Marine Biology 109, 41-51 (1991)
Marine
..................
BiOlOgy
© Springer-Verlag 1991
The ties that bind: inter-clonal cooperation may help
a fragile coral dominate shallow high-energy reefs *' **
E.A. Chornesky
Department of Biology and Stone Harbor Marine Laboratory, Williams Hall, Lehigh University, Bethlehem, Pennsylvania 18015, USA
Date of final manuscript acceptance: December ] 3, 1990. Communicated by J. Grassle, New Brunswick
Abstract. In Belize, shallow fore-reef buttresses are dominated by Agaricia tenuifolia Dana. The ecological importance of this fragile coral in such a high-energy environment may be explained in part by an unusual cooperative
interaction between adjacent clones of A. tenuifolia. The
shallow buttresses are often composed primarily of many
clones of A. tenuifolia growing in close proximity. Surveys conducted at Carrie Bow Cay, Belize, in 1986 and
1987 showed that intraspecific contacts between different
clones are c o m m o n and occur far more frequently than
interspecific encounters with other sessile taxa. In contrast to many other corals, contacts between non-clonemates of A. tenuifolia do not result in competitive interactions, tissue bleaching or death, or significantly altered
patterns of colony growth. Instead, inter-clonal contact
stimulates localized morphological changes in the skeletons of both corals directly beneath the contact interface,
which tend to anchor the two corals against each other,
making them more resistant to breakage and detachment. By mechanically stabilizing clusters of otherwise
fragile corals, these cooperative interactions potentially
enhance the long-term survivorship and hence the fitness
of interacting A. tenuifolia clones.
Introduction
Along the barrier islands of Belize in Central America, a
major topographical feature of shallow fore-reef environments is a series of large well-developed buttresses separated by sand channels (Riitzler and Macintyre 1982). In
contrast to many Caribbean reefs, however, these reef
buttresses are not constructed primarily by massive
corals, such as Montastraea annularis (Ellis & Solander),
whose morphologies can withstand a constant high-energy environment (Goreau ] 959). Instead, the shallow Be* Please address all correspondence to Dr. Chornesky at: Office of
Technology Assessment, U.S. Congress, Washington, D.C. 205108025, USA
** The views expressed here are those of the author and do not
necessarily reflect those of the Office of Technology Assessment
lizean buttresses are dominated by Agaricia tenuifolia
(Riitzler and Macintyre 1982), a relatively fragile coral
which grows in delicate blade-like colonies (Wells 1973,
Cairns 1982).
It is curious that in this wave-swept habitat Agaricia
tenuifolia is among the most abundant corals (Cairns
1982), often forming large mono-specific stands which
spread for distances of meters or more (Fig. 1 A). H o w
does a coral which appears to lack structural fortifications against a high-energy environment achieve such
great local abundances?
In this paper, I describe intraspecific cooperative interactions that may help to mechanically stabilize clusters
of Agaricia tenuifolia colonies and contribute to the ecological importance of this species in shallow reef habitats.
Materials and methods
Study organism
Agaricia tenuifolia Dana colonies usually grow as a series of thin,
bifacial blades (Wells 1973) which secondarily anastomose as they
grow into contact (Fig. 1 B). Growth is directed up and away from
the substratum, and live tissues die back at blade bases. The resulting bare skeletal surfaces are commonly colonized by encrusting
algae and other sessile epibionts. Combined, the two processes of
upward vertical growth and basal tissue death often generate several adjacent colonies (either single coral blades or still-interconnected
groups of blades) that are physiologicallyisolated from one another
but derived from the same initial parent colony and therefore genetically identical That is, the isolated colonies are "clonemates"
which together constitute a "clone".
In this study, color was used as a marker for identifying genetically different clones of Agaricia tenuifolia. Colonies of A. tenuifolia
are often colored by bright animal pigments on the tentacles, oral
disks, and coenosarc. At least 13 distinct "color types" (having
green, pink, orange, or other colors on one or more of the structures
listed above) occurred within the population of A. tenuifolia studied
in 1986 and 1987 on the inner fore reef in front of the Smithsonian
field station at Carrie Bow Cay, Belize (Riitzler and Macintyre
1982).
Three observations suggest that color is a geneticallydetermined
trait in Agarieia wnuifolia and not subject to environmental modification. First, color does not vary over the surface of a colony in
42
E.A. Chornesky: Inter-clonal cooperation in a reef coral
Fig. 1. Agaricia tenuifolia. (A) A typical buttress located at ca. 3 m depth on the inner fore reef of Carrie Bow Cay, Belize. (B) Primary
growth axis of the coral blades is up and away from the substratum. Scale bars=ca. 0.5 m in (A) and ca. 15 cm in (B)
relation to obvious changes in ambient light. Second, known clonemates, identified by continuous normal skeletal connections, are the
same color. Third, different-colored colonies commonly co-occur in
the same habitat, exposed to the same environmental stimuli. Similarly stable phenotypic characters, including color, have been related to underlying genetic differences in other corals such as Porites
compressa Dana (Hunter 1985, Hunter and Kehoe 1986), and color
has been used to characterize distinct behavioral types within populations of the corals Stylophora pistillata (Esper) and Galaxea
fascicularis (Linnaeus) (Rinkevich and Loya 1983 a, Hidaka and
Yamazato 1984, Hidaka 1985 a).
Here, "clone" is used operationally to describe a colony or
group of colonies of one color type, spatially surrounded by conspecifics of different color types, by other coral species, by various
other sessile animals, and/or by bare space. Over time, a clone of
Agaricia tenuifolia can subdivide, with different portions of the
clone eventually becoming spatially isolated from one another.
Consequently, the number of clones (as defined here) probably
overestimates the number of genotypes present. In addition, color
is only one of a myriad of traits likely to vary among true genetic
clones of A. tenuifolia, and different genotypes may have the same
color. Hence, the number of color types within a population is
probably a minimum and conservative estimate of the number of
distinct genotypes present.
Field surveys
To estimate the clonal diversity of the local population of Agaricia
tenuifolia, an in situ survey assessed the number of clones present
per buttress and its relationship to buttress size. Six buttresses of
varying sizes were haphazardly chosen at depths of 3 to 5 m on the
inner fore reef. The curvilinear width and length of each buttress
were measured using a flexible tape marked in 10-cm increments.
Using the criteria outlined above for distinguishing adjacent clones,
the number of clones per buttress and clone color were recorded.
A second field survey examined individual clones of Agaricia
tenuifolia to estimate the frequency and consequences of ongoing
inter-clonal and interspecific interactions, as well as the potential
for future interactions of both types. Fifty-four clones were located
using coordinates derived from a random number table. The following information was recorded for each clone: Inter-clonal: (i) clone
color and size, (ii) number of contracts with non-clonemates and
non-clonemate color, (iii) observable outcome of each of these interclonal contacts, (iv) percent clone perimeter adjacent to, but not
necessarily in contact with, non-clonemates ( = the potential for
future inter-clonal contacts); Interspecific: (v) number of contacts
with sessile animals other than A. tenuifolia, (vi) observable outcomes of each of these interspecific contacts, (vii) percent clone
perimeter adjacent to, but not necessarily in contact with, other
sessile animals ( = the potential for future interspecific contacts).
Description of inter-clonal and intra-clonal contacts
To document the detailed events occurring during inter-clonal interactions, corals with contacts at various stages of development were
collected and examined (n=20). Contacts ranged from instances
where adjacent colonies had only recently grown into contact and
were barely touching to those where well-developed blades were
growing directly against one another along much of their shared
lateral surfaces. The corals were observed at 10 to 50 x while alive
and fully expanded, and then photographed. They were subsequently killed and cleaned, and the contact regions of skeletons were
examined again at 10 to 50 x. These methods were repeated for
intra-clonal contacts (n = 10). Resulting observations of inter- and
intra-clonal contacts were compared.
Photographs of coral interactions in situ were taken with a
housed Nikon FE, 55-mm micro lens, and an underwater strobe.
Close-up photographs of corals following collection were taken
using a Nikon F3 mounted with a close-up bellows and inverted
55-mm micro lens, and illuminated with a pair of strobes.
Results
Clonal diversity
M a n y d i f f e r e n t c l o n e s o f Agaricia tenuifolia u s u a l l y c o n t r i b u t e to t h e d e v e l o p m e n t o f a single r e e f b u t t r e s s . S u r v e y e d b u t t r e s s e s r a n g e d in size f r o m 11.5 to 116.6 m a in
s u r f a c e a r e a , a n d w e r e c o m p o s e d o f f r o m 18 to 92 c l o n e s
r e p r e s e n t i n g f r o m 7 to 13 c o l o r t y p e s (Fig. 2). T h e n u m -
43
E.A. Chornesky: Inter-clonal cooperation in a reef coral
bet of clones per buttress was significantly correlated
with buttress size (Pearson's correlation r=0.91,
P<0.05), as was the number of color types present
(r = 0.91, P < 0.05). Larger buttresses were composed of
more clones representing a larger number of color types.
IO0
A
80'
to
u
m
60.
o
e~
E
40
e-
20
r = .91
0
20
B
¢1
e~
Frequencies of inter-clonal vs interspecific interactions
The potential for interactions between adjacent clones of
Agaricia tenuifolia was great (Fig. 3). On average, each
clone was adjacent to 1.74 (SD = 1.4) other clones of A.
tenuifolia. The mean percentage per clone of perimeter
adjacent to other clones was 28.3% (SD =26.6) (Fig. 3).
Actual contact between blades of different-colored clones
was common. Of the 54 randomly located clones surveyed, most (72%) experienced at least one inter-clonal
contact. The mean number of inter-clonal contacts per
clone was 3.89 (SD=4.56) (Fig. 3).
Inter-clonal interactions occur far more fi'equently for
Agaricia tenuifolia than do interspecific interactions
(Fig. 3). A one-way ANOVA test for differences between
the numbers of contacts per clone involving different
clones versus different species was significant (dfl = 1,
dr2 = 106, F = 29.08, P < 0.001). Similarly, the percentage
of perimeter adjacent to non-clonemates per clone was
significantly greater than the percentage adjacent to different species (dfl =1, df2=106, F=13.23, P<0.001).
For both tests, data were transformed to fulfill the assumptions of ANOVA statistics using in (x+ 1) (Sokal
and Rohlf 1969).
o
Consequences of interspecific contact
e~
10
e~
E
e,.
r= .gl
0
,
r
2o
4o
buttress
=
i
6o
8;
size
,00
,2o
(m 2 )
Fig. 2. Agaricia tenuifolia. Relationships of (A) clone number and
(B) genotype number to buttress size (n = 6). Color types were used
to estimate the number of genotypes present. Significant positive
correlations were found between buttress size and both the number
of clones (r = 0.91) and number of genotypes (r = 0.9 I) present
I0
9
II
All interspecific contacts recorded in this survey involved
either the hydrocoral Millepora sp. or the scleractinian
coral Porites porites (Pallas) (Fig. 4). On average, only
13.6% (SD=23.12) of an Agaricia tenuifolia clone
perimeter was adjacent to either of these other taxa, and
the mean number of interspecific contacts per clone
was 0.43 (SD=0.57) (Fig. 3). Uniformly, contact with
Millepora sp. resulted in the hydrocoral's directly overgrowing A, tenuifolia (Fig. 5 A). In interactions between
A. tenuifolia and P. porites, the Porites tissues adjacent to
A. tenuifolia were damaged (Fig. 5 B). The most likely
mechanism producing this effect is the development and
60
other clones
8
45
7
,--
n(czone$)=
54
6
¢D
es
E
5
¢=
4
30
3
15
2
I
o
number
surrounding
numl3er
OT
contacts
percenL
ui
perimeter
Fig. 3. Agaricia tenuifolia. Frequencies
of inter-clonal vs interspecific interactions for surveyed clones (n = 54). Values shown are mean + 1 SD. Three
measures are given: number of surrounding A. tenuifolia clones or
colonies of other species; number of actual contacts with other clones or other
species; and percentage of a clone's
perimeter adjacent to (but not necessarily in contact with) other clones or
other species
44
E.A. Chornesky: Inter-clonal cooperation in a reef coral
80
i n t e r - clonal
70
interspecific
60
n(contacts) =235
5O
,u 4o
<9
30
20
Fig. 4. Agaricia tenuifolia. Frequencies of different contact types among surveyed clones
(n= 235). Most inter-clonal contacts resulted
in simple contact. Interspecific contact occurred with MiIlepora sp. and Porites porites
I0
simple
contact
fusion
overgrowth
mutual
overgrowth
Millepora s p . P. porites
contact type
Fig. 5. Agaricia tenuifolia. (A) Overgrowth of A. tenuifolia (At) by
Millepora sp. (M). (B) Contracted polyps and damage to Porites
porites (Pp) tissues (arrow) adjacent to the A. tenuifolia (At) was
probably caused by A. tenuifolia sweeper tentacles. Scale bar =ca.
1 cm for both (A) and (B)
deployment of sweeper tentacles by A. tenuifolia. I have
observed expanded sweeper tentacles along margins of
A. tenuifolia colonies adjacent to corals of other species,
including P. porites, Dendrogyra cylindrus Ehrenberg,
and Agaricia agaricites (Linnaeus). It seems likely that
sweeper tentacles on this species develop and are used
during competitive encounters, as in the congeneric coral
A. agaricites (Chornesky 1983).
Consequences of inter-clonal and intra-clonal contact
In contrast to the damage and overgrowth occurring in
interspecific interactions, direct observation of 211 interclonal contacts (Fig. 4) showed the most c o m m o n result
(83%) to be corals simply growing against one another
with no evidence of altered growth or damaged tissues.
This kind of "simple contact" was observed both be-
E.A. Chornesky: Inter-clonal cooperation in a reef coral
45
Fig. 6. Agaricia tenuifolia. Different forms of inter-clonal contact
during naturally occurring interactions. (A) Initial and (B) welldeveloped instances of simple contact with clones growing against
one another. (C) One clone elaborating a small lamellar overgrowth
over another. (D) Fusion betweendifferent-coloredclones (fusion line
lies between the two arrows). Scale bar in (D) =ca. 1 cm for (A-D)
tween clones which had recently grown into proximity
and were barely in contact (Fig. 6 A) and between clones
which had been together for extended periods and had
well-developed contacts along much of their lateral surfaces (Fig. 6B). Based upon considerations of blade
thickness and shape relative to typical growth rates of
Caribbean agariciid corals, such older contacts apparently may persist for periods perhaps as long as years.
Limited overgrowth occurred in 15% of inter-clonal
contacts (Fig. 4). This overgrowth involved foliacious
growth by a thin, unifacial extension of coral blades, and
occurred both in lateral encounters between blades
(Fig. 6 C) and, rarely, at the base of a blade. Limited overgrowth could involve either one blade overgrowing another, or, less frequently, two adjacent blades overgrowing each other. In the latter case, the two blades simultaneously grew against each other on opposite sides of the
double blade: on one side it appeared that one blade was
being overgrown, while on the reverse side it appeared
that the other blade was being overgrown. In both single
and mutual overgrowth, only one side of an overgrown
blade was usually affected. Moreover, overgrowths af-
fected relatively little skeletal surface of either interacting
coral. The maximum linear extent of most overgrowths
was < 1 cm, and in no case was a blade completely overgrown by a different clone. Overgrowth in Agaricia
tenuifolia thus is infrequent, usually involves portions of
corals away from their primary growth axis, and only
extends for very small distances when it does occur. Consequently, limited overgrowth does not appear to function as a strategy for spatial competition in this species.
Fusion, in which the soft tissues and underlying skeletal septo-costae of adjacent corals become continuous,
occurred in 2% of contacts between different-colored
clones (Fig. 4). Corals were scored as fused not only by
external appearance (Fig. 6 D), but also by whether the
tentacles of both adjacent corals contracted when only
one colony was mechanically stimulated. Occasional inter-clonal fusion during grafting experiments has been
previously reported for another agariciid coral, Pavona
cactus (F6rskal) (Willis and Ayre 1985). In addition, I
have observed fusion in Jamaica and Belize between different-colored colonies of Agaricia agaricites in the field
and in Belize between sibling juveniles of A. humilis
E.A. Chornesky:Inter-clonal cooperation in a reef coral
46
Table 1. Agaricia tenuifolia. Percentage of different types of outcomes, for color types and for specificcolor pairs. Mean percentage
_+SD shown
Simple
contact
Per color type (n=13)
Per color pair (n= 14)
Limited
Fusion
overgrowth
79.6+13.8 18.6_+14.4
77.4_+14.9 19.5+_15.2
1.8_+2.8
3.1 -I-6.4
Verrill reared from larvae under laboratory conditions
(unpublished).
The consequences of contact between Agaricia tenuifolia clones (simple contact vs limited overgrowth vs fusion) appeared to be unrelated either to clone color or to
the specific colors of the paired corals among the
211 inter-clonal contacts surveyed. Table 1 shows the
mean percentage of different types of outcomes, both for
color types and for specific color pairs. For each of the 13
color types, simple contact was the most frequent result,
and no color type engaged predominantly in either limited overgrowth or fusion. The 211 inter-clonal contacts
involved 33 different color pairings of A. tenuifolia; for
each color pair in which five or more contacts were observed (n = 14), again, simple contact was the most common outcome, and limited overgrowth and fusion were
rare. These results suggest that limited overgrowth and
fusion occur at some low frequency regardless of the
clonal identities of interacting corals.
The consequences ofinter-clonal contact also were not
related to relative clone size. For 34 contacts in which the
relative sizes of the interacting clones were known, a test
for association between relative clone size (equal or unequal) and contact outcome was not significant (X2 =
0.24, P>0.5, d.f.=2).
In addition, there is no evidence that simple contact is
a temporary phase preceding overgrowth, since both simple contact and limited overgrowth were seen in newly
formed and old contacts between Agaricia tenuifolia
clones. Factors determining whether simple contact or
limited overgrowth occurs may relate more to the angle at
which corals happen to grow into contact (see review of
Lang and Chornesky 1990) than to any real difference in
interaction type.
Separation of inter-clonal contacts at various stages of
development revealed the apparent sequence of events
occurring in these interactions. The initial contact between adjacent colonies is followed by a de-differentiation of polyps of both corals beneath the contact interface (Fig. 7 A). This is accompanied by a distinctive reorganization of the underlying skeletal surface. Characteristic dentations on skeletal septae disappear, and unusual
lateral ridges form between the septae (compare Fig. 7 B
and C). Adjacent skeletons come to interdigitate closely,
and eventually, the live tissues of both corals die beneath
the interface (Fig. 7 D). Once formed, the interdigitating
skeletons make colonies more resistant to lateral sheer
forces. When cleaned skeletons are fitted back together,
they are very resistant to separation by manually applied
lateral pressure. This is not true of unaltered A. tenuifolia
skeletons.
Morphological changes seen in inter-clonal contacts
resemble those which occur during contact between genetically identical blades of Agaricia tenuifolia. Contact
between clonemates results in fusion. However, as in inter-clonal contacts, prior to fusion the adjacent skeletal
surfaces of interacting coral blades reorganize to interdigitate (Fig. 7 E), and tissues overlying the contact surface
regress. Exposed tissues along the border of this contact
interface then fuse, and eventually secrete new skeletal
deposits (Fig. 7 F). Thus, with the exception of soft tissue
fusion and subsequent secondary calcification at the contact border, inter-clonal contacts seem to proceed in the
same way as those between genetically identical clonemates.
Discussion and conclusions
Mechanisms of intraspecific interactions
Reported responses of corals to inter-clonal contact differ among species (Table 2) and may even differ among
various clonal pairings of a given species (Potts 1976,
Rinkevich and Loya 1983 a, Hidaka and Yamazato 1984,
Hidaka 1985 a) (Table 2). Some corals apparently do not
react to encounters with non-clonemates (Hildemann
et al. 1975, Logan 1985). However, most inter-clonal
contacts are characterized by at least an initial soft-tissue
response, involving the formation of a gap between the
soft tissues of the two corals, loss of zooxanthellae, softtissue death adjacent to the contact interface, and/or the
deployment of competitive structures (mesenterial filaments or sweeper tentacles) (Hildemann et al. 1977, 1980,
Jokiel et al. 1983, Neigel and Avise 1983, Rinkevich and
Loya 1983 a, Hidaka and Yamazato 1984, Hidaka 1985 a,
b, Logan 1985, Resing and Ayre 1985, Willis and Ayre
1985). This is often followed by a local enhancement or
alteration of skeletal growth, such as the formation of
"skeletal ridges" (Ports 1976, Hidaka and Yamazato
1984, Hidaka 1985b); infilling between the two corals
(Potts 1976, Willis and Ayre 1985); formation ofholdfast
structures (Collins 1978); or overgrowth (Potts 1976, Bak
and Criens 1982, Willis and Ayre 1985). Prolonged contact between certain non-clonemates of StyIophora pistillata eventually results in the death of one or both interacting corals (Rinkevich and Loya 1983a).
The response of Agaricia tenuifolia colonies to nonclonemates differs notably from these previous descriptions. Results show that the most common outcome is for
colonies of different clones to simply grow against one
another cooperatively (Figs. 4, 6). Polyps below these
contact interfaces de-differentiate, and the underlying
skeletal regions are reorganized into surfaces which interdigitate between adjacent corals and tend to anchor them
against one another (Fig. 7). Only the polyps immediately underlying these contact zones regress. Inter-clonal
contacts in A. tenuifolia are not characterized by the negative reactions seen in many other corals, such as bleaching, soft-tissue death, significantly altered colony growth
patterns, or the deployment of competitive structures adjacent to the contact interface.
E.A. Chornesky: Inter-clonal cooperation in a reef coral
Fig. 7. Agaricia tenuifolia. Events occurring during inter- and intraclonal contact. (A) De-differentiated polyps (d), lacking tentacles
and mouths, underlying the contact interface during initial stages of
an inter-clonal encounter. Arrows (t) and (m) show a normal tentacle and polyp mouth, respectively. (B) Modified skeletal surface
below a contact interface with unusual lateral ridges between septae
(arrow) and lacking dentations on septae. (C) Normal corallites for
comparison. (D) Regressed polyps directly below a contact inter-
47
face; polyps immediateiy adjacent to this contact zone (which now
lacks live tissues) show no evidence of bleaching or other abnormalities. (E) Reorganized skeletal surface beneath an intra-clonal contact interface. (F) Secondary calcification (arrow) that has followed
soft-tissue fusion during an intra-clonal contact. Secondary calcification is limited to the border of the contact zone that, although
now lacking live coral tissue, is darkly colored due to endolithic
algae. Scale bar in (C)=ca. 0.5 cm for ( A - F )
48
E.A. Chornesky: Inter-clonal cooperation in a reef coral
Table 2. Reported consequences of inter-clonal contact for scleractinian corals from studies where clonal relationships are known or can
be reasonably inferred from considerations of distance or phenotype
Family
Species
Consequences of inter-clonal contact
Source
Formation of a gap between live tissues of the two corals
Soft tissue death of all or part of coral
Translocation of photosynthetically derived metabolites between the two corals
Growth of a skeletal ridge between the corals
Altered growth and reproducton
Rinkevich and Loya (1983 a, b,
1985), Resing and Ayre (1985)
Formation of a gap between live tissues of the two corals
Fusion
Resing and Ayre (1985)
Fusion
Bleaching adjacent to contact interface
Soft tissue death of one coral adjacent to contact interface
Growth of a "skeletal ridge" between the two corals
Hidaka (1985b)
Hidaka (1985b)
Madracis mirabilis
No reaction
"Tissue avoidance"
Logan (1985)
M. decactis
No reaction
"Tissue avoidance"
Logan (1985)
Cementation of the corals to one another accompanied by formation of a
gap between their soft tissues and, sometimes, by bleaching, anomalous
growth, and incomplete polyp development adjacent to the interface
Neigel and Avise (1983)
A. .formosa
Failure to grow into contact
Fusion when in contact
Locally enhanced growth by both corals giving rise to "pads" of tissuecovered skeleton resembling holdfast regions
Hildeman et al. (1975), Collins
(1978)
A. palifera
Locally enhanced growth by both corals filling the space between them, often
eventually forming a skeletal ridge along contact interface
Overgrowth of one coral by the other
Potts (1976)
A. palmata
Overgrowth of one coral by the other; overgrowing edge white and devoid
of calices
Bak and Criens (1982)
Montipora verrucosa
Bleaching followed by soft tissue death of one or both coral along the contact
interface
Bleaching, followed by tissue swelling, then mutual soft-tissue death adjacent
to the contact interface
Fusion
"Graft rejection"
Hildeman et al. (1977, 1980),
Jokiel et al. (1983), Heyward
and Stoddart (1985)
M. dilata
Bleaching, followed by tissue swelling, then mutual soft-tissue death adjacent
to the contact interface
Fusion
"Graft rejection"
Jokiel et al. (1983), Heyward
and Stoddart (1985)
Only below contact zone, polyps de-differentiate, skeletons reform to interdigitate, then overlying polyps regress (contact regions can involve limited
overgrowths up to 1 cm)
Fusion
Present study
Soft tissue death of one or both corals adjacent to the contact interface,
followed by either mutual infilling or overgrowth of one coral by the other
Fusion
Willis and Ayre (1985)
N o reaction
Hildeman et al. (1975)
Pocilloporidae
Stylophora pistillata
Seriatopora hystrix
Pocillopora damicornis
Juveniles
Adults
Acroporidae
Acropora cervicornis
Agariciidae
Agarieia tenuifolia
Pavona cactus
Fungiidae
Fungia fungites
Corals move away from one another
Portitidae
Porites andrewsii
Failure to grow into contact
Fusion when in contact
Hildeman et al. (1975)
E.A. Chornesky: Inter-clonal cooperation in a reef coral
49
Table 2. (continued)
Family
Species
Consequences of inter-clonal contact
Source
P. compressa
Bleaching, followed by tissue death and the development of a shallow groove
between the two corals. Sometimes followed by partial overgrowth of one
coral by the other
Hunter (1985), Hunter and
Kehoe (1986)
P. cylindrica
Formation of a gap between live tissues of the two corals
Fusion
Resing and Ayre (1985)
P, nigrescens
Formation of a gap between live tissues of the two corals
Fusion
Resing and Ayre (1985)
Galaxea fascicularis
Formation of a gap between live tissues of the two corals
Growth of a skeletal ridge between the two corals
Development of sweeper tentacles by both corals, with subsequent injury to
one coral
Development of sweeper tentacles by both corals, with subsequent injury to
neither coral
Hidaka and Yamazato (1984)
Montastraea annular~
Extracoelenteric digestion of one coral by the other
Bleaching, followed by localized soft-tissue death, then extracoelenteric digestion
Dustan (personal communication) in Lang (1973), Logan
(1985)
No reaction
Logan (1985)
Faviidae
Oculinidae
Oculina diffusa
Fusion between the skeletons and overlying soft tissues of different coral clones has been reported during
experimental grafts (Hildemann et al. 1975, Heyward
and Stoddart 1985, Logan 1985, Resing and Ayre 1985,
Willis and Ayre 1985) or between newly settled juveniles
(Hidaka 1985a, Chornesky unpublished). In addition,
fusion in nature has been seen occasionally in the solitary
coral Scolymia cubensis (Milne Edwards & Haime) (Lang
1971, Logan 1985). In this study, 2% of naturally occurring contacts between different-colored clones of Agaricia tenuifolia resulted in skeletal and soft-tissue fusion.
This kind of true fusion between non-clonemates (not
"chimeras" as in Rinkevich and Weissman 1987) is generally considered to reflect the limits of the immune recognition system due to genetic or environmental constraints
(Heyward and Stoddart 1985, Resing and Ayre 1985,
Stoddart et al. 1985, Willis and Ayre 1985).
Ecological significance
The ecological and evolutionary importance of any process depends on its frequency in nature. Inter-clonal contact is a predictable and c o m m o n event for clones of
Agaricia tenuifolia (Fig. 3). Thus, if such contacts influence the growth or survivorship of A. tenuifolia clones,
they may, summed over a clone's lifetime, have significant effects on clone fitness.
For Agaricia tenuifolia, inter-clonal contact results in
skeletal reorganization into interdigitating structures
that potentially confer an increased resistance to breakage, since two blades growing against one another should
require greater force to break than one blade alone
(Wainwright et al. 1976). In addition, the ability of an
individual colony of Agaricia tenuifolia to resist breakage
or detachment by wave action may depend on its being
part of a continuous stand of this species (Fig. 1 A).
Specifically, the honeycomb of A. tenuifolia over a buttress may dissipate the energy in incident water masses by
dividing them into thousands of small eddies between
adjacent coral blades, similar to the way in which branches dissipate the momentum of water passing through arborescent corals (Chamberlain and Graus 1975, Jokiel
1978). Consequently, a colony adjacent to a bare gap will
be subject to greater incident force than one adjacent to
another colony of A. tenuifolia. Moreover, this force will
be applied not only to the coral's living portions, but also
to the dead bases of blades which are usually heavily
bored and more breakable (Tunnicliffe 1978). These vulnerable lower regions would be protected if an adjacent
coral were present. Overall, both by increasing resistance
to breakage and by decreasing exposure to wave forces,
binding contacts between different clones of A. tenuifolia
should increase the stability and survivorship of interacting corals.
Several advantages may be associated with decreased
coral breakage and detachment. First, loosened fragments of Agaricia tenuifolia can abrade both the fragments' own tissues and those of adjacent clones as they
rock among attached blades in the tidal surge (own observations). Second, dead pieces of A. tenuifolia skeletons
commonly found in sand channels between buttresses
(own observations) suggest that detached blades are often transported laterally to inhospitable habitats where
they die. Third, in addition to decreasing the likelihood
that fragments are generated, binding contacts between
A. tenuifolia clones may increase the survivorship of such
fragments once they are formed, by stabilizing them
against adjacent clones. Bak and Criens (1982) have
50
suggested that both intraspecific and intrageneric overgrowth m a y stabilize and enhance the survival of loose
fragments in Caribbean Aeropora spp.
Finally, binding between adjacent clones potentially
enhances the stability of the buttress framework. Similar
effects have been attributed to fusion in Acropora cervicornis (Lamarck) (Gilmore and Hall 1976) and to the
effects of reef-dwelling sponges (Wulff and Buss 1979).
Stable buttresses should grow more rapidly and achieve
larger sizes because they are less susceptible to storm
damage. This, in turn, should enhance the survivorship
and growth of resident Agaricia tenuifolia clones. Interclonal interactions in A. tenuifolia thus m a y ultimately
have an indirect positive effect on clone fitness by contributing to overall buttress stability and growth.
Studies of inter-clonal interactions have generally focused on how corals react to one another (Hildemann
et al. 1975, 1977, 1980, H i d a k a and Yamazato 1984, Hidaka 1985 a, b, Logan 1985) and on the potential utility
of these reactions in assaying the genetic structure of
coral populations (Bak and Criens 1982, Jokiel etal.
1983, Neigel and Avise 1983, Heyward and Stoddart
1985, Resing and Ayre 1985, Willis and Ayre 1985). When
the ecological significance of such interactions has been
addressed, they are generally considered to be a form of
competition for space (but see Rinkevich and Weissman
1987), either because some interacting corals are clearly
damaged (Rinkevich and Loya 1983a) or because the
relative abundance of certain clones is correlated with
their ability to overgrow conspecifics (Potts 1976, Willis
and Ayre 1985).
In contrast, contacts between clones of Agaricia
tenufolia apparently are not competitive because they
involve few of the costs usually associated with competitive interactions between corals (Chornesky 1984, 1989).
F o r example, in other species, competing corals commonly lose polyps when wounded or overgrown by adjacent corals and m a y have their future growth constrained
by neighboring corals (see review of Lang and Chornesky
1990). In contrast, polyp loss in A. tenuifolia is limited
to a relatively small portion of the colony surface directly
beneath the contact interface. Moreover, this minute injury occurs exclusively along lateral or basal colony
edges, away from the plane of m a x i m u m growth for this
species. In addition, the minor skeletal reorganization
involved in these inter-clonal contacts probably requires
only a limited allocation of colony resources. Inter-clonal
encounters do not involve any energetic investment into
either the development of specialized soft tissue structures or significantly enhanced local skeletal growth. F o r
example, although A. tenuifolia is capable of deploying
sweeper tentacles during interspecific competitive interactions, I have seen no evidence that colonies do so during inter-clonal contacts, as has been shown for Galaxea
fascicularis (Hidaka and Yamazato 1984, H i d a k a 1985 a).
Comparison of the positive and negative consequences of inter-clonal contacts for Agaricia tenuifolia
suggests that long-term survival benefits exceed the potential cost of a small and localized polyp loss. Consequently, such interactions appear effectively to be cooperative rather than competitive, involving a minimum
E.A. Chornesky: Inter-clonal cooperation in a reef coral
cost while enhancing the fitness of both interacting corals
by decreasing their susceptibility to breakage and detachment and increasing their mechanical stability.
Acknowledgements. I thank C. Wahle, S. Cairns, J. Lang, A. Levite,
I. Macintyre, E. Peters and an anonymous reviewer for helpful
discussion or comments on the manuscript, K. Riitzler and K.
Sandved for advice concerning microphotography techniques, and
T. Totah for field assistance and for preparing the figures for publication. Contribution no. 305 of the Caribbean Coral Reef Ecosystems program of the Smithsonian Institution; funded in part by
Exxon Corporation.
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