Marine Biology (1999) 134: 479±489
Ó Springer-Verlag 1999
O. Langmead á N. E. Chadwick-Furman
Marginal tentacles of the corallimorpharian Rhodactis rhodostoma.
1. Role in competition for space
Received: 1 July 1998 / Accepted: 24 March 1999
Abstract The corallimorpharian Rhodactis rhodostoma
(Ehrenberg, 1934) forms aggregations that dominate
patches on some coral reef ¯ats in the Red Sea. The
outcomes and mechanisms of competition for space between this corallimorpharian and other sessile organisms
are poorly understood. Polyps of R. rhodostoma were
observed to overgrow zoanthids, hydrozoan corals,
sponges and encrusting macroalgae on a fringing reef at
Eilat, northern Red Sea. R. rhodostoma polyps also
damaged, and in some cases overgrew, reef-building
corals in the families Poritidae, Acroporidae and
Pocilloporidae, most of which form branching colonies
with small polyps that are subordinate in coral competitive hierarchies. In contrast, most stony corals in the
families Faviidae and Mussidae had stando€ interactions
with R. rhodostoma, in which they prevented the corallimorpharians from damaging them or approaching
closer than 1 to 3 cm. The latter corals are ranked at the
top of competitive hierarchies for Indo-Paci®c corals,
and they form massive colonies of large polyps which
may develop aggressive organs termed sweeper tentacles.
Some soft corals that exude allelopathic chemicals also
avoided overgrowth by the corallimorpharians. Tentacles along the oral disk margin of R. rhodostoma polyps
were swollen and bulbous during contacts with cnidarians. These bulbous marginal tentacles had signi®cantly
thicker ectoderm and a higher proportion of holotrichous nematocysts than did the normally ®liform mar-
Communicated by R. Cattaneo-Vietti, Genova
O. Langmead
School of Ocean Sciences,
The University of Wales, Bangor,
Menai Bridge Marine Science Laboratory,
Gwynedd, LL 59 5EY, United Kingdom
N.E. Chadwick-Furman (&)
Interuniversity Institute for Marine Science,
P.O. Box 469, Eilat, Israel, and
Faculty of Life Sciences, Bar Ilan University,
Ramat Gan, Israel
ginal tentacles of R. rhodostoma polyps. It is concluded
that, on the reef ¯at at Eilat, this corallimorpharian
damages and overgrows a variety of sessile competitors,
including branching stony corals, via the application of
specialised marginal tentacles ®lled with penetrating nematocysts. R. rhodostoma is an intermediate competitor
in the aggressive hierarchy among Indo-Paci®c Anthozoa, including the reef-building corals.
Introduction
Corallimorpharians are sessile cnidarians that super®cially resemble actinian sea anemones, but are morphologically similar to scleractinian corals. Like the
stony corals, they lack basilar muscles, ciliated siphons
(siphonoglyphs) along the pharynx, and ciliated lobes on
their mesenterial ®laments (Carlgren 1949; den Hartog
1980; Fautin and Lowenstein 1992), and thus have been
classi®ed by some authors as skeleton-less corals (Schmidt 1974; den Hartog 1980 and references therein).
Corallimorpharians are major components of some
temperate and tropical marine communities. Members
of the corallimorpharian genus Corynactis form aggregations that may dominate space on subtidal hard substrata in the northern Paci®c and Atlantic Oceans
(reviewed in Chadwick 1987, 1991). Some corallimorpharians also form large aggregations that dominate patches of substratum on tropical coral reefs, from
which they exclude other benthic organisms (den Hartog
1980; Ridzwan 1993; Chadwick-Furman personal observation).
Some species of corallimorpharians are known to use
specialised aggressive behaviours to attack and kill
competitors. Polyps of Corynactis californica extrude
mesenterial ®laments directionally to kill and overgrow
neighbouring corals and sea anemones (Chadwick 1987).
This behaviour, along with a rapid rate of asexual reproduction (Chadwick and Adams 1991), allows members of this species to monopolise space along the tops of
subtidal boulders in central California kelp forests
480
(Chadwick 1991). The Caribbean corallimorpharian
Discosoma (=Rhodactis) sanctithomae uses inducible
bulbous tentacles to kill stony corals and defend its
space on coral reefs (den Hartog 1977; Miles 1991). In
both species, the use of aggressive organs allows the
corallimorpharians to damage competitors and to
overgrow them on hard substrata.
Little is known concerning the competitive interactions of corallimorpharians in the tropical Indo-Paci®c.
Scattered reports indicate that they are important occupiers of space in some habitats on coral reefs in this
region, and may exclude reef-building corals from
patches of shallow substratum. In the Seychelles, polyps
of Discosoma (=Rhodactis) howesii have been observed
to form patches of considerable size that overgrow and
apparently kill stony corals (den Hartog 1994). Both
D. (=R.) howesii and D. dawydo use bulbous marginal
tentacles to kill stony corals in Malaysia (Ridzwan
1993). In an anecdotal report, Moosleitner (1989)
termed Rhodactis sp. corallimorpharians ``killer anemones'' due to their imputed ability to damage and
overgrow corals in the Maldives.
Rhodactis (=Discosoma) rhodostoma is one of the
most common corallimorpharians on shallow reefs in
the northern Red Sea (Spiegel 1998). Polyps of this
species reproduce asexually to form aggregations that
may cover patches of several square meters on reef ¯ats
and shallow reef slopes, thereby excluding other benthic
organisms (Spiegel 1998; Chadwick-Furman personal
observation). Information on the outcomes and mechanisms of competitive interactions involving this species
would greatly increase our understanding of the importance of corallimorpharians as spatial competitors
on Indo-Paci®c coral reefs.
This study presents the frequency and outcome of
competitive interactions between polyps of Rhodactis
rhodostoma and other sessile organisms on the reef ¯at at
Eilat, northern Red Sea. The morphology and cnidom of
dimorphic marginal tentacles is also described, some of
which may function in the mechanism of interference
competition used by R. rhodostoma. In a companion
paper, it is shown that specialised bulbous tentacles
develop along the oral disk margin of R. rhodostoma
polyps within 3 weeks after initial contact with coral
competitors, and that the application of these specialised
tentacles causes long-term tissue damage to certain
scleractinian corals (Langmead and Chadwick-Furman
1999). These reports constitute the ®rst detailed description of aggressive interactions in a tropical IndoPaci®c corallimorpharian.
Materials and methods
Frequency and outcome of ®eld interactions
The present study was conducted at the Coral Beach Nature Reserve, Eilat, northern Red Sea (29°30¢10¢¢N; 34°55¢15¢¢E). The study
site was a well-developed fringing reef that has been described in
detail by Loya and Slobodkin (1971). Polyps of Rhodactis rhodostoma (Ehrenberg, 1934) formed large aggregations on the reef ¯at
at this site. The frequency of competitive interactions between
R. rhodostoma and other sessile organisms was assessed by haphazardly throwing 20 cm square quadrats onto aggregations, and
examining all polyps within these quadrats, until a total of 1000
polyps had been observed (N = 33 quadrats). The sampling
scheme was limited to the area where this species was most
abundant, and thus also where most intraspeci®c contacts occur, so
it provides a conservative estimate of contact rates with other
species. For each R. rhodostoma polyp, the types of sessile macroorganisms contacted were recorded, and it was noted whether
bulbous marginal tentacles (BMTs) were present on the corallimorpharian (Fig. 1). The polyps were considered to contact other
organisms if close enough for their extended tissues to touch,
within ca. 1 to 3 cm inter-individual distance, depending on the
type of organism contacted (after Lang and Chornesky 1990;
Chadwick 1991). BMTs were de®ned as tentacles with blunt,
swollen, globular white tips that were developed into acrospheres
(after den Hartog 1977; Miles 1991). These tentacles contrasted in
appearance with the normally ®liform marginal tentacles (FMTs)
of R. rhodostoma, which had narrow brown tips (after den Hartog
1977; Miles 1991). Frequencies of polyp contact with macroalgae
were not recorded since preliminary observations indicated that
most polyps of R. rhodostoma were attached to encrusting macroalgae on the reef ¯at.
Polyps within the above quadrats were examined to assess the
outcomes of their competitive interactions, and additional observations were made by snorkelling over the reef ¯at. For each polyp
of Rhodactis rhodostoma that contacted other species of sessile
macro-organisms, information was recorded on the type of organism contacted, any damage to the corallimorpharian or the
other organism, the direction of overgrowth if present, and the
occurrence of BMTs on the corallimorpharian. The outcomes of
contacts with conspeci®c polyps were not recorded; preliminary
observations indicated that no BMTs or damage were evident in
any conspeci®c interactions of R. rhodostoma. In contacts with
members of other species, damage to either partner was de®ned as
the presence of necrotic tissue, excessive mucus, or exposed skeleton along the region of contact (after Sebens 1976; Cope 1981;
Chadwick 1991; Miles 1991). Overgrowth was de®ned as the base
of one of the organisms growing on top of the living tissue or
nonliving skeleton of the other. Interactive reach also was recorded
for contacts with stony and soft corals and was de®ned as the
minimum distance between living tissues of the interacting pair
(after Sheppard 1981).
Tentacle morphology and cnidom
Five polyps of Rhodactis rhodostoma that possessed well-developed
BMTs and ®ve polyps that bore only FMTs were collected from the
reef in order to characterise the morphology and cnidom of the
dimorphic marginal tentacles. All ten polyps were transferred to the
nearby Interuniversity Institute for Marine Science and maintained
in outdoor running seawater aquaria for less than 3 d before
sampling their tentacles. The polyps were then anaesthetised in a
1:1 solution of ®ltered seawater and 7.5% MgCl2 in distilled water
for approximately 1 h or until unresponsive to tactile stimulation.
Four BMTs were removed from each of the ®ve polyps that possessed BMTs, and four FMTs from each of the other ®ve polyps
that did not possess BMTs (=20 tentacles sampled of each type).
Live tissue squashes were prepared by mounting each tentacle in
two drops of ®ltered seawater, and gently applying a coverslip (Size
1, 22 ´ 22 mm). Without further squashing, this preparation was
examined under a Nikon (Type 102) phase contrast microscope
®tted with a calibrated eyepiece reticule. Three measurements were
made on each tentacle: (1) diameter at the tip (= 0.5 mm from the
tip), (2) diameter at the stalk (=1.5 mm from the tip), and (3)
ectodermal thickness at the tip.
For ten tentacles of each type, the above preparations were
further squashed and examined at 400´ magni®cation to determine
481
Fig. 1 Rhodactis rhodostoma. A
naturally occurring interaction
with the massive scleractinian
coral Porites sp. on the reef ¯at
at Eilat, northern Red Sea.
Note the white-tipped bulbous
marginal tentacles of the corallimorpharian, which are expanded over the live tissues of
the coral. Note also the white
area of exposed skeleton on the
coral, and the absence of a clear
tissue-free zone between members of the two species. Scale
bar = 2 cm
the relative abundance of each type of nematocyst present. The ®rst
300 nematocysts were identi®ed in the tip region of each tentacle
along a transect across the slide. For each of ®ve tentacles of each
type, the length and width were measured for the ®rst four undischarged nematocysts of each type encountered (N = 20 capsules of
each nematocyst type measured per tentacle type, after Stephenson
1929; Manuel 1981). Only undischarged capsules were measured,
because discharged cnidae are known to have smaller capsules
(Godknecht and Tardent 1988).
Photographs were taken of tentacle morphology in the above
fresh preparations, using a Nikon labophot phase contrast (1.25)
microscope ®tted with a Nikon FX35 camera. Nematocyst photographs were made from specimens that were ®rst anaesthetised as
above, then ®xed and preserved in 4% formalin in distilled water.
Some of the preserved tentacles were excised, transferred to slides
and squashed. Using a Reichert Polyvar 2 DIC (di€erential interference contrast) microscope, photographs were taken with a Yashica 108 multiprogram camera. All nematocyst types in both
BMTs and FMTs were photographed at 1000´ magni®cation under
oil immersion.
Table 1 Rhodactis rhodostoma.
Frequency of ®eld interactions
with sessile macro-organisms
and occurrence of bulbous
marginal tentacles (BMTs).
N = 1000 polyps observed on
the reef ¯at at Eilat, northern
Red Sea
Results
Frequency and outcome of ®eld interactions
In aggregations on the reef ¯at, polyps of Rhodactis
rhodostoma occurred at high densities of 735 ‹ 491
polyps m)2 (mean ‹ 1 SD, N = 33 quadrats examined). They were unevenly distributed throughout the
aggregations and occurred in localised patches of up to
1700 polyps m)2 and as few as 25 polyps m)2. Most
(>80%) R. rhodostoma polyps contacted only conspeci®cs, and some (6%) occurred as isolated polyps that
did not contact any other sessile organisms (Table 1).
The remaining 13% of the polyps contacted a wide variety of sessile organisms, mostly colonies of the
branching hydrozoan coral Millepora spp., but also
Interaction type
No contact
Contact with conspeci®cs only
Contact with conspeci®cs and:
Porifera (black, encrusting sponge)
Cnidaria
Hydrozoa (Millepora spp.)
Anthozoa
Alcyonaria (Parerythropodium fulvum)
Zoantharia (Palythoa spp.)
Actiniaria (Heteractis crispa)
Scleractinia (Seriatopora hystrix)
Scleractinia (Platygyra spp.)
Corallimorpharia (Actinodiscus nummiformis)
Total in interspeci®c contact
a
R. rhodostoma polyp exhibited tissue damage
Polyps %
With BMTs (%)
6.1
0
80.7
0
0.5
0
11.8
1.5
0.1
0.2
0.1
0.1
0.1
0.3
0.1
0.2
0a
0.1
0.1
0
13.2
2.0
482
The outcomes of interactions with scleractinian corals
varied with the family of coral contacted. In most cases,
the corallimorpharians damaged stony corals in the
families Poritidae (Porites spp., 60% of contacts),
Acroporidae (Montipora spp., 46%, Acropora spp.,
90%), and Pocilloporidae (Seriatopora hystrix, 95%,
Stylophora pistillata, 67%), and induced formation of
BMTs (Fig. 3A). In some cases, the corallimorpharians
were observed to grow over the exposed skeletons of
these corals (Figs. 1, 3A). Corals in the above families
exhibited only a narrow gap between their live tissues
and those of the corallimorpharians, usually <1 cm
(Figs. 1, 3B). In contrast, most stony corals in the
families Faviidae and Mussidae induced BMT formation in all contacts with the corallimorpharians, but
showed no evidence of damage or overgrowth (Fig. 3A).
Corals from the latter two families had relatively large
distances between their live tissues and those of
Poritidae Pocilloporidae Acroporidae
Faviidae
Mussidae
R. rhodostoma with BMTs
Neighbour damaged
Tissues of neighbour overgrown
A
100
% of interaction
zoanthids, sponges, soft corals and stony corals
(Table 1). In the few cases of contact with anthozoan
cnidarians, most of the R. rhodostoma polyps had welldeveloped bulbous marginal tentacles (BMTs), as described above. BMTs were not observed in contacts with
non-cnidarians such as black encrusting sponges
(Table 1) or macroalgae.
The outcome of interspeci®c interactions in Rhodactis
rhodostoma depended on the type of organism contacted.
Sponges, macroalgae and the hydrozoan coral Millepora
spp. were overgrown with no evidence of tissue damage,
and few BMTs were visible on the corallimorpharians
(Fig. 2). During contacts with other types of cnidarians,
polyps of R. rhodostoma had well-developed BMTs in
>50% of observed cases (Fig. 2). In some cases, tissue
damage and overgrowth of neighbouring cnidarians also
was observed (Fig. 2). Actiniarian sea anemones (Heteractis crispa and Entacmea quadricolor) were not damaged or overgrown by the corallimorpharians, but
induced the development of BMTs in all cases (Fig. 2).
The only evidence of damage to R. rhodostoma observed
in the ®eld survey occurred during contact with
H. crispa, on a single polyp. Other species of corallimorpharians (Actinodiscus nummiformis and Actinodiscus sp.) induced development of BMTs in about
50% of observed contacts, and frequently were overgrown by R. rhodostoma, although no tissue damage was
detected (Fig. 2).
75
50
25
R. rhodostoma with BMTs
Neighbour damaged
Tissues of neighbour overgrown
0
3.0
100
1.0
Fig. 2 Rhodactis rhodostoma. Outcomes of naturally occurring ®eld
interactions with other sessile macro-organisms on the reef ¯at, Coral
Nature Reserve, Eilat, northern Red Sea (total number of interactions
observed = 497)
Acanthastrea
echinata (n = 6)
Platygyra spp.
(n = 8)
Favites spp.
(n = 6)
Favia spp.
(n = 4)
Cyphastrea
micropthalma (n = 4)
Macroalgae
(n = 41)
Sponges
(n = 8)
Hydrozoan corals
(n = 175)
Alcyonaria
(n = 59)
Zooantharia
(n = 35)
Scleractinia
(n = 138)
Actiniaria
(n = 14)
0
Corallimorpharia
(n = 27)
0
Acropora spp.
(n = 21)
Goniastrea spp.
(n = 2)
0.5
Montipora spp.
(n = 19)
25
1.5
Stylophora pistillata
(n = 15)
50
2.0
Seriatopora hystrix
(n = 17)
75
Porites spp.
(n = 8)
Distance between tissues (cm)
% of interaction
B
2.5
Fig. 3 Rhodactis rhodostoma. A Outcomes of naturally occurring ®eld
interactions with scleractinian corals. B Distances to live tissues of
scleractinian corals. Distances are presented only for interactions in
which BMTs were observed on R. rhodostoma (mean ‹ 1 SD). All
observations were made on the reef ¯at of the Coral Nature Reserve,
Eilat, northern Red Sea
483
Tentacle morphology and cnidom
The marginal tentacles of Rhodactis rhodostoma polyps
were dimorphic (Figs. 1, 5). BMTs had well-developed
acrospheres, as evidenced by a signi®cantly higher ratio
of tip to stalk diameter (all values given as mean ‹ SD;
1.55 ‹ 0.22, N = 20 tentacles) than that in FMTs
A
B
100
% of interaction
Rhodactis rhodostoma polyps, in most cases >1 cm, and
up to 3 cm for colonies of the massive coral Platygyra
spp. (Fig. 3B). An exception to this familial pattern was
observed in two colonies of Goniastrea spp. in the family
Faviidae, which appeared to be damaged and overgrown
by polyps of R. rhodostoma (Fig. 3A), and also had
relatively short interactive distances (Fig. 3B).
The corallimorpharians were observed to interact
with four genera of alcyonacean soft corals on the reef
¯at. Only one colony of the soft coral Lithophyton sp.
was observed to contact Rhodactis rhodostoma on the
reef ¯at, and no evidence of damage, overgrowth, or
BMT formation was observed. The other three genera of
soft corals had multiple interactions with R. rhodostoma,
and the outcome of contact varied among them (Fig. 4).
Colonies of Sinularia spp. in almost all cases induced
BMT formation on the corallimorpharians, and were
overgrown (Fig. 4). Colonies of the organ pipe coral
Tubipora musica and the soft coral Parerythropodium
fulvum in some cases induced BMT formation on
R. rhodostoma, but were damaged or overgrown at low
frequencies (Fig. 4). The interactive distance between
live tissues of the corallimorpharians and soft corals
varied signi®cantly with the type of soft coral contacted
(Fig. 4) (Kruskal±Wallis test, v2 ˆ 29:60, p < 0.001).
Similar to the pattern in stony corals (Fig. 3), members
of soft coral genera with longer interactive distances
were damaged less frequently than those with shorter
distances to the live tissues of the corallimorpharians
(Fig. 4).
0.06+0.28
R. rhodostoma with BMTs
Neighbour damaged
Tissues of neighbour overgrown
75
0.35+0.29
50
0.65+0.43
25
0
Sinularia spp.
(n = 19)
Tubipora musica Parerythropodium
(n = 6)
fulvum (n = 33)
Fig. 4 Rhodactis rhodostoma. Outcomes of naturally occurring ®eld
interactions with soft corals on the reef ¯at of the Coral Nature
Reserve, Eilat, northern Red Sea. Mean distance between live tissues
(cm) ‹ 1 SD indicated above columns
(1.00 ‹ 0.17, N = 20 tentacles) (two-sample t-test;
t = )8.70, p < 0.001). The FMTs had narrow tips with
no acrospheres (Figs. 1, 5A). The relationship between
the diameter of tip and stalk in each tentacle type was
found to be linear (Pearson's correlation coecient
r = 0.7 and 0.8 for FMTs and BMTs, respectively).
Thus the ratio of the diameter of tentacle tip to stalk was
considered to be a reliable indicator of acrosphere
development.
Fig. 5 Rhodactis rhodostoma. Microscope squashes of marginal
tentacle tips. A Filiform marginal tentacle. B Bulbous marginal
tentacle. Scale bars = 250 lm
484
The thickness of the ectodermal layer in BMTs
(223.00 ‹ 66.26 lm, N = 20 tentacles) was signi®cantly higher than that of FMTs (83.50 ‹ 26.80 lm,
N = 20 tentacles) (Fig. 5B) (two-sample t-test; t =
8.72, p < 0.001). Though ®ve distinct types of
nematocysts were present in all marginal tentacle tips
(Fig. 6A±E), the relative abundance of each nematocyst
type also di€ered signi®cantly between the two tentacle
types (Fig. 7) (Chi-square test for proportions, v2 ˆ
3641:93, p < 0.001). FMTs contained mostly Type 2
microbasic-b-mastigophores (Fig. 6E) (>80% of the
cnidom; Fig. 7), whereas BMTs were ®lled with Type 1
holotrichs (Fig. 6A) (>90% of the cnidom; Fig. 7). In
addition, both of these nematocyst types had signi®cantly larger capsules when present in BMTs than they
did when occurring in FMTs (Tables 2, 3). This size
di€erence can be seen clearly in the size-frequency distributions of Type 1 holotrichs from the two tentacle
types, which show almost no overlap in capsule length
(Fig. 8).
Discussion
This study shows that polyps of the corallimorpharian
Rhodactis rhodostoma occur at high densities in patches
on the reef ¯at at Eilat, northern Red Sea. Members of
this species also dominate parts of the reef ¯at at other
localities in the Red Sea, including at Ras Abu Galum
B
A
C
along the Egyptian coast of the Gulf of Aqaba (Chadwick-Furman personal observation). The abundance of
this corallimorpharian was quanti®ed only on part of
the reef ¯at at Eilat, but qualitative observations at other
sites in the Gulf of Aqaba indicate that members of this
species are limited to sheltered, inner reef ¯at habitats
where they are very patchy in abundance. A congener of
Rhodactis forms rare aggregations of varying size on
reefs in the Maldive Islands (W. Allison personal communication). Other Rhodactis (=Discosoma) species
have been observed to occupy patches covering several
square meters on shallow reefs in the Seychelles (den
Hartog 1994), Taiwan (Chen et al. 1995a, b), Malaysia
(Ridzwan 1993) and the Caribbean (den Hartog 1980).
Thus, these corallimorpharians may competitively exclude stony corals from patches of space in some shallow
habitats on tropical coral reefs worldwide.
It is also demonstrated here that some polyps at the
edges of Rhodactis rhodostoma aggregations interact
with a wide variety of sessile organisms, including
sponges, algae and members of six orders of Cnidaria
(Table 1). A major competitor for space with R. rhodostoma appears to be the hydrozoan Millepora spp.
(Table 1), which is a common organism on the reef ¯at
and shallow slope at Eilat (Loya and Slobodkin 1971).
The unilateral overgrowth of Millepora colonies by
this corallimorpharian leads to the formation of carpets
of R. rhodostoma polyps attached to the non-living
stony skeletons of the hydrozoan. Branching skeletons
of Millepora >1 m in height were observed to be
D
E
Fig. 6 Rhodactis rhodostoma. Nematocyst types present in the
octodermal tips of marginal tentacles: A Type 1 holotrichs; B Type
2 holotrich; C microbasic-p-mastigophore; D Type 1 microbasic-bmastigophore; E Type 2 microbasic-b-mastigophore. Scale bars =
5 lm
100
Filiform tentacle
Bulbous tentacle
75
50
25
M-b-M (2)
M-b-M (1)
M-p-M
Holotrichs (2)
0
Holotrichs (1)
% abundance of nematocysts within marginal tentacle tip
485
Fig. 7 Rhodactis rhodostoma. Relative abundances of nematocyst
types in the ectoderm of ®liform versus bulbous marginal tentacle tips
(mean ‹ 1 SD, N=10 tentacles of each type, 300 capsules examined
per tentacle) (M-p-M microbastic-p-mastigophore; M-b-M microbasic-b-mastigophore, Type 1 and 2)
completely overgrown by the corallimorpharians, the
outline of the former hydrozoan colonies covered by a
continuous carpet of R. rhodostoma polyps, on the reef
¯at at Ras Abu Galum, south of Eilat in the Gulf of
Aqaba (Chadwick-Furman personal observation).
Also, polyps of Rhodactis sp. have been observed
growing on top of the erect skeletons of Millepora
colonies in the Maldives (H. Moosleitner personal
communication).
Of the organisms contacted by Rhodactis rhodostoma,
only actinian sea anemones and some soft and massive
stony corals appeared able to prevent damage or overgrowth. Actinian sea anemones are known to be dominant in contact competition against other sessile
organisms on coral reefs (Bak and Borsboom 1984),
including stony corals (Sebens 1976). Several types of
actinians have been demonstrated to possess potent
mechanisms of interference competition for maintenance
of their living space (Francis 1973; Purcell 1977; Williams 1991). Many actinians on coral reefs occur as
solitary polyps, the most conspicuous being those that
harbour obligate symbiotic clown®sh (Fautin and Allen
1992). Solitary actinians are at high risk of being overgrown by the numerous cnidarians that form colonies,
including stony and soft corals and corallimorpharians.
Thus, it is not surprising that the large, solitary actinians
contacted by R. rhodostoma polyps (see ``Results'')
Table 2 Rhodactis rhodostoma. Sizes of nematocyst capsules in bulbous and ®liform marginal tentacle tips. N=20 capsules from each
tentacle type; mean ‹ 1 SD, range in parentheses
Nematocyst type
Holotrichs (1)
Holotrichs (2)
Microbasic-p-mastigophores
Microbasic-b-mastigophores (1)
Microbasic-b-mastigophores (2)
Filiform marginal tentacle
Bulbous marginal tentacle
length (lm)
width (lm)
length (lm)
width (lm)
32 ‹ 3
(27±37)
33 ‹ 2
(30±36)
23 ‹ 1
(20±25)
19 ‹ 1
(16±21)
29 ‹ 3
(22±36)
6‹1
(4±8)
11 ‹ 1
(9±13)
7‹1
(6±8)
6 ‹ 0.4
(5±6)
4‹1
(3±7)
51 ‹ 6
(36±58)
33 ‹ 2
(30±36)
23 ‹ 1
(20±25)
20 ‹ 2
(16±24)
33 ‹ 4
(26±42)
6‹1
(5±8)
12 ‹ 1
(10±13)
6‹1
(5±8)
6‹1
(5±7)
4‹1
(3±5)
Table 3 Rhodactis rhodostoma. Statistical comparison of ectodermal nematocyst capsule lengths in ®liform versus bulbous
marginal tentacle tips according to Levene's test, con®rming
homogeneity of variance, and two-sample t-test, assuming equal
Nematocyst type
Holotrichs (1)a
Holotrichs (2)
Microbasic-p-mastigophores
Microbasic-b-mastigophores (1)b
Microbasic-b-mastigophores (2)
a
b
variance (df=38 throughout). All data were normally distributed,
Kolmogorov±Smirnov test for goodness of ®t; *indicates signi®cant
di€erences at p < 0.01
Levene's test
Two-sample t-test
F
p
t
p
0.96
1.60
0.35
4.54
0.034
0.33
0.21
0.56
0.04
0.85
)14.01
0.38
1.16
)1.44
)3.94
<0.001*
0.71
0.25
0.16
<0.001*
Indicates data which was log10 transformed to make variances consistent
Indicates where a t-test with separate variance estimates was used
486
Number of capsules
75
Filiform tentacle
Bulbous tentacle
50
25
66-70
61-65
56-60
51-55
46-50
41-45
36-40
31-35
26-30
0-25
0
Size class of type 1 holotrich capsules (length, µm)
Fig. 8 Rhodactis rhodostoma. Size-frequency distribution of Type 1
holotrich capsules in the tips of ®liform versus bulbous marginal
tentacles (N=100 capsules examined in each tentacle type)
appeared to defend their space e€ectively, with no evidence of damage from the interaction (Fig. 3A).
Some of the soft corals contacted by Rhodactis rhodostoma are known to exude allelochemicals in the form
of terpenoid compounds into the water column surrounding their colonies (Coll et al. 1982). This mechanism of allelopathy, which occurs in many soft corals
(Sammarco et al. 1983), may explain the observed inability of R. rhodostoma polyps to overgrow or damage
colonies of the soft coral Parerythropodium fulvum, and
also the wide interactive distance between their tissues
(Fig. 4). P. fulvum contains a variety of toxic organic
compounds (Green et al. 1992), and is poisonous to reef
®sh and marine bacteria (Kelman 1998). It seems feasible that P. fulvum may use these noxious chemicals to
deter R. rhodostoma from invading its space. Members
of at least one of the other soft coral genera contacted,
Sinularia, also are known to possess allelochemical defenses (Coll et al. 1982), but were unable to prevent
damage by the corallimorpharians (Fig. 4).
The massive scleractinian corals that avoided overgrowth by polyps of Rhodactis rhodostoma all are ranked
as aggressive or intermediate in competitive hierarchies
among reef corals (Sheppard 1979; Cope 1981). Members of the family Mussidae are dominant among Hong
Kong corals (Cope 1981), and Faviidae are near the top
of hierarchies among corals in both the Indo-Paci®c and
Caribbean (Lang 1973; Sheppard 1979; Cope 1981;
Logan 1984). Members of some genera in these families,
including the Platygyra spp. and Favites spp. observed
here (Fig. 3), possess the ability to develop sweeper
tentacles, inducible competitive organs that sweep the
area surrounding the coral colony and prevent other
cnidarians from approaching closer than 1 to 3 cm to
their live tissues (Sheppard 1979; Hidaka et al. 1987).
The deployment of these aggressive organs may explain
the wide margin of space maintained between their tissues and those of the corallimorpharians (Fig. 3B), and
also the apparent inability of R. rhodostoma to damage
or overgrow them (Fig. 3A).
The only scleractinian coral in the family Faviidae
that Rhodactis rhodostoma was able to damage was Goniastrea spp. (Fig. 3A). It is not clear why members of
this genus deviated from the pattern for their family,
since Goniastrea spp. are ranked intermediate in aggressive hierarchies (Sheppard 1979) and have a wide reach
when interacting with other corals (Sheppard 1981).
The stony corals that were damaged by polyps of
Rhodactis rhodostoma belonged mostly to three families
of small-polyped, mainly branching corals that are
intermediate or subordinate in hierarchies among IndoPaci®c corals (Sheppard 1979; Cope 1981). Field
experiments con®rm that within 2 weeks R. rhodostoma
polyps may actively damage the branching colonies of at
least one of these corals, Acropora eurystoma, and within
16 months partially overgrow them (Langmead and
Chadwick-Furman 1999). Field observations at Ras
Abu Galum in the Egyptian Red Sea also indicate that
R. rhodostoma polyps grow over the bases and sides of
Acropora spp. coral colonies, and in some cases completely cover their skeletons (Chadwick-Furman personal observation). The very short interactive reach
between the tissues of branching stony corals and corallimorpharians (Fig. 3B) corresponds to the lack of
inducible aggressive structures in these corals, in contrast to the massive corals discussed above. In general,
branching corals appear to invest their resources in rapid
growth and the production of a tall colony shape that
can overtop and shade some opponents, rather than into
mechanisms of direct tissue competition (Lang and
Chornesky 1990).
The interactive distances observed in the present
study between corallimorpharians and stony corals are
similar to those found for interactions among scleractinian corals (Sheppard 1981). This consistency indicates that interactive distance is set by the aggressive
reach of the corals and not by the corallimorpharians.
Some scleractinian corals are known to extend aggressive organs, such as long mesenterial ®laments or
sweeper tentacles, over the tissues of their opponents
(Lang and Chornesky 1990), whereas the aggressive
organs of Rhodactis rhodostoma are short marginal
tentacles that can extend only a few millimeters in length
(Figs. 1, 5). The most aggressive species of corals appeared able to defend their space on the reef by keeping
R. rhodostoma polyps at a distance. Thus, the interactive
reach (sensu Sheppard 1981) of aggressive mechanisms
determines, in part, the success of each type of cnidarian
during competition.
These results place Rhodactis rhodostoma as intermediate in aggressive ability among scleractinian corals
on Indo-Paci®c reefs, between the dominant massive and
subordinate branching corals. They indicate that this
487
corallimorpharian wins during contact competition with
encrusting algae, sponges, hydrozoan corals and
branching stony corals, but is unable to overgrow massive stony corals, actinian sea anemones and some soft
corals. The latter groups include cnidarians with specialised aggressive mechanisms of competition for space
(Sammarco et al. 1983; Williams 1991). R. rhodostoma
appears to dominate patches e€ectively on the reef ¯at
via exploitation of open space by asexual reproduction
(Spiegel 1998), followed by damage and overgrowth of
at least some types of sessile organisms.
The mechanism of interference competition employed
by Rhodactis rhodostoma appears to be the development
of specialised bulbous tentacles along the oral disk
margin (Figs. 1, 5). We have shown through ®eld experiments that these tentacles are induced to develop
from normally ®liform marginal tentacles within 3 weeks
of initial contact with coral competitors (Langmead and
Chadwick-Furman 1999). Field observations in the
present study con®rm that BMTs develop only upon
contact with cnidarians. The low frequency of BMT
development upon contact with the hydrozoan coral
Millipora (Table 1) was possibly due to their taxonomic
distance from corallimorpharians within the phylum
Cnidaria. The highest frequencies of BMT development
were observed in contacts with actinian sea anemones
and massive stony corals, both of which resisted damage
by the corallimorpharians (Figs. 2, 3). Hidaka (1985)
has shown that the ®ring of nematocysts is important for
the induction of aggressive structures in corals. This
factor also may stimulate aggressive organ formation in
corallimorpharians, especially during interactions with
dominant competitors which may ®re large numbers of
nematocysts upon contact.
The BMTs of corallimorpharians are similar in form
and function to the inducible catch tentacles of actinian
sea anemones and the sweeper tentacles of scleractinian
corals (reviewed by Williams 1991). Inducible organs
appear to have evolved in each group due to the selective
pressure of interference competition for limited attachment space on hard substrata. That these structures
develop only during active tissue contacts with other
cnidarians, reverting to normal feeding tentacles upon
cessation of contact (Watson and Mariscal 1983;
Langmead and Chadwick-Furman 1999), indicates that
they may be expensive to maintain in terms of limited
polyp resources, and thus are developed by polyps only
when needed.
The cnidom of BMTs in Rhodactis rhodostoma
(Fig. 7) is similar to that of the aggressive organs of
other types of cnidarians, in that they are dominated by
holotrichous nematocysts (reviewed by Bigger 1988).
Penetrating cnidae such as b-mastigophores and holotrichs are thought to function in defensive and/or aggressive interactions among cnidarians (reviewed by
Lang and Chornesky 1990). In contrast, spirocysts (adhesive cnida) are rare or absent in the specialised aggressive organs of cnidarians (reviewed by Bigger 1988;
Lang and Chornesky 1990) and are thought to function
in prey capture and other processes (Mariscal 1974;
Mariscal et al. 1977; Thomason and Brown 1986).
The BMTs of Rhodactis rhodostoma appear to be most
similar to the bulbous tentacles of its Indo-Paci®c
congeners R. (=Discosoma) howesii, R. dawydo
(Ridzwan 1993) and R. indosinensis (A. Chen personal
communication), in that they develop on polyps in contact with stony corals. The bulbous tentacles of R. (= D.)
sanctithomae in the Caribbean also have been shown to
function during aggressive interactions with corals (Miles
1991). The cnidom of BMTs in R. rhodostoma is similar
to that in R. sanctithomae, in that both are dominated by
holotrichs (= homotrichs) (den Hartog 1977; present
paper, Fig. 7). Also in both species, holotrichous nematocysts are signi®cantly larger in the marginal tentacles with acrospheres than in those without (den Hartog
1977; present paper, Tables 2, 3 and Fig. 8). Relatively
large nematocysts also have been found in the inducible
aggressive structures of stony corals: the sweeper tentacles of Montastrea, Favites, Galaxea and Platygyra have
larger nematocysts than do the feeding tentacles from
which they develop (den Hartog 1977; Hidaka et al.
1987). An increase in nematocyst size may function to
augment the lethal e€ect of aggressive organs in cnidarians. The presence of larger nematocysts in aggressive
rather than feeding tentacles suggests that the cnidom is
replaced completely during tentacle development, with
entirely new capsules being manufactured during the
process of aggressive organ formation (Watson and
Mariscal 1983; Hidaka et al. 1987).
The changeover in cnida types that occurs in Rhodactis rhodostoma tentacles (Fig. 7) does not take place
in its congener R. sanctithomae, in which both bulbous
and ®liform marginal tentacles have a similar cnidom,
composed mostly of homotrichs (=holotrichs) (den
Hartog 1977). The ®ve types of nematocysts that were
recorded in the marginal tentacles of R. rhodostoma were
the same as those noted by Carlgren (1938), with two
exceptions. In the present study, no atrichs were found,
and no ectodermal holotrichs were detected by Carlgren
(1938). The convention distinguishing holotrichs from
atrichs is the presence of spines along the nematocyst
thread (Mariscal 1974). In the present study, the spines
of Type 1 holotrichs were visible only at high magni®cation (1000´). Thus, it is likely that the atrichs of
Carlgren (1938) were in fact the Type 1 holotrichs described here (D. Fautin personal communication). Also,
the Type 2 holotrichs found in the present study were
rare in both tentacle types (<1% of the cnidom, Fig. 7),
and thus may have been overlooked by Carlgren (1938).
In conclusion, the bulbous marginal tentacles
(BMTs) of Rhodactis rhodostoma appear to function as
an e€ective mechanism of interference competition, as
evidenced by their ability to damage the tissues of a
variety of benthic cnidarians on coral reefs. BMTs are
likely to be found on polyps of Rhodactis spp. at sites
throughout the Indo-Paci®c region, and to contribute to
the ability of these corallimorpharians to dominate
patches of space in some shallow reef habitats.
488
Acknowledgements We thank the sta€ of the Interuniversity Institute for Marine Science for assistance during the laboratory
studies. We also thank dive buddies A. Balderman, S. Go€redo, E.
Snider and D. Torovezky for assistance during the ®eld work, and
L. Bonner, A. Colorni and B. Colorni for help with the photomicroscopy. W. Allison, D. Glassom, R. Torres and J. Turner provided constructive criticism of the manuscript. This research was
supported by a grant from the European Social Fund to OL and
from the Israeli Science Foundation to NEC-F.
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