Facies (2010) 56:1–11
DOI 10.1007/s10347-009-0193-5
ORIGINAL ARTICLE
Ecological stages of Maldivian reefs after the coral mass
mortality of 1998
Roberta Lasagna Æ Giancarlo Albertelli Æ
Paolo Colantoni Æ Carla Morri Æ Carlo Nike Bianchi
Received: 24 February 2009 / Accepted: 13 July 2009 / Published online: 6 August 2009
Ó Springer-Verlag 2009
Abstract The bleaching event of 1998 caused wide-
spread mortality on coral reefs in the Maldives. Nearly
10 years after the coral mass mortality, the state of
Maldivian reefs was evaluated paying specific attention to
three ecological stages, linked to the 3D structure of the
coral community: young (high living hard coral cover),
mature (a balance between living coral cover and loose
sediment), and regressive (high amount of rubble and
sand). The relative importance of three biogeomorpholog-
ical descriptors (living hard corals; rubble and sand; cor-
alline algae on rock) in the reef flat (2–7 m depth) and in
the slope (7–18 m) of three reefscapes related to wave
exposure was assessed. The role of wave energy in shaping
ecological stages is different in the reef flat (early stages
are found in low energy conditions) and in the slope (early
stages are associated with high energy sites).
Keywords Biogeomorphology
Coral reefs

Ecological stages
Maldives
Indian Ocean
Introduction
According to Pichon (1974), coral reef communities can
show three different stages ruled by hydrodynamic factors:
(1) young or immature stage, (2) mature stage, and (3)
R. Lasagna (&)
G. Albertelli
C. Morri
C. N. Bianchi
DipTeRis (Department for the study of the Territory
and its Resources), University of Genoa, CoNISMa Local
Research Unit, Corso Europa 26, 16132 Genoa, Italy
e-mail: roberta.lasagna@dipteris.unige.it
P. Colantoni
University of Urbino ‘‘Carlo Bo’’, Campus Scientifico,
Loc. Crocicchia, 61029 Urbino, Italy
regressive stage. In the young stage, biotic factors prevail
and reef communities are characterized by the dominance
of reef builders (scleractinian corals and coralline algae):
reef accretion and consolidation are encouraged and ero-
sion is reduced (Holmes et al. 2000; Spencer and Viles
2002; Perry and Hepburn 2008; Perry et al. 2008). The
mature stage represents a balance between biotic (coral
growth) and abiotic factors (sediment deposition), with a
comparatively lower abundance of scleractinian corals.
Finally, the regressive stage is controlled by the predomi-
nance of abiotic factors, with sparse living hard coral cover
and high amounts of rubble and sand.
Over the last decades, coral reefs have experienced an
increased number of environmental disturbances linked to
global change (Goreau et al. 2000; Barton and Casey 2005).
In 1998, high sea surface temperatures caused by El Niño,
led to the largest bleaching episode on a worldwide scale,
followed by coral mass mortality (Hoegh-Guldberg 1999;
Wilkinson et al. 1999). After such a massive coral die-off,
the three-dimensional structure of reef uppermost veneer
may be maintained over months to a few years by the dead
hard coral colonies still in place; as time goes on, however,
physical and biological erosion of dead colonies may lead
to an increased abundance of loose material (rubble and
sand) and thus to the loss of the three-dimensional structure
of the reef community (Sheppard et al. 2002; Bianchi et al.
2006a, 2006b). This loose material can limit coral recruit-
ment (Loch et al. 2002; Lasagna et al. 2006), as coral larvae
preferentially settle on encrusting calcareous algae
(Heyward and Negri 1999) and frequently avoid rubble as a
settling substratum (Sheppard et al. 2002).
The widespread bleaching episode of 1998 severely
affected a large part of the Indian Ocean (Wilkinson et al.
1999) and the central atolls of the Maldives suffered coral
mortality of up to 90% (Bianchi et al. 2006a). Data on
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Maldivian reef conditions before this mortality event are
scarce (Scheer 1971; Spencer-Davies et al. 1971; Ciarapica
and Passeri 1993; Allison 1995; Morri et al. 1995; Bianchi
et al. 1997) and do not allow direct evaluation of their
previous ecological stage: however, records of living hard
coral cover generally between 30 and 60%, often reaching
100% in shallow water (McClanahan 2000; Zahir 2000;
Bianchi et al. 2006a, 2006b), suggest that they were mostly
in young to mature stages. Seven–eight years after the mass
mortality event, coral cover was found to be only 20%
(Lasagna et al. 2008). The rugosity of the reef uppermost
veneer was low because of the lack of massive or arbo-
rescent coral colonies and the abundance of coral rubble
(Lasagna et al. 2006): most reef communities should
therefore have reached a regressive stage.
First studies aiming at assessing reef state after the coral
mass mortality event in the Maldives have considered coral
cover, recruitment, colony size, and species richness (Loch
et al. 2002, 2004; Bianchi et al. 2006a, 2006b; Lasagna et al.
2006, 2008; Pichon and Benzoni 2007), but little attention
has been given to the quantification of the loss of contribu-
tion to reef surface complexity, with an approach requiring
the interaction between geomorphology and biology
(Andréfouët and Guzman 2005; Graham et al. 2006).
Our study examines the present condition of the
Maldivian reefs, aiming at describing their ecological
stages, using both geomorphological and biological
descriptors. As reef communities are known to vary
according to wave energy (Kench et al. 2006) and water
depth (Goreau 1959; Ciarapica and Passeri 1993; Bianchi
et al. 1997; Riegl and Piller 2000; Dullo 2005), stages in
the Maldivian reefs were studied taking into account
topography, exposure, and depth.
Materials and methods
Study area
Some pioneering studies (Stoddart et al. 1966; Spencer-
Davies et al. 1971) and more recent descriptions (Woodroffe
1992; Ciarapica and Passeri 1993; Allison 1995; Morri et al.
1995; Bianchi et al. 1997; Colantoni et al. 2003) provide
baselines for the morphology of Maldivian reefs. The Mal-
dives are situated on the central part of the Chagos-Mald-
ives-Laccadive Ridge in the Indian Ocean. They are formed
by a single atoll chain in the north and in the south, and by a
double atoll chain in the central part (Price and Clark 2000;
Risk and Sluka 2000). With their 22 atolls and some 1,120
islands, the Maldives extend in a north–south direction from
about 7°070 N to 0°400 S in latitude, rising steeply from the
Indian Ocean abyssal plain, which is 2,500 m deep eastward
and 4,000 m deep westward. By contrast, the sea floor of the
lagoons inside the atolls is 50–60 m deep, while the channels
between the atolls reach a depth of 300–400 m (Ciarapica
and Passeri 1993; Gischler 2006). The climate in the Mal-
dives is monsoon-dominated, with a wet summer monsoon
(April to November) due to winds blowing to the northeast,
and a dry winter monsoon (December to March) with winds
blowing westward (Kench et al. 2006).
Field activities
A total of 16 randomly selected sites of two types of
locations were investigated by scuba diving: eight outer
(ocean-facing sides of faros situated on the atoll rim) reef
sites and eight inner (lagunal faros or lagoon-facing sides
of the atoll rim) reef sites (Table 1; Fig. 1). In each site,

Table 1 Sites and atolls visited

Site Atoll Location Latitude Longitude
by the Albatros Scientific
Cruises in 2006–2007 with 1 Maadhoo Faru South Malé Outer reef 3°530 0400 N 73°280 0600 E
indicated the two types of 0 00
locations (outer and inner reefs), 2 Fufalhi Faru Felidhoo Outer reef 3°39 13 N 73°300 1100 E
0 00
latitude, and longitude 3 Dhangethi Ari Outer reef 3°35 54 N 72°570 2900 E
4 Faanu Mudugau Ari Outer reef 3°550 3400 N 72°570 2900 E
0 00
5 Fushidiggaru Falhu South Malé Outer reef 3°59 33 N 73°310 2900 E
0 00
6 Boldhuffaru South Malé Outer reef 4°05 34 N 73°230 0800 E
0 00
7 Thoddoo E Thoddoo Outer reef 4°26 01 N 72°580 0000 E
0 00
8 Thoddoo NE Thoddoo Outer reef 4°26 33 N 72°570 5600 E
9 Sexy Finolhu South Malé Inner reef 3°570 1900 N 73°270 3000 E
10 Biology Faru Felidhoo Inner reef 3°360 1800 N 73°230 4300 E
0 00
11 Rasheed Finolhu Ari Inner reef 3°36 24 N 72°550 0000 E
0 00
12 Mushimasmingili Ari Inner reef 3°58 02 N 72°540 2400 E
0 00
13 Ali Kuda Faru South Malé Inner reef 4°05 29 N 73°250 3700 E
0 00
14 Rasfari North Malé Inner reef 4°24 19 N 73°220 0200 E
15 Bodufoludhoo Kuda Giri Ari Inner reef 4°110 1400 N 72°470 1600 E
0 00
16 Velidhoo-dhiggaa Kuda Giri Ari Inner reef 4°09 09 N 72°490 2600 E

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Facies (2010) 56:1–11 3

India
6°N
Indian
Ocean
Maldives
0°N 60°E 90°E

4°N

315° N 45°

Thoddoo
90°
7 2°N
14
8 73°E
225°

Rasdhoo North Malé

Atoll Atoll
15

16
6
13
Ari Atoll

12 5
9
4
1 South Malé
Atoll

2
11 10
3

Felidhoo Atoll

OUTER REEF SITES

0 10 km
INNER REEF SITES
3°20’ N

72°40’ E

Fig. 1 Geographical setting of the study sites (diamonds) in the atolls of North Malé, South Malé, Felidhoo, Ari and Thoddoo in the Maldives.
Regional wind rose is also shown (based on data from Kench et al. 2006). Numbers refer to sites as in Table 1

either two or four depth transects, visualized by metric
lines laid on the bottom perpendicularly to the reef edge
(Bianchi et al. 2004; Colantoni 2007), were surveyed
between 4 and 18 m depth, for a total of 48 transects.
Benthic cover was visually estimated using the plan view
technique of Wilson et al. (2007) at depths of 4–6, 10–12, and
16–18 m. This technique, which involves a diver hovering
1–2 m above the bottom and estimating percentage amount
of substrate categories and benthos cover in a 5 m 9 5 m
area, has been shown to provide an accurate and precise
evaluation of coverage by benthic variables (Clua et al.
2006). Three geomorphological and biological descriptors
were considered (Fig. 2a–c): (1) living hard coral, (2) rubble
and sand, (3) coralline algae on rock. Three replicate esti-
mates were obtained for every transect at each depth.
Data analysis
Reef profiles (Figs. 3, 4) were plotted from the transect
data (either two or four transects, according to the site)

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4 Facies (2010) 56:1–11

Fig. 2 Geomorphological and

biological descriptors: a living
hard coral, b rubble and sand,
c coralline algae (amidst
encrusting corals) on rock (a, b
photo R. Lasagna, c photo
E. Giovannetti)

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Facies (2010) 56:1–11 5

Fig. 3 Depth profiles of outer Distance (m)

reef sites. The variability among 0 10 20 30 40 50 60 0 10 20 30 40 50 60
transects within each site is 0
represented by the grey area.
Numbers refer to sites as in 1 2
10
Table 1

20

3 4
10

20
Depth (m)

5 6
10

20

7 8
10

20

Fig. 4 Depth profiles of inner Distance (m)

reef sites. The variability among 0 10 20 30 40 50 60 0 10 20 30 40 50 60
transects within each site is 0
represented by the grey area.
Numbers refer to sites as in 9 10
10
Table 1

20

11 12
10
Depth (m)

20

13 14
10

20

15 16
10

20

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6 Facies (2010) 56:1–11

using AutoCAD software. In each of the 16 sites, the
measurement of the area between the profiles was used as
an estimation of variability among transects within sites. A
coefficient of variation (CV% = standard deviation/
mean 9 100) of each area was computed for each of the
two locations (outer and inner reef) in order to estimate
variability among sites within locations.
For each site, the mean profile was obtained averaging
the horizontal projections of the individual transects for
each depth. Agglomerative hierarchical cluster analysis
based on Euclidean distance and complete linkage was first
applied to the total matrix of the horizontal projections of
the mean profiles of each site in order to identify different
reefscapes. The same analysis, applied to the portions of
the original data matrix relative to each reefscape, allowed
to define distinct depth zones. Terminology of reefscapes
follows Arias-González et al. (2006) to describe spatially
discrete elements of morphological and biological structure
of a coral reef, as defined by clusters. Within each reef-
scape, depth zones were identified by clustering depths.
According to data provided by Kench et al. (2006), a
wind rose divided into octaves shows dominant wind
direction as NWW, SWW, and NEE (Fig. 1). Sites were
therefore classified, depending on their geographic posi-
tion, as sheltered, exposed, or very exposed, and subjected
to low, moderate, or high wave energy (Grigg 1998). Non-
parametric univariate Kruskal–Wallis one-way ANOVA on
ranks was used to test the null hypothesis of no differences
in wave energy among the studied reefscapes.
The dip angle and the roughness of each profile were
averaged over the reefscapes and reef depth zones. Dip
angle was measured in degrees, and roughness through an
index calculated with the formula:
dissimilarities and 4,999 random permutations, and con-
sidering ‘‘depth zone’’ as fixed factor (Anderson 2001b).
Results
Reef profiles
All the outer reef sites showed shallow terraces, 30–40 m
wide on the east side of the atolls (sites 1, 2, and 5 in
Table 1) and 5–20 m wide in the sea tract inside the double
atoll chain (3, 4, 6–8); variability among transects within
sites was generally low, except for at sites 6 and 8 (Fig. 3).
Inner reef sites showed no (10–13, 15, 16) or short (9 and
14) shallow terraces; variability among transects within
sites was frequently higher than in outer sites, especially at
site 9 (Fig. 4). Reef profile variability among sites within
locations was lower for outer reefs (CV = 35.8%) than for
inner ones (CV = 67.3%).
Reefscapes
Cluster analysis grouped sites into three distinct reefscapes
(Fig. 5). The first reefscape (A) included mostly outer reef
sites; the second reefscape (B) was represented essentially
by inner reef sites; finally, the third reefscape (C) was
comprised of both outer and inner reef sites. Kruskal–
Wallis one-way ANOVA showed a significant difference
(P \ 0.001) in wave energy, with A being mostly charac-
terized by moderate wave energy, B by low wave energy,
and C by high wave energy (Fig. 6).
120
Euclidean distance

100
RI ¼ 1  Lo =Lr
80
where Lo is the projected length and Lr is the measured 60
length of the transect line. The index ranges between 0 40
(minimum reef complexity) and 1 (maximum reef com- 20

plexity). Mann–Whitney U test was used to test the null 0

1 2 5 14 7 11 10 12 15 16 6 4 8 13 9 3
hypotheses of no differences for either reef dip or rough- A B C
ness values among reefscapes and depth zones.
In order to evaluate the ecological stage of reefscapes Fig. 5 The three reefscapes (A, B, and C) resulting from cluster
and depth zones, ternary diagrams representing the three analysis of horizontal projections of the mean profiles. Numbers refer
to sites as in Table 1
dominant categories of coral reef descriptors (living hard
corals; rubble and sand; coralline algae on rock) were
plotted. Ternary diagrams were similarly used by 3
Perry et al. (2008) to individuate carbonate production 2
N
states. 1
Differences in percentage amount of each descriptor 0
among depth zones within each reefscape were assessed L M H L M H L M H
A B C
through PERMANOVA, a non-parametric multivariate
one-way analysis of variance based on permutations Fig. 6 Number of sites (N) for each reefscape affected by low (L),
(Anderson 2001a). Data were analyzed using Bray–Curtis moderate (M), and high (H) wave energy

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Facies (2010) 56:1–11 7

Fig. 7 The two depth zones Reef flat 4 2 Reef flat 3

(reef flat and reef slope) 5 Reef flat 3 4
4 5
resulting from cluster analysis 6
5
of horizontal projections of the 7 6
6
8 7
mean profiles within each of the 7
8
three reefscapes (A, B, and C). 9 8
10 9 9
Numbers refer to depth in 10 10
11
meters 11 11
12
12 12
Reef slope 13 13
13 Reef slope
14 14
Reef slope 14
15 15 15
16 16 16
A B C
17 17 17
18 18 18
120 100 80 60 40 20 0 120 100 80 60 40 20 0 120 100 80 60 40 20 0
Euclidean distance

Depth zones a 50 ** ns **
40

Dip angle (°)

Analyzing the mean profiles of the sites included in the
three reefscapes separately made it possible to identify two 30

different depth zones (Fig. 7): the first between 2–4 and 6– 20
7 m depth, henceforth called ‘‘reef flat’’; the second 10
between 6–7 and 18 m, henceforth called ‘‘reef slope’’. A
0
minor discontinuity in the reef profiles was recognized in A B C
all the three reefscapes around 13 m depth. ***
ns
In reefscapes A and C, the difference in dip angle
*
between flat and slope was significant (U-test, P \ 0.01 in
b 0.6
both cases), whereas no difference (U-test, P [ 0.05) was
found in reefscape B (Fig. 8a). Overall reef dip angle was
0.4
different between reefscapes A and B (U-test, P \ 0.001) ** ** **
RI

and between A and C (U-test, P \ 0.05), but not between B

0.2
and C (U-test, P [ 0.05).
Roughness index increased significantly (U-test,
P \ 0.01) passing from flat to slope in all reefscapes 0.0
A B C
(Fig. 8b). Again, there was difference in roughness
**
between reefscapes A and B (U-test, P \ 0.01) and ns
between A and C (U-test, P \ 0.05), but no between B and *
C (U-test, P [ 0.05). Reef flat Reef slope

Ecological stages
Significant differences in percentage amount of geomor-
phological and biological descriptors between flat and
slope were found in all the three reefscapes (PERMANO-
VA, P \ 0.001 for reefscape A and P \ 0.01 for both B
and C).
All three of the ecological stages described by Pichon
(1974) were recognized in Maldivian reefs, together with
bare rock areas that were mostly interpreted as relict
structures (Fig. 9). Ecological stages were differently dis-
tributed among reefscapes and depth zones. In reefscape A,
the high amount of rubble and sand allowed to classify the
flat as in regressive stage, whereas higher hard coral cover
on the slope was taken as indicative of mature stage
prevalently. Reefscape B exhibited a flat frequently rich in
Fig. 8 Mean (?SE) dip angle (a) and roughness index RI (b) in the
three reefscapes (A, B, and C) and in the two depth zones (reef flat and
reef slope). nsP [ 0.05; *P \ 0.05; **P \ 0.01; ***P \ 0.001
corals, thus suggesting a young stage, and a slope with a
large amount of rubble and sand, interpreted as a regressive
stage. Finally, in reefscape C, rubble and sand were
abundant on the flat, living hard corals on the slope, which
were therefore classified as in regressive and young stages,
respectively (Fig. 10).
Discussion
The highest local morphological variability in the Maldives
was found in inner reefs where sand chutes, vertical walls,

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8 Facies (2010) 56:1–11

Fig. 9 Examples of the three reef ecological stages described in the text: a young, b mature, c regressive, and d of a relict structure (a photo
U. Cardini, b–d photo R. Lasagna)

Fig. 10 Ternary diagrams Hard Hard Hard

representing the dominant coral coral coral
geomorphological and
biological descriptors (living
hard coral, rubble and sand, A B C
coralline algae on rock) at the
16 reef sites in the two depth
zones (reef flat and reef slope)
for each reefscape (A, B, and C).
The two dashed lines within
each ternary diagrams separate
the three ecological stages Rubble Coralline Rubble Coralline Rubble Coralline
and sand algae and sand algae and sand algae

Reef flat Reef slope

inclined slopes, and rubble accumulations are known to be
frequent (Bianchi et al. 1997). Outer reefs showed larger
shallow terraces but less variable slopes. The reefscapes
recognized by cluster analysis were not in complete
agreement with the distinction between outer and inner
reefs. Although outer and inner reefs were expected to face
different conditions of wave energy, a major constraint for
the development of coral reefs (Done 1983; Grigg 1998;
Sheppard et al. 2005), the discontinuous rim of Maldivian
atolls (Ciarapica and Passeri 1993) prevents a clear dis-
tinction between outer and inner reefs: waves are able to
propagate through large and deep passes in the atoll rim,

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Facies (2010) 56:1–11
Fig. 11 A summarizing scheme of the ecological stages observed in
the three reefscapes (profiles) and the two depth zones (reef flat and
reef slope) studied, according to the relative intensity of wave energy
(see text for explanation)
entering the lagoon without substantial energy loss (Kench
et al. 2006).
The three reefscapes identified in the present study
correlated with exposure to wave energy, which is known
to act on a broad spatial scale but is able to generate
identifiable structures on a finer scale (Madin et al. 2006),
such as those reflected in the topographic features (i.e., reef
dip angle and roughness index) of individual sites. In all
the reefscapes there was a major break at around 6–7 m
depth, marking the edge of the reef flat, and a minor break
at around 13 m, due to notches and overhangs. These
findings are consistent with the features described at sim-
ilar depths by Bianchi et al. (1997). Based on the sea-level
curve proposed by Gischler et al. (2008) for the Maldives,
both breaks should have been produced during sea level
rise between 8 and 2 kyr BP. Perhaps not coincidentally,
major changes in quality and quantity of water movement
occur worldwide at similar depths (Riedl 1971), and are
mirrored in coral zonation (Done 1983).
In each of the three reefscapes, the ecological stage
(Pichon 1974) in the reef flat differed from that in the reef
slope (Fig. 11). Flat appeared in young stage where wave
energy was predominantly low and in regressive stage
where energy was moderate to high. Thus, wave energy in
the flat acts essentially as a disturbance for coral growth. In
the slope, the ecological stage appeared inversely related to
wave energy: ‘young’ if in presence of high energy,
‘mature’ with moderate energy, ‘regressive’ with low. On
the slope, therefore, wave energy may be favoring reef
vitality.
Conclusion
Taken as whole, a great number of the reefs studied were in
an ecological regressive stage, some were in the young
stage, and few in the mature one (Fig. 11). Rubble and sand
were widespread in all sites; coralline algae, which con-
tribute to their cementation (Rasser and Riegl 2002; Perry
9
and Hepburn 2008), were comparatively infrequent. Loose
detrital elements can either be produced within the reef or
imported (Perry et al. 2008): a great amount of rubble was
accumulated in place by the erosion of the colonies dead in
1998 (Schuhmacher et al. 2005; Bianchi et al. 2006a,
2006b), whereas the Sumatra-Andaman tsunami of
December 2004 drove sand, rubble, and detritus to reef
flats and slopes (Gischler and Kikinger 2006; Bianchi et al.
2009). Whatever the origin, the amount of loose sediment
was higher than reported in earlier years by Scheer (1971).
The roughness of the reef uppermost veneer, and hence the
3D-structure of the coral community, was low in all reef-
scapes and depth zones, in spite of a tremendous increase
in hard coral cover (Lasagna et al. 2008) if compared to the
values observed shortly after the 1998 coral mass mortality
episode (McClanahan 2000; Zahir 2000; Loch et al. 2002;
Schuhmacher et al. 2005). However, if compared with pre-
mortality values, coral cover is still low (Bianchi et al.
2006b; Lasagna et al. 2008). Recovery of Maldivian reefs
might thus appear lower than that of other Indian Ocean
reefs hit by the mass mortality event of 1998 (McClanahan
et al. 2007; Burt et al. 2008; Sheppard et al. 2008; Smith
et al. 2008). Decreased coral cover may shift the balance
between reef accretion and erosion (Sheppard et al. 2002)
and eventually lead, as suggested by Ciarapica and Passeri
(1993), to platform drowning. However, the fact that reef
communities are in a regressive ecological stage does not
necessarily imply a concern about the maintenance of the
reefs themselves (Hopley et al. 2007). Some of the
Maldivian reef communities were shown to be in a young
ecological stage, thus suggesting potentiality for future
recovery. It is obviously impossible to foresee if coral
cover will keep on increasing to reach again the pre-
bleaching values: nevertheless, coupling geomorphological
and biological descriptors to define ecological stages might
represent a useful tool to track future reef evolution.
Acknowledgments Albatros Top Boat (Verbania and Malé) orga-
nized our scientific cruise in the Maldives: we would especially like to
thank Donatella ‘Dodi’ Telli and Massimo Sandrini for their support.
Isotta Gattorna, Elisa Giovannetti, Matia Grondona, Ambra Milani,
and Romina Rivella (Genoa) participated in some field activities and
Elisa Giovannetti and Ulisse Cardini also kindly provided photo-
graphs. Thanks are also due to an anonymous referee whose com-
ments greatly improved the paper.
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