B. Riegl Vertical versus horizontal growth

Int J Earth Sci (Geol Rundsch) (2003) 92:511–519
DOI 10.1007/s00531-003-0317-z
ORIGINAL PAPER
W. E. Piller · B. Riegl
Vertical versus horizontal growth strategies
of coral frameworks (Tulamben, Bali, Indonesia)
Received: 5 April 2002 / Accepted: 1 December 2002 / Published online: 16 April 2003
Springer-Verlag 2003
Abstract Two different coral framework structures located in a shallow subtidal area on the east coast of Bali
are described in this study. One structure is a typical coral
carpet with a distinct internal succession of coral taxa and
growth forms. It starts with a variety of coral species
exhibiting massive, tabular, branching, and platy growth
forms settling on volcanic boulders and cobbles. The
main body of the coral carpet is composed almost
monospecifically of Acropora cf. vaughani, which has
filled all accommodating spaces up to the low-water sea
level. Mostof this carpet died during the bleaching event
of 1998 and the resultant dead Acropora framework is
now capped by a platy Montipora assemblage. Some of
the Acropora branches within the dead carpet, however,
are still alive and display active growth. The Montipora
cover protects the dead Acropora framework against
mechanical and biological destruction. The few still
growing Acropora branches may also contribute to the
strength of the framework. The second coral framework is
made up almost monogenerically of Montipora. One
species of Montipora is of a laminar growth form and
produces whorl-like colonies. Within this framework,
only part of the Montipora colonies are dead; however,
these are intensively fragmented. The fragments have
been rapidly settled by a platy Montipora species, which
has stabilized the fragments. In this case, the fragment
shedding of the Montipora offers the opportunity for
progradation of the framework on these fragments.
Concerning the Acropora carpet, similar examples from
the fossil record of the Miocene era of Spain and Austria
have been reported.
W. E. Piller ())
Institut fr Geologie und Palontologie,
Universitt Graz,
Heinrichstrasse 26, 8010 Graz, Austria
e-mail: [email protected]
B. Riegl
National Coral Reef Institute, Oceanographic Center,
Nova Southeastern University,
8000 N. Ocean Drive, Dania, FL, 33004, USA
Keywords Coral ecology · Coral carpet · Acropora
thicket · Montipora framework · Actuopaleontology · Bali
Introduction
On the east coast of Bali, near Tulamben, no true coral
reefs have formed. Since the area is rich in corals and
exhibits flourishing coral growth on rocks, one of the
reasons for the absence of reefs is likely due to repeated
disturbance by lava-flows emanating from Mount Gunung
Agung. In protected bays, however, a dense cover of coral
frameworks is found on volcanic substrate. Most of these
dense coral stands were heavily affected by the bleaching
event caused by the 1997–1998 El Nio Southern
Oscillation (Wilkinson 2000) and died. This event has
offered the opportunity to investigate these dead frameworks by excavating parts of it and studying their internal
composition and successions. These studies may provide
insight into the growth of modern non-reef coral frame
stones, offering the possibility of developing models for
fossil counterparts.
Study area
The study area is located at the E–NE corner of Bali
(Indonesia), a few hundred meters east of the village of
Tulamben (see Fig. 1). The particular study sites are
located immediately in front of a Hindu Temple (see
Fig. 1) and are easily accessible from the shore. The
coastal area is covered by a lava flow which has been
reworked along the beach forming coarse volcanic
boulders and cobbles. A few to several tens of meters
off the coast, the shallow water area is densely settled by
scleractinian corals growing from a depth of 1–3 m up to
the surface of the water. The little embayment directly in
front of the temple is framed by two old lava flows that
emanated from Mount Gunung Agung, reaching the sea in
1963 (local oral tradition and Ruddiman 2001, p. 379).
The solidified lava formed steep sea cliffs of 2–10 m in
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Fig. 1A, B General location of
the study area. C Detail of the
area around Tulamben. D Location of the two study sites
(circles) east of Tulamben with
bathymetry. Light-gray shaded
areas in C and D represent
abundant coral growth (C and D
after Pickell and Siagian 2000)
height (cf. Pickell and Siagian 2000). The bay is densely
covered by a coral thicket predominantly made up of
branching Acropora colonies. Adjacent to the eastern
section, the neighboring bay is densely settled by
foliaceous Montipora colonies. This area is not as densely
covered as that of the Acropora thickets. The gullies
between the Montipora areas have not been settled by
corals, and the Montipora forms clusters of up to several
hundreds of square meters in size. Both Acropora and
Montipora thickets have attained a thickness of more than
1 m.
Materials and methods
The area was documented by photographic transects starting at the
coast and moving seawards. After an intense survey, two sites
within dense Acropora thickets were selected. Here, two trenches
were excavated using a pickaxe, hammer and shovel in order to
study the growth successions from the substratum up to the surface
of the coral thicket. Detailed measuring in the field was followed by
both a thin-sectioning of the corals and overgrowing organisms, as
well as further measurements taken with a light and electron
microscope.
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Results
Acropora thickets
The Acropora-dominated thickets exhibit dense growth
and cover an area of several thousands of square meters,
which is only interrupted in some places. The thickness of
approximately 80 cm, is relatively uniform, increasing
slightly, however, just offshore from the beach. Generally, the upper surface is relatively flat in correlation to the
low-water sea level.
Vertical succession in Acropora thickets
The excavations of the two trenches within the thicket
display a clear succession of corals that are similar in both
examples (see Fig. 2).
The base
The base of the thicket is formed by a substratum of
volcanic boulders and pebbles. These represent fragments
of the lava rocks which, because the bay is open to the
east and thus exposed to winter storms, have become
rounded due to frequent mobilization caused by wave
action. This mobilization among the larger components
has caused sand and gravel of a volcanic material to
occur.
Initiation to termination sequence
The basal sequence in the excavated framework shows a
combination of massive, tabular, branching, and encrusting corals in direct contact with the volcanic cobbles and
pebbles (see Figs. 2 and 3). The species found to encrust
individual rocks were faviids and most frequently, Favites
pentagona. Acropora palifera was found to encrust
several cobbles with the same colony, thus leading to a
binding of these cobbles and a stabilization of the
substratum. Acropora cf. hyacinthus was found to first
attach to a single cobble and then to overtop several
others. While the tabular species did not actively bind
several cobbles, as did the Acropora palifera, which has a
broader encrusting base, the overshadowing of several
cobbles nevertheless sheltered them from wave action and
stabilized them.
Acropora cf. vaughani, which forms the framework of
the thicket (see Fig. 4), started to grow simultaneously
with the other basal corals, and, somewhat later, even
grew on some of them, particularly on the platy ones.
Later on, this species had overgrown and buried all the
corals of the initial assemblage. At an early stage, such
frameworks are still low and punctuated in many areas by
large boulders, which have the potential of becoming
mobile in heavy seas, thus having the capacity to destroy
the frameworks. As the Acropora thicket grows, these
Fig. 2 Schematic drawing of internal succession of the Acroproa
carpet
boulders become more and more enveloped until they are
totally covered and stabilized.
This dense thicket forms a more or less continuous
coral framework of up to a thickness of 0.8–1 m . Viewed
from the outer surface and from the excavated lateral
surfaces, this framework is composed of corals that are
apparently dead. Approximately 20 cm of the uppermost
portion of the Acropora branches is intensively encrusted
with coralline algae. In a few places, however, several
live branch tips were found inside the dead and encrusted
framework of Acropora cf. vaughani (Riegl and Piller
2001). These live tissues mostly occurred approximately
10 cm below the upper surface of the frame and, as
ascertained by visual assessment, were of normal color
and vitality. The branchlets observed were primarily
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Fig. 3 Initial association of the Acropora carpet. A General view of
the excavated trench with volcanic boulders at the base and small
branching Acropra in between, a crustose coral layer on the
boulders, and branching Acropora cf. vaughani thicket. B Basal
volcanic pebbles encrusted by faviids, which are overgrown by a
laminar coral colony and the Acropora cf. vaughani thicket. C
Detail of B showing the crustose and massive faviid species. D
Small branching Pocillopora verrucosa, Acropora palifera and
Favites pentagona form the very base
oriented laterally, since upward growth was blocked by
competing branches of the same colony (Riegl and Piller
2001).
The surface of the dead Acropora framework was
covered by laterally continuous colonies of platy Mon-
tipora (see Figs. 2, 4). These Montipora colonies grew on
the tips of the Acropora cf. vaughani branches, bridging
the space between branches and providing rigidity and
protection for the dead framework (see Fig. 4). In places,
the Montipora did not only cover and bridge the Acropora
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Fig. 4 A Top part of the Acropora cf. vaughani thicket overgrown by encrusting Montipora with protuberances. B Top view of the
Acropora carpet with the cover of encrusting Montipora. C Detail of top of the encrusting Montipora with short protrusions
branches, but also the branch tips of the Acropora were
encrusted for a few centimeters. Besides these protrusions, resulting from the encrustation of the Acropora
branches underneath, the upper surface of the Montipora
cover exhibited vertically arranged short branches (sensu
Veron 2000) of a few centimeters in length (see Fig. 4C).
Individual platy Montipora colonies did not fuse laterally
(see Fig. 4B).
In depressions and gullies within the thicket and
surrounding areas, relatively little Acropora rubble was
found. Only the immediate margin of the thickets
exhibited minor amounts of shed rubble.
Horizontal succession (landward–seaward)
The beaches in the Tulamben area are made up of coarse
black sand covered by rounded lava pebbles and cobbles
(see Fig. 5A, B). On these coarse volcanics between the
beach and the Acropora thicket described above, a coral
association similar to the initiation assemblage at the base
of the thicket was found. Cobbles and boulders were
primarily encrusted with faviids that rarely overgrew
more than one cobble and thus generally did not lead to
binding of the substratum. Frequently, however, acrop-
orid, pocilloporid and montiporid colonies settled in the
fissures in between adjacent boulders and then encrusted
both boulders with their basal plates, further stabilizing
the boulders with their upward growing branches wedged
into free spaces (see Fig. 5). Later, many colonies grew
big enough to envelop the boulders and thus began to
stabilize them. Finally, Acropora growth became denser,
representing the beginning of the thicket (see Fig. 5C).
Montipora frameworks
In the slightly more sheltered bay east of the Acropora
thicket a framework of densely spaced, laminar Montipora colonies of whorl-like growth were found (see
Fig. 6A). The total coverage of this framework was
several thousands of square meters, with a thickness of
about 1 m in the portions that were better developed.
Although no excavations were carried out (due to a
generally high concentration of living colonies), in
adjacent areas, Montipora was seen encrusting over
several cobbles or boulders, forming whorls in the
fissures between the cobbles. Although this particular
Montipora area had suffered less mortality than the
Acropora thicket nearby, and about half of the framework
516
fragments were not transported any further and remained
angular and unrounded. The talus and the rubble beds in
between the colonies were densely settled by the
encrusting Montipora species which overgrew the surfaces of the dead Acropora framework. Thus, the
Montipora rubble layers were stabilized by the binding
activity of another encrusting Montipora species (see
Fig. 6C). In addition to stabilization, the encrustation
prevented further destruction via bioerosion and offered
the opportunity for the Montipora to prograde over its
own fragments (see Fig. 6C).
Discussion
Acropora thicket
Fig. 5 Pioneer coral associations along the shore. A Initial
encrustation of volcanic pebbles by numerous faviids and small
Acropora colonies between the pebbles. B Small Acropora and
faviids between volcanic pebbles. C Initial Acropora thicket
already covering most of the volcanic components
was still alive, there were enough dead colonies to allow
for a significant disintegration of skeletal material to take
place. The Montipora colonies tended to break into
shingle-like fragments filling the free spaces in between
the colonies and, where no free space was available,
forming a talus in front of the framework (see Fig. 6B, C).
Except for this shedding into the talus, the Montipora
The vertical succession within the thicket and the
composition of coral assemblages between the beach
and the thicket represent a good example of Walther’s
law: the basal coral assemblage in the thicket (a mixture
of massive, tabular, branching, and platy corals), and the
assemblage between the beach and the thicket are the
same and represent a pioneer coral association. Some of
the corals were able to overgrow adjacent volcanic
boulders and pebbles (e. g., Acropora palifera), others
grew on a single boulder but overshadowed several
adjacent blocks. Both growth strategies offer protection
against damage by hydrodynamic energy and also stabilize the substratum. This stabilization makes the upward
growth of dense Acropora cf. vaughani possible. Dense
upward growth of Acropora cf. vaughani can only be
observed in some of the more protected parts of the
coastal strip. The reason for this is believed to be wave
energy, which is, at least during winter storms, too high to
allow for long-lasting colonization. A few tens of meters
from the beach, at a depth of only 1–2 m, the energy level
seems to already be favorable for permanent and upward
coral growth. These corals cover wide areas reaching the
neap tide sea level, and therefore are a good example of
catch-up coral frameworks (Neumann and Macintyre
1985).
Since this dense thicket had caught up to the water
level, it was exposed to high temperatures and irradiance
levels and, as a consequence, had become almost entirely
bleached to death during the positive sea-surface temperature anomaly associated with the unusually strong El
Nio Southern Oscillation of 1997–1998(Schaffelner,
personal communication). The dead tips of this Acropora
were quickly and intensively encrusted with coralline red
algae followed by settlement and coverage by platy
Montipora. These platy corals served to cap the upper
surface of the framework and, by keeping bioeroders
away and accreting actively, helped to maintain the
integrity of the largely dead Acropora framework.
Despite the encrustation and shading by the coverage,
several live and flourishing branch tips of Acropora cf.
vaughani were still found. This indicates three strategies
followed by the coral. While in healthy colonies most live
517
Fig. 6 Montipora carpet. A Detail of the laminar Montipora
species forming upright whorls. B Margin of Montipora carpet with
talus of Montipora fragments. C Detail of a Montipora carpet
margin with the main frame of the laminar Montipora species and
the fragment-talus colonized by encrusting Montipora species with
protrusions
tissue is concentrated in the uppermost layer of the
framework closest to light, at least some cryptic tissue
remains intact after the surface of the thicket dies off.
These cryptic branches may provide a nucleus for the
recovery and resettlement of the surface by re-growth
from below. Even if these cryptic branches are unable to
reach the surface again, their further growth and production of new branchlets will continue to fill free spaces
inside the framework. This may help to increase the
density, mechanical stability and, consequently, the
longevity of the framework.
From a more geological perspective, different aspects
of this Acropora thickets may be considered to be
important:
– The distinct internal zonation within the thicket (from
more robust at the base to branching growth forms
above) might be interpreted as a record of changing
energy conditions. However, the robust initiation
assemblage stabilizes the volcanic pebbles, which is
a prerequisite for the establishment of a branching
thicket.
– If only seen in outcrop, the succession observed here at
the top part of the thicket (platy corals covering a
518
branching thicket) could be interpreted to suggest a
deepening of the environment, since platy growth is
often interpreted as a typical low -light adaptation
(e.g., McCall et al. 1994; Schuster and Wielandt 1999).
In reality, the mechanism leading to this succession is
nearly the opposite: full utilization of accomodating
spaces by Acropora cf. vaughani reflects a catch-up
scenario. Subsequently, what happens is the death of
the Acropora thicket due to the encrustation of
coralline algae and bleaching, followed finally by
settlement by—better adapted or opportunistic (?)—
platy Montipora.
– Due to capping by the Montipora, the branched
Acropora-framework is protected against biological
and physical destruction; and because of the cryptic,
still living Acropora branches, the framework may
even gain additional strength due to further internal
growth. Both aspects are a clear indication that this
framework, although affected by heavy winter storms
with waves of several meters height, may remain
cohesive even after it has died (Schaffelner, personal
communication). This is supported by low amounts of
Acropora rubble in and around the thickets, which
indicates that individual broken Acropora skeletons do
not live long among volcanic cobbles. When these
move during storms, they grind the softer carbonate
rubble to sand.
Terminologically the described structures may be
called a coral thicket, coral carpet, or incipient reef.
Since we cannot predict future evolution of the structure,
the term coral carpet is preferred (Riegl and Piller 2000a).
In the geological record, coral carpets are classified with
biostromes, particularly as autobiostromes (Kershaw
1994; Sanderstrm and Kershaw 2002). The Acropora
structures studied are therefore an excellent example of a
modern coral carpet as already recorded in a few other
places within different reef provinces (e.g., Red Sea:
Piller and Pervesler 1989; Riegl and Piller 1997, 1999,
2000a; Arabian Gulf: Riegl 1999; Caribbean: Geister
1983; Miller et al. 2001). Since coral studies of the
Cenozoic usually focus on reefs sensu stricto (bioherms),
neither modern nor ancient coral carpets are well
documented. The modern example described, however,
matches the description of fossil coral carpets from the
Miocene very well. Other good examples come from the
Tortonian (Upper Miocene) of southeastern (Almanzora
corridor: Martin et al. 1989) and southern Spain (Granada
Basin: Braga et al. 1990). In these examples (called reefs
by Martin et al. 1989 and Braga et al. 1990), several
cycles of frameworks have developed in which corals
started to grow on coarse clastics (deltaic conglomerates)
and exhibit an internal succession (from Porites to
Tarbellastrea). These cycles are interpreted as being the
result of ecological successions, and colonization by
Tarbellastrea was only possible after the stabilization of
the substratum by Porites (Martin et al. 1989). From the
Middle Miocene Leitha Limestone of Austria (Central
Paratethys), Riegl and Piller (2000b) report several types
of coral carpets (biostromes). In one of these coral carpets
the authors relate the internal succession (corals and
encrusting red algae) to ecological disturbances, e.g.,
mortality events. Also, in this fossil case, no breakdown
of the framework occurred due to either encrustation of
branching corals by algae and capping of the whole
structure by encrusting corals (Riegl and Piller 2000b).
Montipora frameworks
The growth form of the framework building Montipora is
very open and the platy skeleton is thin and fragile. Since
part of the framework had died and no distinct encrustation by other organisms was observed, this led to rapid
disintegration and fragmentation by wave action and
bioerosion. Open areas between Montipora colonies and
the surrounding areas were covered by a thick talus of
these fragments, which remained angular and unrounded.
Therefore stabilization had to occur rapidly after fragment
shedding. This means that colonization of the fragments
by platy Montipora was fast. The importance of this
capping sequence is stabilization and defense against
intense bioerosion that could otherwise remove the
framework and talus. By forming the dense rubble talus,
stabilized by subsequent encrustation, the Montipora
framework is an example of progradation by fragmentshedding. This means that fragmentation and shedding of
one Montipora species produces substrate for settlement
and encrustation by another Montipora species. In doing
so, this mechanism favors and speeds up lateral growth of
the framework, which may again be classified as a coral
carpet. From a geological perspective, contrary to the
Acropora carpet, most of this carpet may be preserved as
a bed of densely packed Montipora fragments with
encrusting Montipora, probably in situ, in between. In
terms of Kershaw’s biostrome classification (1994), this
type would by classified as autoparabiostrome or even as
parabiostrome, although disruption of coral does not
necessarily relate to storm activity.
Acknowledgements This study was funded by the Austrian
Science Foundation via grant P-13165-GEO. We thank Josef
Schaffelner (Vienna/Tulamben) for introducing us to the area of
Tulamben, and for providing all his detailed knowledge of the area
as well as his excellent underwater photographs of the area before,
during and after the bleaching event of 1998. Thanks go also to
Rachel Wood (Cambridge, U.K.) and Juan C. Braga (Granada) for
providing constructive reviews.
References
Braga JC, Martin JM, Alcala B (1990) Coral reefs in coarseterrigenous sedimentary environments (Upper Tortonian,
Granada Basin, southern Spain). Sediment Geol 66:135–150
Geister J (1983) Holozne westindische Korallenriffe: Geomorphologie, kologie und Fazies. Facies 9:173–284
Kershaw S (1994) Classification and geological significance of
biostromes. Facies 31:81–92
Martin JM, Braga, JC, Rivas P (1989) Coral successions in Upper
Tortonian reefs in SE Spain. Lethaia 22:271–286
519
McCall J, Rosen B, Darrell J (1994) Carbonate deposition in
accretionary prism settings: Early Miocene coral limestones
and corals of the Makran Mountain Range in Southern Iran.
Facies 31:141–178
Miller SL, Chiappone M, Swanson DW, Ault JS, Smith SG,
Meester GA, Luo J, Franklin EC (2001) An extensive deep reef
terrace on the Tortugas Bank, Florida Keys National Marine
Sanctuary. Coral Reefs 20:299–300
Neumann AC, Macintyre IG (1985) Reef response to sea-level rise:
keep-up, catch-up, or give-up. Proceedings of the 5th International Coral Reef Symposium, Tahiti 3:105–110
Pickell D, Siagian W (2000) Diving Bali. The underwater jewel of
southeast Asia. Periplus, Singapore, pp 1–223
Piller WE, Pervesler P (1989) The Northern Bay of Safaga (Red
Sea, Egypt): an actuopalaeontological approach. 1.Topography
and Bottom facies. Beitr Palontol sterr 15:103–147
Riegl B (1999) Coral in a non-reef setting in the southern Arabian
Gulf (Dubai, UAE): fauna and community structure in response
to recurring mass mortality. Coral Reefs 18:63–74
Riegl B, Piller WE (1997) Distribution and environmental control
of coral assemblages in Northern Safaga Bay (Red Sea, Egypt).
Facies 36:141–162
Riegl B, Piller WE (1999) Coral frameworks revisited—reefs and
coral carpets in the northern Red Sea. Coral Reefs 18:241–253
Riegl B, Piller WE (2000a) Reefs and coral carpets in the northern
Red Sea as models for organism-environment feedback in coral
communities and its reflection in growth fabrics. In: Insalaco E,
Skelton PW, Palmer TJ (eds) Carbonate Platform Systems:
components and interactions. Geol Soc Lond Spec Publ
178:71–88
Riegl B, Piller WE (2000b) Biostromal Coral Facies—A Miocene
example from the Leitha Limestone (Austria) and its Actualistic Interpretation. Palaios 15:399–413
Riegl B, Piller WE (2001) “Cryptic” tissues inside Acropora
frameworks (Indonesia): a mechanism to enhance tissue
survival in hard times while also increasing framework density.
Coral Reefs 20:67–68
Ruddiman WF (2001) Earth’s climate: past and future. WH
Freeman, New York, pp 1-465
Sanderstrm O, Kershaw S (2002) Ludlow (Silurian) stromatoporoid biostromes from Gotland, Sweden: facies, depositional
models and modern analogues. Sedimentology 49:379–395
Schuster F, Wielandt U (1999) Oligocene and Early Miocene coral
faunas from Iran: palaeoecology and palaeobiogeography. Int J
Earth Sci 88:571–581
Veron JEN (2000) Corals of the world, vol 1. Aust Inst Mar Sci,
Townsville, pp 1-463
Wilkinson C (2000) Status of the coral reefs of the world: 2000.
Aust Inst Mar Sci, Townsville, pp 1-363