Self-generated morphology in lagoon

reefs
David Blakeway1,∗ and Michael G. Hamblin2
1 School of Earth and Environment, University of Western Australia, Crawley, Western Australia,

Australia
2 School of Mechanical and Chemical Engineering, University of Western Australia, Crawley,

Western Australia, Australia

∗
Current affiliation: Fathom 5 Marine Research, Lathlain, Western Australia, Australia

ABSTRACT
The three-dimensional form of a coral reef develops through interactions and
feedbacks between its constituent organisms and their environment. Reef morphol-
ogy therefore contains a potential wealth of ecological information, accessible if the
relationships between morphology and ecology can be decoded. Traditionally, reef
morphology has been attributed to external controls such as substrate topography
or hydrodynamic influences. Little is known about inherent reef morphology in the
absence of external control. Here we use reef growth simulations, based on observa-
tions in the cellular reefs of Western Australia’s Houtman Abrolhos Islands, to show
that reef morphology is fundamentally determined by the mechanical behaviour of
the reef-building organisms themselves—specifically their tendency to either remain
in place or to collapse. Reef-building organisms that tend to remain in place, such
as massive and encrusting corals or coralline algae, produce nodular reefs, whereas
those that tend to collapse, such as branching Acropora, produce cellular reefs. The
purest reef growth forms arise in sheltered lagoons dominated by a single type of
reef builder, as in the branching Acropora-dominated lagoons of the Abrolhos. In
these situations reef morphology can be considered a phenotype of the predominant
reef building organism. The capacity to infer coral type from reef morphology can
potentially be used to identify and map specific coral habitat in remotely sensed
images. More generally, identifying ecological mechanisms underlying other
Submitted 1 November 2014 examples of self-generated reef morphology can potentially improve our understand-
Accepted 15 April 2015
Published 12 May 2015 ing of present-day reef ecology, because any ecological process capable of shaping a
reef will almost invariably be an important process in real time on the living reef.
Corresponding author
David Blakeway,
fathom5marineresearch@gmail.com
Subjects Computational Biology, Ecology, Marine Biology
Academic editor
Keywords Acropora, Automaton, Cellular, Coral, Geomorphology, Holocene,
Kenneth De Baets
Houtman Abrolhos, Reticulate, Self-organised, Space-for-time
Additional Information and
Declarations can be found on
page 24
INTRODUCTION
DOI 10.7717/peerj.935 Coral reefs are large organic structures constructed over centuries to millennia by relatively
Copyright small individual organisms. The anatomy of coral reefs varies along a continuum from
2015 Blakeway and Hamblin
‘framework’ reefs consisting primarily of coral skeletons in growth position (Lowenstam,
Distributed under 1950; Fagerstrom, 1987) to ‘garbage piles’ of toppled or wave-transported corals, coralgal
Creative Commons CC-BY 4.0
fragments and sediment (Hubbard, Miller & Scaturo, 1990; Blanchon, Jones & Kalbfleisch,
OPEN ACCESS 1997). The three-dimensional form of a reef, particularly at the framework end of the

How to cite this article Blakeway and Hamblin (2015), Self-generated morphology in lagoon reefs. PeerJ 3:e935; DOI 10.7717/peerj.935
 continuum, is a potential repository of ecological information, because it represents
a long-term integration and distillation of interactions and feedbacks between the
reef-building organisms and their physical, chemical and biological environment (Roberts,
Murray & Suhayda, 1975; Hopley, Smithers & Parnell, 2007; Perry, 2011). Investigating
the morphological development of reefs can therefore help provide the historical context
within which present-day reef ecology is embedded (Hopley, Smithers & Parnell, 2007).
The primary influences on reef morphology differ across spatial scales, from the
inherent forms of reef-building organisms at the small scale to the configuration of
continental shelves at the large scale. Over intermediate scales (metres to kilometres)
reefs exhibit a great diversity of forms, reflecting the multitude of interacting processes
affecting them. But within the diversity is a subset of globally recurring forms, indicating
that there are some consistent influences governing reef morphology worldwide (Wells,
1957; Stoddart, 1969; Stoddart, 1978; Goreau, Goreau & Goreau, 1979; Blanchon, 2011;
Schlager & Purkis, 2015). Traditionally, these influences have been envisaged as external
controls operating at or above the scale of the morphological features, for example
substrate topography (MacNeil, 1954; Purdy, 1974; Choi & Ginsburg, 1982) or the wave
field (Munk & Sargent, 1954; Roberts, 1974; Storlazzi et al., 2002). While these factors are
undoubtedly responsible for many aspects of reef morphology, they raise an interesting
question: what would reefs look like in the absence of such external influences? This
question brings the focus down to the reef-building organisms themselves. Because these
organisms cumulatively become the reef, there is significant potential for behaviour and
events at their scale to be expressed in reef morphology at the intermediate scale. Such
‘emergence’ of self-organised patterns from small scale processes is ubiquitous in physical
and biological systems (Nicolis & Prigogine, 1977; Ball, 1999; Camazine et al., 2001). While
it is recognised that coral reefs are likely to exhibit this trait (Drummond & Dugan, 1999;
Mistr & Bercovici, 2003; Rietkerk & van de Koppel, 2008; Blanchon, 2011; Schlager & Purkis,
2015), it has not been directly demonstrated.
Lagoons are the most likely settings for inherent reef growth forms to arise, as they are
generally flat-floored and sheltered. Several characteristic lagoon reef forms are repeated
worldwide, ranging from simple mound-like patch reefs to complex cellular1 reef networks
1 Cellular reefs (terminology after Hoskin, (Fig. 1; Stoddart, 1969; Hopley, 1982; Blanchon, 2011). Patch reef development can be
1963) are also widely known as reticulate readily visualised in terms of expansion from a nucleus, and this mode of growth has been
reefs, from the latin reticulum: a network
or net-like structure. However, the term
demonstrated repeatedly, from various nuclei including topographic highs in underlying
reticulate has been applied to a variety limestones (Halley et al., 1977; Mazzullo et al., 1992), sedimentary structures (Perry
of lagoon reef forms that probably
develop through different mechanisms et al., 2012; Novak et al., 2013), or early-colonising corals (Jones, 1977; Crame, 1981).
(Schlager & Purkis, 2015). Therefore we Cellular morphology, in contrast, is not an intuitive growth form. Cellular reefs distinctly
consider cellular reefs to be a subdivision
of reticulate reefs, distinguished by
resemble negative landforms, particularly karst terrains (terrestrial erosion landforms
subcircular depressions as shown in created in limestone through dissolution by rainwater). Based on this resemblance,
Fig. 1.
and the recognition that the foundations of most reefs have been exposed to at least
100,000 years of weathering during Interglacial periods, cellular reef morphology has
long been interpreted as an inheritance from underlying karst (Fairbridge, 1948; Purdy,

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 Figure 1 Cellular reefs in the Pelsaert Group lagoon, Houtman Abrolhos Islands, Western Australia
(28◦ 54′ S, 114◦ E). Reproduced by permission of the Western Australian Land Information Authority
(Landgate) 2015.

1974; Guilcher, 1988; Searle, 1994; Macintyre, Precht & Aronson, 2000; Purkis et al., 2010;
Kan et al., 2015. However, there has always been an opposing view attributing cellular
morphology to reef growth (Dakin, 1919; GIE Raro Moana, 1985; Collins et al., 1993;
Wyrwoll et al., 2006; Barott et al., 2010; Blanchon, 2011; Schlager & Purkis, 2015). The
growth alternative is gradually gaining acceptance, having been confirmed for the cellular
reefs of Mataiva Atoll in French Polynesia (GIE Raro Moana, 1985; Rossfelder, 1990) and
the Houtman Abrolhos Islands in Western Australia (Collins et al., 1993; Collins, Zhu &
Wyrwoll, 1996; Collins, Zhu & Wyrwoll, 1998; Wyrwoll et al., 2006). Seismic surveys and
coring at Mataiva showed the Holocene reef to be 10 to 20 m thick and demonstrated that,
although the reef is underlain by a karst Tertiary limestone, the karst features are relatively
small-scale and were infilled before submergence, such that the present reef morphology
is independent of the substrate (Rossfelder, 1990). Similarly, seismic and coring in the
Abrolhos lagoons recorded a Holocene reef thickness of 40 m over a flat Last Interglacial
grainstone, again demonstrating independence from the substrate (Collins et al., 1993;
Collins, Zhu & Wyrwoll, 1996; Collins, Zhu & Wyrwoll, 1998).
While the seismic and coring has proven beyond reasonable doubt that the cellular
reefs of Mataiva and the Abrolhos have grown into their present configuration, it has not

Blakeway and Hamblin (2015), PeerJ, DOI 10.7717/peerj.935 3/30

 provided a generally accepted growth mechanism. Four alternative mechanisms have been
proposed. The first, developed independently by GIE Raro Moana (1985) at Mataiva and
Barott et al. (2010) at Millenium Atoll, is the colonisation of the lagoon floor by networks
of massive corals, which are subsequently colonised by other corals and grow upward to
the surface. The second, proposed by Wyrwoll et al. (2006) for the Abrolhos, is growth to
sea level of isolated branching Acropora pinnacles and stellate (star-shaped) reefs, which
subsequently extend laterally and coalesce to surround enclosed depressions. The third,
proposed by Blanchon (2011), is a self-limitation mechanism based on negative feedback
between reef growth and water circulation—reef growth reduces water circulation which
reduces reef growth, such that the cellular depressions become self-reinforcing as the
surrounding reefs grow. The fourth mechanism, proposed by Schlager & Purkis (2015)
is biological self-organisation through short-range support and long-range inhibition,
conceptually based on Turing’s (1952) reaction–diffusion mechanism of natural pattern
formation.
The alternative mechanisms outlined above are hypothetical and have not been
comprehensively evaluated in real cellular reefs. In this article we use field observations and
reef growth simulations to examine the process of cellular reef development in one of the
type examples of cellular reefs mentioned above, those of the Houtman Abrolhos Islands.
These reefs are an ideal case study site due to their flat pre-Holocene substrate, known
accretion history and very pure reef-building community—cores through the Abrolhos
cellular reefs consist almost entirely of branching Acropora, with a few tabular Acropora
appearing as the reefs approached sea level (Collins et al., 1993; Collins, Zhu & Wyrwoll,
1996; Collins, Zhu & Wyrwoll, 1998). Furthermore, an apparent sequence of cellular reef
development is evident in the Abrolhos lagoons (Wyrwoll et al., 2006), progressing from
pinnacle reefs to stellate reefs surrounding semi-enclosed depressions to a reef platform
surrounding enclosed depressions. Under the assumption that these are sequential stages
of reef development, surveys of the pinnacle-stellate-platform sequence represent surveys
through time. Space-for-time substitution (Darwin, 1842; Davis, 1899; Maxwell, 1968;
Hopley, 1982) can therefore be applied to describe the evolution of the Abrolhos cellular
reefs and, potentially, to reveal their formative mechanism.

REEF SURVEY
Methods
We examined replicate sites of each stage in a 15 km2 cellular reef complex known as
the Maze in the Easter Group of the Abrolhos (Fig. 2). We surveyed fifteen sites in detail
and many more in brief visits, including some in the Pelsaert Group to the south and the
Wallabi Group to the north. At each of the fifteen Maze sites we established four transects
oriented to the cardinal directions, running upslope from the deepest to shallowest habitat.
Transects varied in length from 5 m at site A (maximum depth 3 m), to 75 m at site
K (maximum depth 30 m). We constructed a topographic profile of each transect by
recording tide-corrected depth at one metre intervals along each transect, and quantified
substrate composition by filming each transect and point counting sequential still images,

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 Figure 2 Aerial image of the Maze in the Easter Group of the Houtman Abrolhos Islands (28◦ 41′ S
113◦ 49′ E). The 15 survey sites are labelled A to O. Reproduced by permission of the Western Australian
Land Information Authority (Landgate) 2015.

using five fixed points per image (English, Wilkinson & Baker, 1997) and 25 benthic
substrate categories (Data S1). The 25 substrate categories were condensed into seven
categories for graphical representation: tabular Acropora, branching Acropora, massive and
encrusting coral, soft coral, macroalgae, dead coral, and sediment.

Results
Underwater observations show that the different reef stages are joined in a continuous reef
blanket with a distinctive undulating form, resembling the ‘egg box’ structure described by
Kan et al. (2015) in the cellular reefs of Nagura Bay, Japan. The relationship between the
shapes of the different stages can be envisaged by imagining sequentially deeper horizontal
slices through a solid egg box. The initial slices contact the peaks, producing circular
shapes. These reefs correspond to Wyrwoll et al.’s (2006) pinnacles but we subsequently
refer to them as haystacks, based on earlier descriptions of similar Acropora-dominated
reefs in the Caribbean (Goreau, 1959; Kinzie, 1973). Deeper slices reach the ridges
between adjacent peaks, producing stellate shapes. Subsequent slices produce a platform
surrounding enclosed depressions and eventually a solid platform. Below we describe the
sequence in the three idealised stages: haystack, stellate and platform. However, it should be
noted that the sequence is a continuum and that sites within each stage may have features
of earlier and/or later stages. Figure 3 shows representative transect profiles from each
stage and Fig. 4 is a schematic block diagram incorporating the main features of the three
idealised stages.

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 Figure 3 Representative transect profiles and benthic substrate composition graphs from haystack,
stellate and enclosed sites in the Maze.

Haystacks
Haystacks occur around the margin of the Maze (e.g., sites K and M; Fig. 2). The reef
surface at these sites has a sinusoidal profile, curving up over dome-shaped reef tops
then descending into bowl-shaped depressions (Fig. 3). The wavelength and amplitude
of the profile vary within ranges of approximately 40–100 m and 15–30 m, respectively.
The Abrolhos haystacks, like those of the Caribbean (Goreau, 1959; Kinzie, 1973), consist
of loosely interlocked branching Acropora colonies, most in growth position but many
collapsed and overturned. Adjacent haystacks are linked by saddle-shaped ridges of
branching Acropora. The predominant Acropora species on the haystack reefs and ridges
are A. formosa/muricata and A. abrolhosensis. Tabular A. spicifera is abundant at site M on

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Figure 4 Block diagram illustrating the Maze’s egg-box topography and the three idealised stages of
cellular reef development. The cross-section is hypothetical but consistent with seismic and core data.

the exposed northern margin of the Maze but absent from the more sheltered site K to the
south. Live Acropora cover is 60–100% on the reef tops and ridges at both sites, decreasing
to approximately 30% within the site M depressions and 0% within the more enclosed and
restricted site K depressions. Dead Acropora branches at depth are occupied by macroalgae
at both sites, predominantly Sargassum spp. at site M and Lobophora variegata at site K.
Beyond the outermost haystacks, the reef surface slopes down to a flat sandy seafloor at
35 m without breaking into isolated patches (Fig. 4). Corals on these outer slopes are
predominantly branching and tabular Acropora to approximately 25 m depth (Wilson &
Marsh, 1979). Below 25 m the coral community is more diverse, with a high proportion of
foliose genera, particularly Leptoseris and Pachyseris.
Three islands of storm-deposited Acropora rubble line the eastern margin of the Maze
(Collins, Zhao & Freeman, 2006), and a series of submerged east–west trending linear reef
banks occur on the northern margin of the Maze. Two banks can be seen in Fig. 2 and two
deeper banks lie beyond them. The bank crests are 2 to 15 m deep, sloping downward to
U-shaped troughs at 20 to 30 m. The outermost bank reaches the seafloor at 35 m. Coral
cover and zonation on the banks is equivalent to that of the haystack reefs.
Stellate reefs
In the stellate stage the haystack reef tops and ridges reach sea level, producing a network of
flat-topped star-shaped reefs (sites B, E, F, J, L, N). Water circulation within the intervening
depressions is further reduced and the water column is often stratified and stagnant.
Live coral is consequently restricted to shallow depths, often less than 15 m in the more
enclosed depressions. The shallow subtidal reef slopes and ridges remain dominated by live
branching Acropora (Fig. 5) and occasional foliose Montipora. Dead Acropora branches at
depth are colonised by Nephthea soft corals and Lobophora variegata, and fine sediment
accumulates in the bases of the depressions.

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 Figure 5 Dense in-situ (A) and collapsed (B) Acropora colonies on a stellate reef in the Pelsaert Group
lagoon.

A distinct shallow coral community begins to appear in the stellate reefs, consisting
of diverse massive and encrusting corals, the most abundant genera being Montipora,
Goniastrea, Favia, Favites, Merulina, Astreopora, Montastrea, Mycedium, Echinophyllia,
Cyphastrea, Alveopora and Lobophyllia. Several apparent developmental stages of this
community are present, initiating as a discontinuous cover of small colonies on dead
Acropora branches (Fig. 6A) and culminating in vertical or overhanging walls descending
from the surface to as deep as ten metres, but typically between two and eight metres
(Fig. 6B).
Reef platform with enclosed depressions
In the platform stage (sites C, D, I, O) the trends in water quality and coral distribution
that were established in the stellate reefs develop further: most depressions are rimmed
by vertical walls of massive and encrusting coral, live Acropora cover below the walls
declines rapidly with depth, the water column is usually stratified, and the depressions
typically have a deep sediment fill. Late-stage enclosed depressions (A, G, H) gradually
fill with sediment to the level of the surrounding reef flat. As they fill, the fringe of live
Acropora beneath the vertical walls migrates upward, eventually overgrowing the walls and
encroaching over the depression floors.

MODEL
Rationale
Based on the survey results described above, the Abrolhos cellular reefs appear to exhibit
a straightforward developmental sequence. However, they provide little direct insight
into the origin of cellular morphology because the cellular form is already present at

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 Figure 6 Inferred early (A) and late (B) stages of reef wall development in the Pelsaert Group la-
goon. The walls appear to initiate through the colonisation of dead Acropora branches by massive and
encrusting corals (A), and subsequently grow to become vertical or overhanging (B).

the haystack stage. Given the high coral cover on the haystack reef tops and ridges,
subsequent growth will inevitably enclose the depressions. Although the haystacks must
have progressed through earlier stages to reach their present configuration, the existing
space-for-time sequence does not extend back to the earlier stages, presumably because
coral colonisation of the Last Interglacial surface ceased when it became deeply submerged
and covered by sand in the mid Holocene. If this is the case, even the youngest haystacks
probably initiated more than 4,000 years ago. Several processes appear to be suppressing
live coral cover, and therefore accretion, within the present-day haystack reef depressions,
including reduced water circulation and macroalgal colonisation. But in the absence of
earlier stages in the space-for-time sequence it is impossible to determine whether these
processes could have initiated the depressions or whether they are consequential. In this
situation, computer simulation provides a potential means of investigating the early stages
of reef development.

Methods
The model we describe below is configured as a cellular automaton: an array of
identically-programmed interacting cells (Von Neumann, 1951; Ulam, 1962; Data S2).
This structure is well-suited to simulating reef growth because each cell in the array can
be considered to represent a square metre of seafloor, and reefs can grow on the seafloor
as three-dimensional stacks of cubic ‘corals.’ Using this approach, we simulate lagoon reef
development as the growth and coalescence of patch reefs from individual coral recruits

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 on a flat seafloor. We first describe a basic model in which colonisation and growth is
essentially random and unconstrained except by sea level, and subsequently introduce a
parameter representing branching Acropora.
Basic model
The basic model is initialised by defining the seafloor depth, the array dimensions and the
number of coral recruits. We used a default configuration of 30 m depth (static, i.e., no
sea level variation), a 160 × 160 cell array (representing 160 × 160 m, or 2.56 hectares, of
seafloor), and 64 randomly-spaced coral recruits, occupying 0.25% of the array. The 160
× 160 m recruitment array was centered within a larger array of 250 × 250 m, giving the
reefs a 45 m margin for lateral growth. We chose 30 m as the default depth, rather than
the 40 m of the Maze, because cellular reefs elsewhere appear to be thinner than the Maze;
those at Mataiva, for example, are only 10 to 20 m thick (Rossfelder, 1990). The horizontal
dimensions of the array were selected to minimise computation time while still allowing
adequate spatial representation of reef morphology. The colonisation density was selected
such that the resulting patch reefs were close enough to eventually coalesce but not so close
as to immediately coalesce. We examined variations to the default configuration, including
sea level rise, and describe them later under ‘additional modifications.’
Growth from the initial coral recruits is effected by assigning two growth probabilities
to each cell in the array in each iteration: a vertical probability representing the likelihood
of the cell growing upward itself and a neighbour probability representing the likelihood
of the cell being overgrown by a neighbouring coral (Fig. 7). The vertical probability of
vacant seafloor cells is zero, and the vertical probability of coral-filled cells is random.
The neighbour probability of each cell is the product of a random number between zero
and one and a ‘neighbour value’ that depends on the state of the eight surrounding cells.
Cells with no shallower neighbours are assigned a neighbour value of zero; otherwise, the
cell’s neighbour value rises incrementally for each shallower neighbour. If a cell becomes
surrounded by shallower neighbours, it is guaranteed to be overgrown. Otherwise, growth
is determined by comparing the cell’s vertical and neighbour probabilities against two
random numbers between zero and one. If either or both probabilities exceed their
respective random numbers, the cell grows by one metre when the array is updated prior
to the next iteration. Vertical accretion is halted at sea level but lateral accretion continues.
The time represented by each iteration is arbitrary but we consider it to be 100 years, giving
a mean vertical reef accretion rate of 7 mm/yr (the theoretical maximum rate of 10 mm/yr
is not achieved because corals do not grow in every iteration).
Branching Acropora model
Representation of branching Acropora was guided by the output of the basic model (Fig. 8).
The basic model reefs have an irregular ‘spiky’ surface, with corals projecting up to four
metres above the surrounding reef. Such projections cannot occur on real branching
Acropora reefs because, due to their ‘brittle tree’ morphology, any branching Acropora
colonies that grow more than a metre or two above their surroundings will inevitably
collapse (Maragos, 1972; Bak, 1976; see Fig. 5B). This is not necessarily a disadvantage.

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 Figure 7 Cross-section through a hypothetical model reef. Upward-pointing arrows indicate vertical
growth directions, horizontal and diagonal arrows indicate neighbour growth directions.

Because broken fragments can survive and grow to form new colonies, collapse and
fragmentation are recognised as inherent and significant modes of reproduction and
short range dispersal in branching Acropora (Gilmore & Hall, 1976; Tunnicliffe, 1981;
Bothwell, 1982; Highsmith, 1982). Collapse is represented in the branching Acropora
model by imposing a maximum height differential between neighbours (hereafter termed
collapse limit) of two metres, such that corals growing to project two metres above
any neighbouring cell are prevented from growing upward until the deeper cell grows.
Although they cannot grow upward, projecting corals contribute to the growth probability
of neighbouring cells in two ways: first, they ‘support’ neighbouring corals, ensuring
they are unrestricted by the collapse limit; and second, they may ‘collapse into’ deeper
neighbouring cells (i.e., they increase the neighbour probability of those cells). Although
this representation of collapse involves no subtraction of height from the projecting colony,
it remains valid because it is equivalent to the projecting colony growing a metre then
collapsing back a metre during the iteration. Because the imposition of the collapse limit
slows reef growth, the time represented by each iteration is reduced to 40 years. This gives
a mean vertical reef accretion rate of 9 mm/yr, approximating that of the Abrolhos cellular
reefs (Eisenhauer et al., 1993; Collins et al., 1993).
Additional modifications
We examined the effects of increasing the collapse limit, altering water depth, altering
colonisation density, and periodically adding new coral recruits. We also simulated sea
level rise and depth-dependent growth, using a simplified linear sea level rise of 10 mm/yr,
stabilising at 30 m depth, and a simplified linear reduction of the coral growth rate to 10%
of the surface rate at 30 m.

Results
Basic model
Patch reefs created with the basic model appear approximately circular in plan view and
steeply conical in oblique view (Figs. 8A and 8B). The individual patch reefs maintain their
conical form as they enlarge and coalesce with neighbouring patches (Figs. 8C and 8D).

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 Figure 8 Reefs generated by the basic model. (A) Two-dimensional plan view of a patch reef after 80
iterations (8,000 years) of growth from a single seed coral. Shading corresponds to depth—the reef top
at sea level is white and the surrounding seafloor at 30 m depth is black. This patch reef reached sea level
in approximately 45 iterations (4,500 years), and by 80 iterations has developed a 15 m wide reef flat.
(B) Three-dimensional oblique view of the patch reef in (A), showing the irregular surface morphology
caused by projecting corals. The reef slopes are approximately 65◦ . (C) Two-dimensional plan view of
a coalescing patch reef system after 80 iterations. Only the uppermost 10 m of the reef system is shown,
simulating an aerial view with 10 m water visibility. (D) Three-dimensional oblique view of the reefs in C.

We use the term ‘nodular’ to describe the shapes and forms generated by the basic model.
While the nodular reefs resemble many natural patch reefs (e.g., Fig. 9), they bear little
resemblance to cellular reefs. In fact, their shapes are the inverse of cellular reefs; nodular
reefs appear convex and subcircular in plan view, whereas cellular reefs are concave and
stellate, surrounding subcircular depressions. However, the basic model is generic and does
not intentionally represent any particular coral type.

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 Figure 9 Coalescing nodular patch reefs exposed on a low spring tide at Cockatoo Island in the Buccaneer Archipelago, Western Australia
(16◦ 4.8′ S 123◦ 35′ E). Photograph by John MacFadyen.

Branching Acropora model

Reefs created with the branching Acropora model closely resemble the Abrolhos cellular
reefs (Fig. 10). The model reproduces the characteristic egg box form of the real reefs and
all its corollaries including haystack reefs, stellate reefs with radiating ridges, reef platforms
enclosing bowl-shaped depressions, scalloped platform margins and the presence of
multiple small depressions within larger multi-lobed depressions. The 45◦ slopes of the
model reefs are steeper than the mean of the real Acropora slopes (37◦ ± SD 6◦ ) but
within their recorded range. Figure 11 shows sequential stages in the development of
the branching Acropora reefs, demonstrating the emergence of their egg box morphology.
The key process is the formation of ridges between adjacent patch reefs. This process
begins when the patch reefs meet, whereupon the valleys between them grow rapidly
upward to become saddle-shaped ridges (Figs. 11C and 11D). The depressions surrounded
by the reefs and ridges are initially irregular in outline but are progressively smoothed
to subcircular shapes as the surrounding reef grows. Eventually the depressions become
completely enclosed within the reef platform and infilled by coral (Fig. 11E).

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 Figure 10 Plan view of model (A) and real (B) branching Acropora reefs. Only the uppermost 10 m
of the model reef is shown, simulating an aerial view with 10 m water visibility. This reef grew in 100
iterations (4,000 years) from 225 corals seeded at the default colonisation density (0.25%) in a 300
× 300 m array. The real reefs shown in B are those from Fig. 1, in the Pelsaert Group of the Abrolhos.
The arrowed annotations indicate the locations of photographs shown in Figs. 5A and 5B. Figure 10B is
reproduced by permission of the Western Australian Land Information Authority (Landgate) 2015.

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 Figure 11 Sequential stages in the development of model branching Acropora reefs. (A) Plan view of
the 64 randomly spaced seed corals from which the model reefs developed. This seed coral configuration
is the same as that used to create the basic model reefs in Figs. 8C and 8D. (B) After 25 iterations (1,000
years) the seed corals have developed into conical patch reefs with 45◦ slopes. (C) After 50 iterations
(2,000 years) the patch reefs have enlarged and many have merged. When patch reefs meet, the valleys
between them grow upward rapidly to become saddle-shaped ridges. (continued on next page...)

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 Figure 11 (...continued)
(D) After 100 iterations (4,000 years) most of the reef tops have reached sea level and the system of
ridges has developed to enclose and isolate depressions, producing egg-box morphology. (E) After 140
iterations (5,600 years) an extensive sea level platform has developed, and most of the depressions have
filled. (F) Plan view showing the uppermost 10 m of the reef in D, simulating an aerial view with 10 m
water visibility. The video shows model branching Acropora reef development at five iteration intervals to
100 iterations, then 120 and 140 iterations.

Additional modifications
Increasing the collapse limit was the most influential of the additional modifications.
Progressively increasing the collapse limit beyond the two metres of the branching
Acropora model produces a transition from cellular to nodular reef forms. A three metre
collapse limit creates reefs with weakly developed subcircular depressions (Figs. 12A and
12B) and a four metre collapse limit creates reefs with very few depressions (Figs. 12C and
12D). Collapse limits of more than four metres produce nodular reefs equivalent to those
of the basic model.
Varying water depth also significantly influences reef morphology. Reducing depth
reduces reef thickness, which constrains the morphological expression of the collapse
limit such that the appearance of the branching Acropora reefs transforms from cellular
to nodular as depth decreases (Figs. 13A and 13B). In the extreme case of reefs growing in
only one or two metres water depth, where the collapse limit has no effect, all variants of
the model produce identical nodular reefs. Increasing depth, by itself, has little influence
on reef morphology (Figs. 13C and 13D). However, more realistic representations
incorporating sea level rise and depth-dependent growth cause reef slopes to steepen
significantly as depth increases (Figs. 13E and 13F). Variations in colonisation density and
timing have relatively little effect on reef morphology, besides the expected crowding of
patch reefs at high density (Fig. 14).

DISCUSSION
Model
The resemblance in shape and form between the model reefs and real reefs suggests that
the model adequately represents reality. This interpretation is supported by the model’s
simplicity: it has only one rule—collapse if too steep—which is intuitively reasonable and
supported by field observations. Model reef morphology is hyper-sensitive to that rule,
running through a nodular to cellular spectrum as permissible steepness is reduced and
collapse becomes more frequent.
The nodular reefs produced by the basic model appear straightforward and visually
‘correct’ as growth forms, because the individual patch reefs maintain their forms as
they grow and merge. This straightforward morphology is indicative of pure in situ (in
place) growth. Cellular reefs are more complex because the patch reefs transform as they
merge, eventually becoming linked by a network of ridges. This transformation results
from the high frequency of collapse in the branching Acropora model. However, it is not
simply the frequency of collapse that produces ridges; more important is the distribution

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 Figure 12 Influence of the collapse limit on model reef morphology. (A) Plan view, 0–10 m depth, of a
model reef system with a 3 m collapse limit after 90 growth iterations. (B) Oblique view of the model reef
in A. The reef slopes are approximately 55◦ . (C) Plan view, 0–10 m depth, of a model reef system with a
4 m collapse limit after 85 growth iterations. (D) Oblique view of the model reef in C. The reef slopes are
approximately 60◦ .

of collapse. Because the valleys between merging patch reefs are low points in the reef
structure, coral colonies in the valleys are less likely to project above their neighbours than
corals elsewhere. Consequently, they are relatively unrestricted by the collapse limit and
are therefore more likely to remain in place as they grow, and less likely to collapse, than
colonies elsewhere (Fig. 15). The retention of in-situ colonies transforms the V-shaped
valleys into saddle-shaped ridges that grow to sea level, enclosing depressions (Figs. 11C
and 11D, Fig. 11 Video). The subcircular shapes of the depressions arise through the same
non-uniform distribution of collapse. Colonies in the re-entrant concavities of early-stage
depressions are supported by neighbours and therefore tend to remain in place while those

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 Figure 13 Influence of water depth on model reef morphology. These modifications were undertaken
in a smaller (90 × 90 m) array, but maintained the default 0.25% colonisation density. (A) Branching
Acropora reefs grown in 10 m depth exhibit a transition toward the nodular forms of the basic model
reefs shown in (B). (C) Branching Acropora reefs grown in 50 m depth retain (continued on next page...)

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 Figure 13 (...continued)
their cellular morphology. (D) Basic model reefs grown in 50 m depth retain their nodular morphology.
(E) Branching Acropora reefs incorporating sea level rise and depth-dependent growth steepen to 60◦ .
The blocky appearance of these reefs is a consequence of being forced to their maximum slope, which
overrides the model’s randomness. (F) Basic model reefs incorporating sea level rise and depth-dependent
growth steepen to approximately 85◦ .

on projecting convexities tend to collapse. Over time this creates smooth rounded shapes,
the ultimate smooth shape being a circle.

Abrolhos cellular reefs

The foregoing descriptions of the model branching Acropora reefs provide two testable
predictions regarding real cellular reefs. First, their slopes should have consistent and
relatively low gradients, representing the angle of repose (maximum slope stability angle)
of branching Acropora. Second, the proportion of in-situ colonies should be highest in the
valleys and ridges between adjacent patch reefs, and lowest on reef slopes. Both predictions
are supported in the Abrolhos, where Acropora slopes average 37◦ ± SD 6◦ (Fig. 3) and
Acropora colonies in valleys and ridges are generally upright and in situ (Fig. 5A, see Fig. 10
for photo location) while those on reef slopes are often overturned (Fig. 5B, see Fig. 10 for
photo location). We conclude that the Abrolhos cellular reefs have developed according to
the model and that Fig. 11 closely describes their morphological progression.
One significant difference between the real and model reefs is the reduced accretion
rate of the real reefs once they reach sea level. Model branching Acropora reefs reach sea
level from 30 m depth in approximately 90 iterations (3,600 years) and only require 70
more iterations (2,800 years) to completely fill the platform, whereas the Maze reefs, in
40 m depth, reached present sea level in approximately 4,500 years (Eisenhauer et al.,
1993; Collins et al., 1993) but still have not filled the platform nearly 7,000 years later.
The reduced accretion of the real reefs probably results from two factors not represented
in the model. The first is the reduction of Acropora cover and vitality at depth, as water
circulation is restricted by the enclosure of the depressions (Wyrwoll et al., 2006). This
is an example of self-limitation through negative feedback between reef growth and
water circulation (Blanchon, 2011). Self-limitation is therefore a significant influence
on the Abrolhos cellular reefs, but operates primarily on their accretion rate not their
morphology. The second factor is the colonisation of upper reef slopes by relatively
slow-growing massive and encrusting corals. The steep walls created by these corals
effectively exclude branching Acropora, because any branching Acropora that colonise
the walls are likely to break off once they grow too large to be supported at their base. By
‘engineering’ steep walls (sensu Jones, Lawton & Shachak, 1994), massive and encrusting
corals are able to monopolise—for thousands of years—prime shallow subtidal habitat
that would otherwise be occupied by fast-growing branching Acropora. The combination
of reduced water circulation at depth and steep walls in the shallows restricts live Acropora
to a fraction of their previous distribution, significantly slowing the overall reef accretion

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 Figure 14 Influence of colonisation density and timing on model reef morphology. These plan view
images show the effects of decreasing the recruitment rate from the default 0.25% to 0.125% (A:
branching Acropora reef, 100 iterations), (B: basic reef, 80 iterations), increasing the recruitment rateto
1% (C: branching Acropora reef, 90 iterations, D: basic reef, 60 iterations), and periodically adding new
recruits during reef growth (E: branching Acropora reef, 100 iterations, F: basic reef, 70 iterations).

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 Figure 15 Diagram illustrating the proposed mechanism of ridge formation derived from the branch-
ing Acropora model. The diagram shows a cross-section through two merging patch reefs after 50
iterations (the two uppermost patch reefs in Fig. 11C). Isochrons at 20 and 40 iterations show that the
patch reefs were initially conical, and that the valley between them has accreted rapidly since the patch
reefs merged. Rapid accretion is attributed to the tendency for colonies in valleys to remain in place and
for colonies on reef slopes to collapse.

rate. Model cellular reefs, in contrast, rapidly fill the platform because ‘live’ Acropora
occupy all subtidal habitats including the depression slopes and floors.
Another significant difference between the real and model reefs is the series of linear reef
banks on the northern margin of the Maze. We interpret these as early to mid Holocene
wave-deposited structures, resulting either from storms, cyclones (Scheffers et al., 2012) or
tsunamis (Scheffers et al., 2008).

Application to other reefs

The morphology of cellular reefs elsewhere appears similar enough to the Abrolhos reefs
to suggest they have developed the same way, an inference supported by the abundance
of branching Acropora in documented examples (Alacran Reef: Hoskin, 1963; Solomon
Islands: Morton, 1974; Tétembia Reef: de Vel & Bour, 1990; Cocos Keeling Atoll: Williams,
1994; Pelican Keys: Aronson, Precht & Macintyre, 1998; Elizabeth Reef: Woodroffe et al.,
2004; Pohnpei: Turak & DeVantier, 2005; Tun Sakaran: Montagne et al., 2013; Nagura Bay:
Kan et al., 2015). At least two of these examples, the Solomon Islands (Morton, 1974) and
Nagura Bay (Kan et al., 2015), exhibit vertical walls of massive and encrusting corals above
the Acropora zone, suggesting they have undergone the late-stage shallow coral community
succession observed in the Abrolhos.
We have separated Mataiva Atoll from the list above as Porites is abundant there and
has been considered responsible for the cellular morphology (GIE Raro Moana, 1985;
Delesalle, 1985). However, branching Acropora are also abundant at Mataiva (Delesalle,
1985; Rossfelder, 1990). We suggest that branching Acropora are the primary reef builders at
Mataiva and Porites are colonisers of the Acropora reef, not framework builders. Another
possible exception to the rule of Acropora dominance is the ‘Type-1’ reticulate reef of the
Red Sea (Purkis et al., 2010), where Porites is also abundant (Bruckner, 2011). However,

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 we would not classify all Type-1 Red Sea reefs as cellular because, although deep, the
depressions are not always circular; more often resembling the transitional depressions
produced by intermediate collapse limits (see Purkis et al.’s Fig. 2). Some Red Sea reefs are
distinctly cellular and we predict those to be Acropora-dominated (e.g., 27◦ 57′ N, 35◦ 13′ E).
Closer examination of these and other cellular reefs is required to determine whether the
predominance of branching Acropora is universal, and whether the reef slope gradients and
the distribution of collapsed colonies conform to the Abrolhos example.
We have not classified the previously-mentioned Millenium Atoll with the cellular reefs
listed above because the scale of the cellular morphology at Millenium and in many other
Pacific atoll lagoons is up to an order of magnitude larger than the Abrolhos. While the
large-scale cellular reefs also seem to consist predominantly of branching Acropora (Roy
& Smith, 1971; Grovhoug & Henderson, 1976; Valencia, 1977; Barott et al., 2010), we do
not believe our model applies directly to them because it cannot produce cells of their
horizontal dimensions unless it is scaled up massively, to unrealistic depths of at least
100 m. We are currently investigating the large-scale cellular morphology.
The transitional and nodular shapes produced by increasing the collapse limit in the
model also occur in real reefs (e.g., Fig. 9). The simplest interpretation of these shapes is
that they indicate coral types, or mixtures of coral types, progressively less prone to collapse
than branching Acropora. In this interpretation, transitional shapes represent reef builders
that occasionally collapse, such as foliose and tabular corals, and nodular shapes represent
reef builders that rarely collapse, such as massive and encrusting corals or coralline algae.
The nodular reefs of Cockatoo Island in Fig. 9 conform to this interpretation, as they
consist of massive and encrusting corals cemented by coralline algae (D Blakeway, pers.
obs., 2010). However, the model indicates that transitional and nodular reef shapes are
not necessarily diagnostic of coral type, because branching Acropora patch reefs appear
nodular (i.e., circular in plan view) before they merge with adjacent patch reefs, and
transitional to nodular after they merge in shallow water (e.g. Fig. 13A). This suggests
that additional information on water depth, reef thickness and reef slope gradients
will be required to reliably infer coral type from reef morphology in transitional and
nodular reefs. Such three-dimensional data are becoming increasingly available through
reef-oriented remote sensing (Zawada & Brock, 2009; Zieger, Stieglitz & Kininmonth,
2009; Goodman, Purkis & Phinn, 2013 and references therein; Leon et al., 2013; Leon et
al., 2015). In two-dimensional aerial images, however, the only diagnostic morphology
is cellular—signifying relatively thick (>∼10 m) reefs constructed by collapse-prone
organisms.

Branching Acropora
The default collapse-prone reef builders on modern reefs are branching Acropora.
While it seems possible for other branching coral genera or other calcareous branching
invertebrates (e.g. Millepora) to create cellular reefs, observations worldwide (listed
above) suggest it is almost exclusively Acropora: A. cervicornis in the Atlantic and multiple
species in the Indo-Pacific. This is probably because branching Acropora have the ultimate

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 strategy for rapid pre-emption of space in lagoon environments. Acropora branches not
only grow quickly (up to 19 cm/yr in the Maze; Blakeway, 2000), they regularly develop
new branches which themselves branch and rebranch, giving them the potential for
exponential expansion (Shinn, 1976). Constant growth, branching and collapse produce
an open three-dimensional structure that rapidly fills lagoons (Davis, 1982). Our model
indicates that, given adequate depth, cellular reefs are the inevitable result. Cellular reefs
are essentially a phenotype of the branching Acropora genome(s), emerging from the
innate behaviour of branching Acropora colonies just as colony morphology emerges from
the innate behaviour of polyps.
If the relationship between cellular reef morphology and branching Acropora holds, the
distinctive shapes of cellular reefs in remotely sensed images can potentially be used to
identify and map branching Acropora habitat. This could be useful in reef conservation,
as the sensitivity of branching Acropora to environmental conditions makes them
something of a canary in the coral reef coalmine (Marshall & Baird, 2000; Loya et al.,
2001; Acropora Biological Review Team, 2005; Roth & Deheyn, 2013). However, assessing
anthropogenic impacts in apparently degraded Acropora-dominated lagoons will rarely be
straightforward, because natural self-limitation and community succession can drastically
reduce Acropora cover and vitality in the mid to late stages of reef development. Aronson,
Precht & Macintyre (1998), Aronson (2011) and Perry & Smithers (2011) highlight the
value of documenting and understanding such intrinsic trends, generated by the reef itself,
before attempting to evaluate the effects of extrinsic influences imposed from outside the
reef, including anthropogenic stresses.

Conclusions
Our simulations indicate that reef morphology is fundamentally determined by the extent
to which reef-building organisms either remain in place or collapse. This control is best
expressed in lagoons, where diminished hydrodynamic and substrate influences allow
reefs to grow into their inherent forms. The purest growth forms arise in sheltered lagoons
dominated by a single type of reef builder, as in the cellular reefs of the Abrolhos. In
these situations, reef morphology can be considered a phenotype of the predominant
reef-building organism.
While the propensity for collapse appears to explain the nodular to cellular spectrum of
lagoon reef morphology, many more relationships between reef ecology and morphology
remain to be discovered. Many of the recurrent patterns in reef morphology are likely
to be ecological phenomena (Blanchon, 2011; Schlager & Purkis, 2015). Quantifying
these patterns and identifying their underlying mechanisms can potentially improve
our understanding of present-day reef ecology, because any ecological process capable of
shaping a reef will almost invariably be an important process in real time on the living reef.
Investigation of the relationships between reef morphology and ecology is benefiting
from advances in the availability, resolution and processing of remotely sensed imagery.
However, the single most important research technique remains careful and objective
underwater observation. Any consistent correlations between reef morphology and

Blakeway and Hamblin (2015), PeerJ, DOI 10.7717/peerj.935 23/30

 underwater survey data, such as coral type, can be considered potential causal relationships
warranting closer examination.
In surveying modern reefs, it should be recognised that a reef ’s current state may
not represent its formative state, particularly if the reef has reached sea level. While
seismic and coring can access the history stored within such reefs, both techniques are
logistically demanding and expensive. The complementary methods we employed in the
Abrolhos, space-for-time substitution and computer simulation, are relatively simple and
inexpensive but can provide a comprehensive reconstruction of a reef ’s history and a sound
basis for extrapolating its future development.

ACKNOWLEDGEMENTS
Many thanks to field volunteers Nik Sander, Gary Watson, Tim Benfield, Nokome Bentley,
Matz Berggren, Freda Blakeway, Richard Campbell, Robin Cornish, Simon Cutler, Geoff
Deacon, Tim Fisher, Steven Fletcher, Erez Jacobsen, Margaret Jones, Jason Kennington,
Helen Kirby, Clare Taylor and Roland Tyson. Logistic support from the mainland was
provided by Freda Blakeway, Philip Blakeway and Wendy Perriam. Logistic support in
the Islands was provided by the Western Australian Department of Fisheries, especially
Kim Nardi, Michael Byrne, Chris Chubb , Boze Hancock, David Murphy and Tony Paust.
Transport to and from the Islands was provided by David Kingdom, Mal McRae, David
van der Oord, Ian Rowlands, Chris Shine, Fred Tucker and Geoff Whitehurst. Thanks to
Justin Parker, PeerJ Academic Editor Kenneth De Baets and two anonymous reviewers for
improvements to the manuscript.

ADDITIONAL INFORMATION AND DECLARATIONS

Funding
Research funding was provided by the Australian Research Council. David Blakeway
and Michael Hamblin were supported by Australian Postgraduate Research Award
scholarships. The funders had no role in study design, data collection and analysis, decision
to publish, or preparation of the manuscript.

Grant Disclosures
The following grant information was disclosed by the authors:
Australian Research Council.
Australian Postgraduate Research Award.

Competing Interests
David Blakeway is an employee of Fathom 5 Marine Research.

Author Contributions
• David Blakeway conceived and designed the experiments, performed the experiments,
analyzed the data, wrote the paper, prepared figures and/or tables.
• Michael G. Hamblin conceived and designed the experiments, performed the experi-
ments, reviewed drafts of the paper.

Blakeway and Hamblin (2015), PeerJ, DOI 10.7717/peerj.935 24/30

 Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/
10.7717/peerj.935#supplemental-information.

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