Archipelago. Bot. Mar. 41: 345-348.
Kraft G.T. 1989. Cylindraxis rotundatus gen. et sp. nov. and its generic relationship within the
Liagoraceae (Nemaliales, Rhodophyta). Phycologia 28: 275-304.
Leliaert, F. 2000. Marine benthic macroalgae and seagrasses of the Socotra Archipelago. In:
Conservation and sustainable use of biodiversity of Socotra Archipelago. Marine habitat,
biodiversity and fisheries surveys and management. Progress report of phase III (Ed. by Apel M.
& Hariri K.I.), pp. 13-48. Senckenberg Research Institute, Frankfurt a.M., Germany.

138 Chapter 8
Masuda M. & Abe T. 2002. Two similar red algal species, Melanamansia glomerata and Amansia
rhodantha (Rhodomelaceae, Ceramiales), from the north-western Pacific Ocean. Cryptog. Algol.
23: 107-121.
Masuda M., Kato A., Shimada S., Kawaguchi S. & Phang S.M. 2000. Taxonomic notes on marine
algae from Malaysia. II. Seven species of Rhodophyceae. Bot. Mar. 43: 181-190.
Norris R.E. 1995. Melanamansia glomerata, comb. nov., and Amansia rhodantha, two hitherto
confused species of Indo-Pacific Rhodophyceae. Taxon 44: 65-68.
N’Yeurt A.D.R. 2002. A revision of Amansia glomerata C. Agardh, Amansia rhodantha (Harvey) J.
Agardh and Melanamansia glomerata (C. Agardh) R.E. Norris (Rhodophyta: Rhodomelaceae).
Bot. Mar. 45: 231-242.
Ormond R.F.G. & Banaimoon S.A. 1994. Ecology of intertidal macroalgal assemblages on the
Hadramout coast of southern Yemen, an area of seasonal upwelling. Mar. Ecol. Progr. Ser. 105:
105-120.
Sheppard C.R.C., Price A.R.G. & Roberts C.A. 1992. Marine ecology of the Arabian region.
Academic Press Ltd, London. 359 pp.
South G.R. & Skelton P.A. 1999. Amansia paloloensis sp. nov. (Rhodomelaceae, Rhodophyta) from
Samoa, South Pacific. Phycologia 38: 245-250.
Wilson S. 1999. Corals. In: Preliminary Report Scientific Mission Oman 99, Sultanate of Oman,
November - December 1999 (Ed. by Planes S. & Galzin R.), pp. 28-29, 76-77. Ardoukoba, Paris.
Wynne M.J. 1999a. Pseudogrinnellia barratiae gen. et sp. nov., a new member of the red algal family
Delesseriaceae from the Sultanate of Oman. Bot. Mar. 42: 37-42.
Wynne M.J. 1999b. New records of benthic marine algae from the Sultanate of Oman. Contr. Univ.
Michigan Herb. 22: 189-208.
Wynne M.J. 2000. Further connections between the benthic marine algal floras of the northern
Arabian Sea and Japan. Phycol. Res. 48: 211-220.
Zuccarello G.C. & West J.A. 2002. Phylogeography of the Bostrychia calliptera-B. pinnata complex
(Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid
DNA markers. Phycologia 41: 49-60.
Zuccarello G.C., Sandercock B. & West J.A. 2002. Diversity within red algal species: variation in
world-wide samples of Spyridia filamentosa (Ceramiaceae) and Murrayella periclados
(Rhodomelaceae) using DNA markers and breeding studies. Eur. J. Phycol. 37: 403-417.

Synthese en perspectieven 139
HOOFDSTUK 9
S
YNTHESE EN PERSPECTIEVEN
In deze studie worden de mariene plantengemeenschappen, voornamelijk bestaande uit
macrowieren, van de Arabische Zee onderzocht. De Arabische Zee is gelegen in het
noordelijk deel van de Indische Oceaan en grenst in het westen aan de Golf van Aden en het
Afrikaans continent, en in het oosten aan de Golf van Oman en het Indisch subcontinent. De
ecologie en de oceanografie van de Arabische Zee worden bepaald door de seizoenale
moessonwinden, die in bepaalde gebieden kustgebonden opwelling induceren. De mariene
levensgemeenschappen van deze opwellingskusten zijn relatief weinig bestudeerd en blijken
binnen de Indische Oceaan een aparte eenheid te vormen. De Socotra Archipel (Jemen) en
het eiland Masirah (Oman) bevinden zich in twee geografisch gescheiden opwellings-
gebieden van de Arabische zee en bevatten beide een grote diversiteit aan habitats op een
beperkte oppervlakte. De uniciteit van de plantengemeenschappen van deze eilanden komt
tot uiting in hun floristische, biogeogeografische en ecologische aspecten. In deze studie
worden de taxonomische onderwerpen eerst behandeld, gevolgd door de gemeenschaps-
analysen.
Soortenlijsten
De soortenlijsten van de Arabische Zee die in de ecologische analysen gebruikt werden
bevatten verschillende nieuwe soortswaarnemingen voor de regio. Het aantal nieuwe
waarnemingen voor de onderzochte gebieden worden hier achtereenvolgens vernoemd, het
eerste cijfer vertegenwoordigt het aantal mariene planten die tot op de soort gedetermineerd
zijn en het tweede cijfer deze tot op genusniveau (de eerste waarnemingen van deze genera,
of soorten verschillend van de tot op heden vermelde taxa): het eiland Masirah, 90 en 19
soorten; Oman, 48 en 12 soorten; de Socotra Archipel, 130 en 28 soorten; Jemen, 92 en 20
soorten. Toekomstige taxonomische studies naar macrowieren van de Arabische Zee zullen
ongetwijfeld in nieuwe soortswaarnemingen resulteren, zeker wanneer deze zich toeleggen
op complexe soortengroepen (b.v. Laurencia), epifyten en korstvormende wieren, die
grotendeels verzuimd werden in deze eerste studies.
Taxonomie en biogeografie op soortsniveau
De soortswaarnemingen vormen steeds de basisgegevens van de uitgevoerde analysen,
bijgevolg werden de taxonomische studies naar de wieren van de Arabische Zee in de eerste
hoofdstukken besproken (2-5). De hoofdstukken 2 en 3 rapporteren over de gelatineuze
roodwieren van de families Dumontiaceae, Nemastomataceae, Schizymeniaceae en
Naccariaceae. Naast de morfologische en anatomische waarnemingen, is de studie van de
reproductieve kenmerken en de post-fertilisatiegebeurtenissen van belang met betrekking tot
betrouwbare soortsidentificaties van deze wieren. Op grond van dit gedetailleerd onderzoek,
werden de soorten Platoma heteromorphum en Reticulocaulis obpyriformis nieuw
beschreven van respectievelijk het eiland Masirah en de Socotra Archipel. Veel gametofyten
van de gelatineuze roodwieren zijn slechts seizoenaal aanwezig, wat de cyclische
veranderingen in de milieuomstandigheden ten gevolge van fysische fenomenen (b.v.
opwelling) en andere temporele variabelen (b.v. daglengte) weergeeft. De studie van de

140 Hoofdstuk 9
Dumontiaceae, Nemastomataceae en Schizymeniaceae van de Arabische Zee (hoofdstuk 2)
en hun voorkomen over het Indo-Pacifisch gebied, toont dat de verspreiding momenteel
onvoldoende gekend is. Ongepubliceerde gegevens van Indische Oceaanwaarnemingen
(Herbarium Universiteit Gent) geven aan dat deze gelatineuze roodwieren meer algemeen
verspreid voorkomen en een groter gebied beslaan dan tot op heden werd aangenomen.
Bijgevolg zijn deze soorten onbruikbaar voor traditionele biogeografische analysen
gebaseerd op soortsverspreidingen. Het omgekeerde geldt voor beide Reticulocaulis-soorten
(hoofdstuk 3) die een verband vertonen met ver verwijderde gebieden en waarvan de
afwezigheid in de tussenliggende gebieden waarschijnlijk niet toe te schrijven is aan een
gebrek aan bemonsteringen. De Naccariaceae is immers een kleine familie die
gekarakteriseerd wordt door een specifieke levenscyclus en typerende reproductieve
kenmerken. Buiten de ongepubliceerde waarneming van Naccaria naccarioides voor West-
Australië (G.T. Kraft & G.W. Saunders pers. med.), is er voordien geen enkele Naccariaceae
vermeld voor de Indische Oceaan. De bestudeerde gelatineuze roodwieren hebben dus
contrasterende geografische verspreidingen in de Indo-Pacific: hetzij dispers (Naccariaceae),
hetzij ononderbroken (Dumontiaceae, Nemastomataceae en Schizymeniaceae). Daarom
kunnen zij een uitgelezen groep zijn om biogeografische vragen te beantwoorden vanuit een
gecombineerde moleculair-anatomische invalshoek. De graad van genetische divergentie
tussen specimens van wijdverspreide soorten (b.v. Predaea weldii) uit verschillende
gebieden van de Indo-Pacific kan gebruikt worden om de biogeografische verbanden te
kwantificeren. De families Nemastomataceae en Schizymeniaceae werden recent gescheiden
op basis van verschillen in post-fertilisatiegebeurtenissen. Bijkomende moleculaire studies
naar andere genera van deze families kunnen een inzicht bieden in hun fylogenie.
Aanvullend hierbij kan de status van de huidige morfologisch gedefinieerde soorten
geëvalueerd worden aan de hand van hun genetische informatie (b.v. de opheldering van de
soortendiversiteit binnen enigmatische genera zoals Titanophora), aangezien
vertegenwoordigers van deze families tot op heden ontoereikend geïncludeerd werden in
moleculaire studies. Om het belang van vicariantiegebeurtenissen ten opzichte van de
mogelijkheden tot lange-afstandsverbreiding voor disjuncte Arabische Zee taxa vast te
stellen, kan de moleculaire analyse van de twee Reticulocaulis soorten uit Arabië en R.
mucosissimus uit Hawaï zulke onderliggende fylogeografieën ophelderen. Aanvullende
sequenties van de twee andere Naccariaceae genera, Naccaria en Atractophora, en het
waarschijnlijk verwante genus Liagorothamnion kunnen nieuwe argumenten bieden voor
hun plaatsing op ordeniveau en hun onderverdeling in de verschillende families (zie
hoofdstuk 3). Besluitend kunnen we stellen dat een holistische benadering van moleculaire,
biogeografische en anatomische studies naar deze gelatineuze roodwieren een eenduidig
soortsconcept kan opleveren. Idealiter zullen de onderzochte Arabische Zee taxa dan als een
model voor deze roodwierfamilies kunnen fungeren.
In hoofdstuk 4 wordt een nieuwe Rhodymeniales soort, Chamaebotrys erectus, afkomstig
van de Socotra Archipel beschreven. Chamaebotrys werd recent beschreven door Huisman
(1996) op basis van reproductieve kenmerken, namelijk de terminale tetrasporocysten in
nemathecium sori. De opmerkelijke eigenschappen die C. erectus onderscheiden van beide
andere Chamaebotrys-soorten zijn de grote, rechtopstaande thallus en de in situ (vastgehecht
aan de tetrasporofyt) kieming van de tetrasporen tot gametofyten. Naast de samengestelde
tetrasporofyt- en carposporofytthallus, zijn er ook vrijlevende gametofyten aangetroffen. De
uitzonderlijke grootte, in vergelijking met de andere vertegenwoordigers van het genus, staat
waarschijnlijk in verband met de opwelling van koud, nutriëntenrijk water aangezien de

Synthese en perspectieven 141
soort enkel ter hoogte van de zuidkust van Socotra ingezameld werd. Champia gigantea is
een gelijkaardige Rhodymenialessoort: een endeem van de Arabische Zee, gekenmerkt door
een opmerkelijk grote thallus. In de bespreking van C. erectus wordt de eerst geobserveerde
carpogoniumtak van het genus beschreven. Deze ondersteunt de nauwe verwantschap met
Coelarthrum en de plaatsing van het genus in de Rhodymeniaceae.
Het laatste taxonomisch deel (hoofdstuk 5) behandelt het wier Izziella orientalis, een
wijdverspreide soort in de (sub)tropische Indo-Pacific. De revalorisatie van het genus Izziella
is gebaseerd op Liagora orientalis. Abbott (1990) beschouwde de aan haar opgedragen soort,
Izziella abbottiae, als synoniem van L. orientalis. Tijdens het screenen van de Liagoraceae
(Nemaliales) van de Arabische Zee kon L. orientalis duidelijk onderscheiden worden van
andere Liagoraceae genera. Dit gebeurde op basis van de gecombineerde kenmerken van de
carpogoniumtak, het cystocarp en het grote ondersteunend complex van versmolten cellen,
wat de heroprichting van het genus Izziella verantwoordde. In navolging van de beschrijving
van Ganonema (Huisman & Kraft 1994), vormt de heroprichting van het genus Izziella een
tweede stap in het opsplitsen van het genus Liagora in meerdere genera. Dit lijkt ook logisch
omdat het genus momenteel vele taxa omvat met een grote verscheidenheid in morfologie en
cystocarptypes (Kraft 1989; Huisman & Kraft 1994).
Deze taxonomische studies naar de Rhodophyceae van de Arabische Zee onderschrijven
vroegere anecdotische waarnemingen (Børgesen 1934; Wynne 2000) van de biogeografische
affiniteit met ver afgelegen gebieden (Australië, Hawaï, Japan, Zuid-Afrika). De studie naar
de macrowieren van de Socotra Archipel vergroot het verspreidingsgebied van deze disjunct
verspreide soorten aanzienlijk. Persoonlijke waarnemingen (T. Schils) in de loop van deze
studie bevestigen deze bevindingen. De Delesseriaceae van het bestudeerde gebied vormen
hier een goed voorbeeld van. Het voorlopige aantal soorten Delesseriaceae voor Jemen en
Oman bedraagt 15. Deze vormen een sympatrische flora bestaande uit typisch Oost-
Afrikaanse wieren (Duckerella ferlusii); bepaalde Zuidoost-Aziatische en Pacifische wieren
(Zellera tawallina); en algemene Indo-Pacifische wieren, inclusief enkele zeldzame Indische
Oceaansoorten (Chauviniella coriifolia en C. jadinii). Gelijkaardig aan Chamaebotrys
erectus zijn er uitzonderlijk grote Delesseriaceae endemen, Cryptopleura robusta M.J.
Wynne en Pseudogrinnellia barrattiae M.J. Wynne, beschreven voor Oman (Wynne 1999a,
b). De gemengde verspreidingspatronen van de Delesseriaceae flora en hun opvallend fraai
uitzicht (gemakkelijk waar te nemen op het terrein) maken deze wieren uitgelezen
studieobjecten om volledige soortenlijsten van deze groep op te stellen en aan de hand
hiervan nauwkeurige biogeografische analysen uit te voeren. Sympodothamnion is een ander
opmerkelijk genus van de Ceramiales dat ingezameld werd rond de Socotra Archipel. Dit
monospecifieke genus was enkel gekend voor zuidelijk Japan. Naast de biogeografische
aspecten, zijn de soortsidentiteit en de plaatsing op familieniveau boeiend. Het genus werd
oorspronkelijk ondergebracht in de Dasyaceae (Itono 1977) maar de huidige consensus is dat
het tot de Ceramiaceae behoort (Athanasiadis 1996; de Jong et al. 1997). De observaties van
de Socotra specimens duiden evenwel op een plaatsing in de Rhodomelaceae. Andere
Rhodomelaceae taxa die actueel van biogeografisch belang zijn behoren tot de Amansieae
(Masuda & Abe 2002; N’Yeurt 2002). Onze inzamelingen includeren vier soorten van deze
tribus. Cornilly (2002) bestudeerde deze specimens, aangevuld met een obscure endeem van
Jemen, Amansia arabica J. Agardh ex Newton nom. inval. De veronderstelde
fytogeografische scheiding van Amansia- en Melanamansia-soorten (Norris 1995) in de
Indo-Pacific (uitgezonderd Zuid-Afrika) is niet van toepassing in de Arabische Zee. Dit
stemt overeen met recente waarnemingen van hun gemeenschappelijk voorkomen in andere

142 Hoofdstuk 9
gebieden van de Indo-Pacific (South & Skelton 1999; Masuda et al. 2000). Ook deze
wiergroep omvat zowel algemene soorten [Amansia rhodantha en Osmundaria melvillii (J.
Agardh) R.E. Norris] als disjunct verspreide soorten [Neurymenia nigricans T. Tanaka &
Itono: Natal (Zuid-Afrika), Socotra (Jemen) en zuidelijk Japan; Melanamansia daemelii
(Sonder) R.E. Norris: Hawaï, Masirah (Oman), Queensland (Australië) en Socotra (Jemen)].
De endeem Amansia arabica, eveneens gekenmerkt door grote afmetingen, zal
hoogstwaarschijnlijk in het genus Melanamansia geplaatst moeten worden. In de toekomst
kunnen de hierboven besproken vertegenwoordigers van de Ceramiales belangrijk blijken in
studies met DNA merkers en moleculaire kloktoepassingen. Die zouden een inzicht kunnen
bieden in de fylogeografische patronen (genetische voorgeschiedenis en genenuitwisseling)
en de belangrijke vicariantiegebeurtenissen (divergentiesnelheden) van de macrowieren in de
Arabische Zee. Recente cryptische introducties, die deze patronen kunnen vervagen, worden
verondersteld van minimaal belang te zijn aangezien (i) het aantal havens in de Arabische
Zee beperkt is, (ii) de onderzochte subtidale roodwieren minder geschikt zijn voor
antropogene verspreiding en (iii) ze minder succesvol zijn in de daaropvolgende vestiging.
De eerste moleculaire klok (Zuccarello & West 2002) en fylogeografische studies
(Zuccarello et al. 2002) naar de Ceramiales leverden reeds interessante en onverwachte
resultaten op.
Ecologie en biogeografie op gemeenschapsniveau
De analyse van de infralitorale opnamegegevens van de Socotra Archipel resulteerde in
duidelijk verschillende plantengemeenschappen, overeenstemmend met hun geografische
positie in de archipel (hoofdstuk 6). In tegenstelling tot het focussen op bepaalde taxa met
een bijzonder verspreidingspatroon (zie Biogeografie op soortsniveau), wordt hier de
biogeografische affiniteit van alle samenstellende soorten van een gemeenschap nagegaan.
De twee contrasterende wiergemeenschappen van het hoofdeiland zijn deze van de noord- en
de zuidkust. Het zijn beide goed ontwikkelde wiergemeenschappen (geen significant verschil
in soortenrijkdom, biomassa en alfa-diversiteit van de kwadraten) die evenwel verschillen in
hun soortensamenstelling (beta-diversiteitsindices). De biogeografische affiniteiten,
weergegeven door de Simpson coëfficiënt, van beide gemeenschappen zijn ook anders
(hoofdstuk 6). De zuidkust van Socotra vertoont een lagere algemene affiniteit met de
Indische Oceaanflora in vergelijking met deze van de noordkust. Algemeen kan gesteld
worden dat de biogeografische affiniteit van de wiergemeenschappen rond Socotra met de
Indische Oceaanflora stijgt van een minimum in zuidelijk Afrika tot een maximum ter
hoogte van de tropische kusten van Kenia en Tanzania. Die affiniteit daalt dan weer ter
hoogte van de Arabische Zee naar een minimum voor Iran en Pakistan (wellicht een artefact
door de schaarse bemonstering). Daarna blijft de affiniteit in de oostelijke Indische Oceaan
tamelijk constant en laag. Naast de noord- en zuidkust, werden vier bijkomende
plantengemeenschappen geïdentificeerd. Het oostelijke uiteinde van het eiland Socotra
herbergt gemeenschappen met elementen van beide voornoemde entiteiten, evenwel met een
merkelijk hogere affiniteit voor de flora van de zuidkust. De gemengde gemeenschap van
deze overgangszone bevat de meest soortenrijke en diverse kwadraten van de archipel,
voornamelijk wegens de bijzondere roodwierflora. De intense en complexe stromings-
patronen rond dit oostelijk uiteinde reguleren de temperatuur en zorgen voor een constante
nutriëntenaanvoer, twee gunstige factoren die wiergroei bevorderen. De biogeografische
affiniteit van de overgangszone is intermediair tussen deze van de noord- en de zuidkust. De
wiervegetaties van de omringende eilandjes zijn onderhevig aan grote fluctuaties in

Synthese en perspectieven 143
fosfaatconcentratie en temperatuur, een gevolg van het beperkte kustgebied en de drastische
veranderingen in de omgevende stromingspatronen. De soortensamenstelling van deze
gemeenschap is het meest gelijkaardig aan dat van Socotra's zuidkust en de biogeografische
affiniteiten zijn gelijkaardig aan die van andere gemeenschappen, maar verschillend voor elk
van de drie hoofdregio's binnen de Indische Oceaan (Oost-Afrikaanse kust, Arabische Zee en
de oostelijke Indische Oceaan). De laatste twee gemeenschappen, de zeegrasvelden van de
Qalansiyah lagune en de koraal-gedomineerde gemeenschap van de noordkust, zijn
essentieel verschillend in soortenrijkdom, diversiteit en biomassa van de vorige vier
gemeenschappen. De soortensamenstelling van deze plantengemeenschappen vertoont echter
wel verbanden met de noordkust. Beide gemeenschappen kunnen beschouwd worden als
sub-entiteiten van de noordkust. Deze habitats worden door uitzonderlijke
milieuomstandigheden beïnvloed (zoals hoog zoutgehalte, hoge temperatuur en
zandbedekking) alsook door biotische competitie (voornamelijk met koralen). Deze
veroorzaken een verarmde floristische soortenrijkdom en een lage floristische diversiteit. De
biomassa's (versgewicht per vegetatieopname) van deze twee sub-entiteiten variëren van de
laagste (koraal-gedomineerde gemeenschap) tot de hoogste waarden (zeegrasvelden) voor de
Socotra Archipel. Vanuit algologisch standpunt zijn Socotra's zuidkust, de overgangszone en
de omringende eilanden, gebieden met een unieke infralitorale flora in de Indische Oceaan.
Zij worden gekenmerkt door een hoge soortenrijkdom en een hoge diversiteit. Het ontstaan
van deze unieke gemeenschappen is nauw verbonden met de invloed van de kustgebonden
opwelling in de Arabische Zee. Het is van cruciaal belang dat toekomstige bestemmings- en
ontwikkelingsplannen voor de Socotra Archipel delen van deze exclusieve mariene
gemeenschappen aanduiden als beschermde gebieden en ze opvolgen in een
monitoringsprogramma. De noordkust van Socotra, inclusief de koraal-gedomineerde
gemeenschappen en de zeegrasvelden, huisvest enerzijds algemene Indische Oceaanwieren,
maar anderzijds ook unieke faunagemeenschappen en gebieden die belangrijk zijn als
kraamkamers van mariene fauna. De groepen van mariene organismen die een hoge graad
van endemisme en allopatrie vertonen zijn essentieel verschillend voor de contrasterende
kustgebieden. De faunistische samenstelling van de noordelijke gemeenschappen is uniek
voor de regio, terwijl de zuidelijke gemeenschappen gekenmerkt worden door een bijzondere
wierflora. Het fenomeen van opwelling is zowel voor de warm- (noordkusten) als
koudwaterbiota (zuidkusten) de verbreidingsbarrière in dit noordelijk deel van de Indische
Oceaan.
In een tweede ecologisch luik (hoofdstuk 7) worden de infralitorale vegetaties van de
Socotra Archipel en het eiland Masirah geanalyseerd aan de hand van volledige
soortenlijsten voor de verschillende bemonsteringsplaatsen. De ordinatieresultaten van de
soortenlijsten hebben een lagere resolutie in vergelijking met deze van de vegetatieopnames
van Socotra. Bepaalde gemeenschappen (overgangszone en omringende eilanden) worden
namelijk niet afzonderlijk geïdentificeerd en zitten vervat in andere gemeenschappen (noord-
en zuidkust van Socotra). De ordinatieverwerking toont zes plantengemeenschappen aan.
Vergelijkbare gemeenschappen van Socotra en Masirah worden gegroepeerd in grotere
eenheden (vier biotopen), gebaseerd op ordinatieresultaten, de driedelige similariteitsindex
en overeenstemmende biogeografische affiniteiten (gebruikmakend van zowel soorts- als
genuswaarnemingen). De milieuomstandigheden en de indicatorsoorten die deze
gemeenschappen en biotopen kenmerken worden besproken. De gecombineerde interpretatie
van de ordinatie met milieuparameters (voornamelijk chlorofyl a) en de biogeografische
analysen wijst er op dat het effect van opwelling groter is voor Masirah. Dit wordt

144 Hoofdstuk 9
weerpiegeld in wiergemeenschappen die meer gedivergeerd zijn van de Oost-Afrikaanse
flora. Alle bestudeerde gemeenschappen vertonen nochtans een uitgesproken
fytogeografische affiniteit met de Oost-Afrikaanse kust. Een overzicht hiervan wordt
gegeven in de Principale Componenten Analyse (hierna PCA) van de wierverspreidings-
patronen (landen van de Indische Oceaan) voor de soortenlijsten van Socotra en Masirah
(Fig. 1). De bijzonder hoge eigenwaarde van de eerste as (0,827) wijst er op dat de scheiding
van landen volgens deze as veruit de belangrijkste component in de analyse is. De
soortenlijsten van Masirah en Socotra (punten in Fig. 1) vertonen een hoge affiniteit met de
(sub)tropische landen van Oost-Afrika, West-Australië, Sri Lanka en de oostkust van Zuid-
Afrika. De biogeografische affiniteit met andere landen en eilanden van het oostelijk en
centrale deel van de Indische Oceaan is merkelijk lager. De PCA geeft drie aparte groepen
van staalnameplaatsen weer (Fig. 1). Cluster A omvat de bemonsteringsplaatsen met een
hoge biogeografische affiniteit voor de Oost-Afrikaanse kust, die behoren tot de volgende
gemeenschappen (afkortingen: zie hoofdstuk 7): MAS WC, S&O NC, SOC NC en SOC SG.
Cluster B groepeert beschutte sites, ook samengesteld uit gemeenschappen (delen van MAS
SG en S&O SC) met een hoge affiniteit voor de Oost-Afrikaanse flora. Cluster C (MAS EC
en S&O SC) wordt gescheiden van de clusters A en B volgens de tweede as. De lage
eigenwaarde van deze as, een bijdrage van slechts 4,2 % aan de totale variatie in de
soortensamenstelling, laat zien dat behalve de sterke gelijkenissen met Oost-Afrika, een
beperkt aantal soorten een speciale affiniteit vertonen met lokale (b.v. Pakistan en Somalië)
en verafgelegen (b.v. West-Australië en Zuid-Afrika) koud-gematigde flora's.
Fig. 1. Principale Componenten Analyse van de wierverspreiding in de Indische Oceaan gebaseerd op de
soortenlijsten van de verschillende staalnameplaatsen. De Indische Oceaanverspreiding van elke soort van
een bepaalde bemonsteringsplaats werd geregistreerd, waarna de soortswaarnemingen per land opgeteld
werden voor elke site. De bemonsteringsplaatsen vormden de “sample input” en de Indische
Oceaanlanden werden gebruikt als de "species input". De geïncludeerde landen zijn: Zuid-Afrika (ZAf),
Mozambique (Moz), Madagaskar (Mad), Réunion (Réu), Mauritius (Mau), Rodrigues (Rod), Tanzania
(Tan), Seychellen (Sey), Kenia (Ken), Somalië (Som), Iran (Ira), Pakistan (Pak), Laccadive eilanden (Lac),
Malediven (Mald), Sri Lanka (Sri), Bangladesh (Ban), Andaman eilanden (And), Maleisië (Mals), Indonesië
(Ind), West-Australië (Aus). Er worden drie groepen van staalnameplaatsen onderscheiden, namelijk de
clusters A, B en C. De eigenwaarden van de eerste twee assen zijn respectievelijk 0,827 en 0,042.
Sheppard et al. (1992) verwachten dat de verspreidingspatronen van de meeste soorten in
de Arabische Zeeën (bestaande uit de Rode Zee, Golf van Aden, Arabische Zee, Golf van
Oman en de Perzische Golf) niets meer dan kansverdelingen zijn en dat het gehele gebied
één biogeografische subregio vormt. Behoudens enkele uitzonderingen (b.v. de hoge graad
van endemisme onder de vlindervissen), veronderstellen Sheppard et al. (1992) dat de

Synthese en perspectieven 145
biogeografische patronen een gevolg zijn van de geringe verbreidingstijd sinds het begin van
het Holoceen en het onvolledig mengen van fauna doorheen de geschikte habitats van de
Indische Oceaan. Deze auteurs merken ook op dat de onderverdeling van de Arabische
Zeeën in kleinere biogeografische eenheden mogelijk is voor bepaalde visgroepen, maar
voor andere organismen, en in het bijzonder de planten, is er volgens hen geen aanleiding tot
een indeling onder het niveau van een biogeografische provincie. Diverse analysetechnieken
(hoofdstukken 6, 7) duiden nochtans op afzonderlijke plantengemeenschappen en
plantenbiotopen in overeenstemming met de verschillen in milieuparameters. De door
opwelling beïnvloede gemeenschappen zijn hiervan het meest typerend voor de unieke
Arabische Zeeflora. Bepaalde soorten van deze gemeenschappen vertonen disjuncte
verspreidingspatronen doorheen de Indo-Pacific en zijn waarschijnlijk ook van
biogeografisch belang binnen de Arabische regio. Dit, in combinatie met het toenemend
aantal beschreven wier-endemen, doet ons besluiten dat de Arabische Zee een
fytogeografische (sub)provincie vertegenwoordigt in de Indo-Pacific en de Arabische regio.
Toekomstig terreinwerk in de noordelijke Arabische Zee (Al Qad, Oman) kan het
onderzoeksgebied aanzienlijk verruimen om biogeografische (dis)continuïteiten aan de grens
van de Arabische Zee met de Golf van Oman vast te stellen. De belangrijke vraagstellingen
zijn: (i) de graad van divergentie met betrekking tot de Oost-Afrikaanse flora, (ii) de impact
van opwelling op deze gemeenschappen, (iii) het gebruik van deze lokatie in een
geografische gradiënt, van de Arabische Zee over de Golf van Oman naar de Perzische Golf,
om het verloop in wiersoorten te toetsen aan de afname in substraatbeschikbaarheid
(sedimentkusten als biogeografische barrière). Recent werden de eerste temperatuurrecorders
geplaatst rond Masirah (Wilson 1999) om accurate kustwatergegevens te bekomen op een
gedetailleerde temporele en ruimtelijke schaal. Deze nauwkeurige gegevens zijn
noodzakelijk om de relatie tussen milieuparameters en biotische interacties (b.v. de
competitie tussen wieren en koralen) te kunnen begrijpen.
Seizoenaliteit
Nizamuddinia zanardinii is een groot bruinwier (Fucales) endemisch voor de
opwellingsgebieden van de Arabische Zee. In de eerste vermelding van het wier voor de
Socotra Archipel, merkt Kemp (1998) op dat er verschillen in seizoenale groei bestaan
tussen de populaties van Socotra en deze van zuidelijk Arabië. Twee hypothesen werden
geopperd: (i) een temporele verschuiving in de groeicyclus (tot zes maanden) van N.
zanardinii rond Socotra in vergelijking met de populaties van het vasteland, of (ii) twee
(re)productieve pieken voor dit wier ter hoogte van Socotra, in tegenstelling tot één voor
deze van zuidelijk Arabië. Hoewel initieel vooropgesteld, waren langere periodes van
terreinwerk in functie van een seizoenaliteitsonderzoek niet mogelijk ten gevolge van
praktische problemen (zie hoofdstuk 1). Toch leverden de waarnemingen van de eerste drie
veldwerkperiodes enig inzicht in de seizoenale groeipatronen van deze sleutelsoort. Het
gelijktijdig voorkomen van zowel volgroeide, fertiele N. zanardinii specimens in de
intertidale rotspoeltjes van Masirah als onontwikkelde, kleine rozetten ter hoogte van Barr
al-Hikman, blijkt er op te wijzen dat de (re)productieve periodes kunnen fluctueren binnen
een specifiek geografisch gebied, afhankelijk van het habitat en/of de zonatie van
voorkomen. Gelijkaardige verschillen werden waargenomen voor de Socotra Archipel:
terwijl Kemp (1998) de reproductieve assen opmerkte in februari-maart 1996 en Leliaert
(2000) in januari-februari 1999, werden er enkel kleine thalli geobserveerd tijdens het
terreinwerk in maart-mei 2000. Dit doet vermoeden dat er twee reproductieve periodes

146 Hoofdstuk 9
bestaan (cf. Hadramoutkust in Jemen, Ormond & Banaimoon 1994), gerelateerd aan de twee
opwellingsperiodes, met temporele (jaarlijkse) en lokale fluctuaties. Hierbij wordt er van
uitgegaan dat de (re)productieve respons van de Nizamuddinia-populaties van Jemen en
Oman groter is gedurende de zuidwest- dan tijdens de noordoostmoesson.
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